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European Journal of Physical and Rehabilitation Medicine

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Prognostic value of balance performance for improvements


of community ambulation among stroke patients: a cohort
study.
Francesc MEDINA-MIRAPEIX, Mª José CRISOSTOMO, Rodrigo MARTíN-SAN
AGUSTíN, Mª Piedad SáNCHEZ-MARTíNEZ

European Journal of Physical and Rehabilitation Medicine 2021 Sep 09


DOI: 10.23736/S1973-9087.21.06996-3

Article type: Original Article

© 2021 EDIZIONI MINERVA MEDICA

Article first published online: September 9, 2021


Manuscript accepted: August 31, 2021
Manuscript revised: July 20, 2021
Manuscript received: April 8, 2021

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Title: Prognostic value of balance performance for improvements of community


ambulation among stroke patients: a cohort study.

Running title: Prognostic value of balance performance

Francesc Medina-Mirapeix1, Mª José Crisostomo2, Rodrigo Martín San Agustín3*,


Mª Piedad Sánchez-Martínez1.
1
Department of Physical Therapy, University of Murcia, 30100 Murcia, Spain;
mirapeix@um.es; mariapiedad.sanchez1@um.es
2
Department of Rehabilitation, Jerez Hospital, Jerez de la Frontera, Spain;
mjcriso@gmail.com
3
Department of Physical Therapy, University of Valencia, 46010 Valencia, Spain;
rodrigo.martin@uv.es

* Corresponding author: Rodrigo Martín-San Agustín, Department of Physiotherapy,


Calle Gascó Oliag, 5. PC: 46010, Valencia (Spain). E-mail: rodrigo.martin@uv.es Tel.
+34 963 983 853 Fax +34 963 983 852

ABSTRACT

BACKGROUND: Despite the positive impact of improving the level of community

ambulation among stroke patients, little prognostic research has focused on this indicator.

AIM: To investigate the prognostic value of the side-by-side, semi-tandem, and tandem

standing balance positions and the five-sit-stand (5STS) test for discriminating patients

undergoing physical rehabilitation who improve level of functional ambulation and

predicting transition time.

DESIGN: A cohort study with assessments repeated monthly until discharge for classifying

patients in a community ambulation class.

SETTING: A neurological rehabilitation unit of a hospital in Spain.

POPULATION: A consecutive sample of 109 stroke patients (68.5 ±12.0 years) was

screened and included within four months post stroke. Of them no one refused, 3 died, and

5 were lost earlier to transition or discharge.

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METHODS: Balance tests, the 5STS and gait speed were measured at the center at baseline

and monthly until discharge. Transition from household or limited community ambulation

to a higher ambulatory capacity or class. Area under the curve (AUC) were used to compare

discriminative abilities of the tests and Cox regression analysis to evaluate the association

between the tests and time of transition.

RESULTS: For household non-ambulators, the semi-tandem was the best discriminative

test (AUC=0.850) and the three balance tests showed an association with time to transition.

Among the limited community ambulators, the 5STS test also revealed discriminative

ability (AUC: 0.822 [0.63-1.00]), with a good prognostic cut-off (14.8 seconds) and

association with time to transition (Hazard Ratio: 1.22; 95%CI: 1.05-1.43).

CONCLUSIONS: Semi-tandem and the 5STS tests can discriminate patients who improve

level of functional ambulation and predict transition times within three months in non-

ambulators and limited community ambulation patients, respectively.

CLINICAL REHABILITATION IMPACT: The semi-tandem and the 5STS tests can be

performed easily in clinical settings to predict improvement of functional ambulation level

in patients following stroke.

Key Words: Postural Balance; Stroke Rehabilitation; Walking; Transitions.

Introduction
For rehabilitation professionals and stroke patients undergoing physical rehabilitation, the

restoration of community ambulation is the most important goal.1,2 In spite of efforts, many

patients who are classified as non-ambulators, household ambulators (<0.4 m/s) or limited

community ambulators (between 0.4 and 0.8 m/s) at the beginning of physical rehabilitation

are not able to be full community ambulators (>0.8 m/s) again.1,3–5 Nevertheless, some

studies reported that about half of these patients improved to a higher level of ambulation

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within three months (e.g., from household ambulation to limited community ambulation),

and that transitioning was associated with substantially better function and quality of life.5

Despite the positive impact of improving the level of community ambulation among stroke

patients, little is known about transition rates that take place later than three months in

physical rehabilitation. Often more attention is paid to known rates of other indicators of

gait recovery such as gait speed, walking distance or asymmetrical gait parameters.1,6–11

Likewise, prognostic research has also focused on these gait recovery indicators,12–16 for

identifying prognostic factors such as balance12,13 and muscle strength of lower

extremities,14 regardless of age12 and the initial gait speed.5,13,15 Nevertheless, there is still

no confirmation as to whether these factors also have value for transition to a higher class

of ambulation. This paper wanted to test prognostic ability of the five-sit-to-stand (5STS)

test and the three balance tests included in the Short Physical Performance Battery (SPPB).17

We selected the 5STS because it evaluates a functional task that requires both lower limb

strength and efficient balance control.18–21 We deemed those three isolated balance tests

because multi-item scales (eg. Berg balance scale) have floor effects among household

ambulators.22

The main aim of this study was to investigate the prognostic value of three isolated standing

balance positions17 and the 5STS test for discriminating patients undergoing physical

rehabilitation who improve level of functional ambulation and predicting transition time. A

secondary aim was to determine transition rates over time beyond three months. We

hypothesized that (1) the prognostic value of these tests would differ according to the

baseline level of community ambulation; (2) within each baseline ambulation class, patients

with good balance performance will transition faster than patients with poor balance

performance.

Materials and methods

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Study design
A cohort study was conducted including patients with a first episode of stroke admitted to

the Rehabilitation Service of the Jerez Hospital (Spain) between October 2016 and October

2018 to participate in a physical rehabilitation after receiving acute stroke care at that

hospital or nearby. Assessments were made within two days of admission and repeated

monthly until the patient transitioned to the level of full community ambulation or

discharge. The study protocol was approved by the Ethical Committee of the Jerez Hospital

(approval number: EST-42/16).

Participants
Participants were prospectively recruited and screened. The inclusion criteria included:

patients who (1) were at least 30 years, (2) and were screened within four months post

stroke. The following exclusion criteria were applied: patients who were full community

ambulators at baseline (>0.8 m/s), those who remembered having a gait speed lower than

0.8 m/s (e.g., more than 8 s for 10 m) during the month before the stroke, or subjects who

displayed cognitive or language impairments (in the subscales of the Cognistat).23 The first

exclusion criterion was established because no transitioning would be possible. The pre-

stroke gait speed criterion was established to avoid the possibility of limited recovery of

ambulation due to a poor ambulation status or additional neurological impairments prior to

the stroke. The cognitive and language criteria were based on the need to ensure that patients

could provide reasonable answers. All study patients provided written informed consent.

Outcome measure
The primary outcome measurement used was the first improvement transition, without

relapse before discharge, to a higher class of ambulation in the Perry’s classification, which

established three categories: household ambulators (<0.4 m/s), limited community

ambulators (between >0.4 m/s and <0.8 m/s) and full community ambulators (>0.8m/s).3

Transition (yes/no) was defined when participants shifted from household to limited

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community, and from limited ambulation to full community ambulation. Time (months)

from the beginning of physical rehabilitation to transition was also recorded. We canceled

transitions with relapse, i.e., when they were followed by a transition to a lower class before

discharge.

Tests and other characteristics


Balance tests, the 5STS and gait speed were measured at the center at baseline and monthly

until discharge. In addition, at baseline, five characteristics (age, sex, type of the stroke, side

affected and time from stroke to admission) were collected from medical records in order

to describe participants. Moreover, because age and time from stroke have been associated

with gait speed,12–14 they were also used to control the association of the examined tests

with the time to transitioning.

The balance tests included different standing positions. Standing positions were evaluated

in three progressively more difficult stances regarding the SPPB: (a) feet side-by-side,

touching; (b) semi-tandem, the side of the heel of one foot touching the big toe of the other

foot; and (c) tandem, the heel of one foot directly in front of and touching the toes of the

other foot. If the participant held a stance for 10 seconds, he/she was asked to try the next

more difficult position.17,24

The 5STS test was measured as the time taken to complete 5 repetitions of the sit-to-stand

task. All sit-to-stand tasks were performed from a chair without an arm rest.18 Participants

unable to complete five repetitions within 1 min were given a score of 60 s, as in previous

research.25

Gait velocity was assessed with a 4-m gait speed test and reported in m/s. Subjects were

asked to complete the 4-m walk at their ‘‘most comfortable speed’’,26 and a stopwatch

recorded the time. Timing began after an acceleration distance of 1m and ceased as they

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crossed a finish line. Subjects performed two trials, and the faster time was recorded.27

Patients unable to walk were classified as household non-ambulators.

Statistical analysis
Participants’ characteristics at admission were summarized for the whole sample and by

each level of community ambulation. In total, three groups were established: household

ambulator, non-ambulators and limited community ambulators (Table 1). Chi-square and

ANOVA tests were used to compare baseline characteristics between these three groups.

The percentages of transitioning of these three groups to a higher ambulation class, and time

to transitioning was described by Kaplan-Meier survival curves and compared by the log

rank test.

Subsequently, we tested the prognostic value of the examined tests in each group (household

ambulator, non-ambulators and limited community ambulators). First, the area under the

ROC curve (AUC) and predictive likelihood ratios (LRs) were used to assess the ability of

balance tests and 5STS to discriminate individual participant’s transition to a higher

ambulation class at two points in time: at three months and at discharge.28 The AUCs were

compared by DeLong’s test. The LRs were based on the optimal cut-off point of the ROC

curve, which was identified by the maximal Youden Index calculated as (sensitivity +

specificity - 1) and compared. Second, multivariate Cox regression analysis adjusted by the

selected covariates (age and time since stroke) were performed to estimate the hazard ratios

(HRs) and 95% confidence intervals (CIs) of the balance tests and 5STS for each level of

community ambulation.

Finally, for those groups with a discriminative test (AUC>0.8), we also calculated Kaplan-

Meier survival curves and compared with the log rank test whether patients with high

balance performance (defined by the optimal cut-off point identified previously)

transitioned faster than patients with poor balance performance. All analyses were

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performed using the Statistical Package for the Social Sciences (SPSS) version 24.0 (IBM

SPSS, Chicago, IL, USA). A two-sided P<0.05 was considered significant.

Results
Patient characteristics
In total, 123 stroke patients were screened for inclusion. Figure 1 shows the reasons for

exclusion of 14 patients. Table 1 summarizes relevant patient characteristics and baseline

balance measurements of the 109 patients according to ambulation class. The mean age was

68.5 (SD=12.0), 55% of the subjects were male and 83.5% had an ischemic stroke. The

mean time since stroke onset was 52.1 days (SD=31.4). Only a percentage of patients were

able to complete the balance tests (range 70.7% for side-by-side to 40.4% for tandem stand)

and/or the 5STS test (46.8%).

Figure 1.⎯ Flowchart of patients who met inclusion/exclusion criteria for the study
population.
Table I.⎯ Baseline demographics and overall stroke patient characteristics in total and separated by level
of community ambulation.
Level of community ambulation
Household Limited
All Community P-
Variable
(n=109) Non- (n=32) Value
Ambulators
ambulators
(n=33)
(n=44)
Demographics
Age, y 68,5(12,0) 69,45(12,3) 71,0(10,7) 64,6(12,2) 0,079
Male, n(%) 60(55) 24(54,5) 16(48,5) 20(62,5) 0,523
Stroke characteristics
Side affected (right), n(%) 57(52,3) 27(61,4) 12(36,4) 18(56,3) 0,082
Type of stroke (ischemic), n(%) 91(83,5) 37(84,1) 27(81,8) 27(84,4) 0,953
Time from stroke to admission, 52,1(31,4) 50,8(31,5) 56,0(32,7) 50,0(30,6) 0,709
days
Standing balance tests
Side-by-side position
Patients able to stand ≥1s, n(%) 77(70,7) 13(29,5) 32(97) 32(100) <0.001
time (s) 6,86(4,55) 2,75(4,39) 9,3(2,15) 10,0(0) <0.001
Semi-tandem position
Patients able to stand ≥1s, n(%) 69(63,3) 9(20,5) 29(87,9) 31(98,9) <0.001
time (s) 5,83(4,73) 1,57(3,42) 7,9(3,63) 9,56(1,88) <0.001

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Tandem position
Patients able to stand ≥1s, n(%) 44(40,4) 2(4,6) 14(42,4) 28(87,5) <0.001
time (s) 3,2(4,38) 0,40(1,89) 3,39(4,38) 6,85(4,16) <0.001
5STS
Patients able to do it, n(%) 51(46,8) 4(9,1) 18(54,5) 29(90,6) <0.001
time (s) 40,34(21,63) 56,65(10,77) 39,19(20,35) 19,11(14,06) <0.001
Gait speed, m/s 0,31(0,2) 0(0) 0,29(0,06) 0,59(0,12) <0.001
5STS indicates five-repetition sit-to-stand. Values are mean (SD) where appropriate.

A total of 44 (40.36%) patients were classified as household non-ambulators, and 32 of the

65 ambulators were limited community ambulators. These patient groups did not display

significant differences in demographic and clinical characteristics, although they did present

significant differences in their assessments. For the four examined tests, the three groups

showed significant differences regarding both mean time (P-values <0.001) and number of

patients able to do them (P-values <0.001).

Of the 109 patients who were enrolled at admission, 55 (50.5%) transitioned to a higher

ambulation class before discharge, and 8 (7.4%) dropped out earlier (7 dropped out in the

first three months). The demographic and stroke baseline characteristics of these 8 patients

did not significantly differ from the 101 patients who continued throughout the study until

discharge (P-value ranged between 0.208 and 0.814).

Transition rates in patients of each ambulation class


The Kaplan-Meier plot (Figure 2) shows that the level of community ambulation was

associated with a reduction of transition time (X2[2]=28.92 log rank; P<0.001). The

cumulative percentage of transitions in household non-ambulators increased more slowly

over time, and their rates of transitioning at three months and at discharge were 26.1% and

45.1%, respectively. Among ambulators the cumulative percentage of transitions for

household ambulators increased slightly faster than limited community ambulators upon the

three months, and this percentage was also higher for household patients at this time (85.3%

and 63.2%, respectively).

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Figure 2.⎯ Cumulative percentage of transitioning to a higher ambulation class by months:


household non-ambulators (dashed line), household ambulators (solid line) and limited community
ambulators (dotted line).

Prognostic value of the tests in patients of each ambulation class


Table 2 shows AUCs and cut-off values of balance tests and the 5STS for discriminating

transitions at three months and at discharge. For household non-ambulators, side-by-side

standing and semi-tandem standing positions showed discriminative ability (AUCs>0.7) for

the ability to transition at these two time-points, however the semi-tandem position showed

better AUCs. The optimal cut-off points of this test (stand for 1s), which was the same at

three months and at discharge, also provided more positive LRs than the cut-off points of

the side-by-side standing position for transitioning at these two points in time (7.46 vs. 5.71

at discharge; >10 vs. 4.67 at three months). For household ambulators, all tests showed

AUCs<0.7 (values not showed in table 3). In contrast, for limited community ambulators

the 5STS test showed AUCs>0.8 at three months and again at discharge. The cut-off rates

for the 5-STS test (14.8s) were the same at two points in time, because they had similar

rates.

Table II.⎯Areas under curve (AUC) and cut-off values of standing balance tests and the 5STS for discriminating transitioning at
3-months and at discharge, and their statistics indicators.
Baseline
ambulation Time Tests AUC* 95% CI Cut-off Sensitivity Specificity LR + 1/LR-
class
Side-by-side position(s) 0,779 0,54-1,00 5 0,70 0,85 4,67 2,84
At 3-months Semi-tandem position(s) 0,850 0,66-1,00 1 0,70 1,00 >10 3,33
Household Tandem position(s) 0,600 0,32-0,87 3,9 0,20 1,00 >10 1,25
non-
ambulators Side-by-side position(s) 0,721 0,54-0,89 8,5 0,57 0,9 5,71 2,12
At discharge Semi-tandem position(s) 0,726 0,54-0,90 1 0,50 0,93 7,46 1,88
Tandem position(s) 0,571 0,38-0,76 3,9 0,14 1,00 >10 1,16
Limited At 3-months 5STS (s) 0,822 0,63-1,00 14,8 0,78 0,80 3,90 3,63
community
ambulators At discharge 5STS (s) 0,857 0,71-1,00 14,8 0,78 0,86 5,44 4,00

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AUC indicates area under the curve; CI, confidence interval; LR, likelihood ratio; 5STS: five-repetition sit-to-stand.
*Only tests con AUC>0.55 are shown (Tests for household ambulators are not shown because this reason).

Figure 3 shows a forest plot of the HRs and their 95%CI -adjusted by age and time since

stroke- of the balance tests and 5STS with time to transitioning in participants of each

ambulation class. For household non-ambulator patients, the three standing balance

positions revealed lower limits of 95%CI of their HRs higher than 1 (P<0.05) and were

associated to transitioning to a higher class of ambulation. The 5STS test was not associated

with time to transitioning in this group. In contrast, the 5STS test was associated with limited

community ambulators (HR: 1.22; 95%CI: 1.05-1.43), although the standing balance

positions did not. None of the four tests showed an association with transition time among

household ambulators.

Figure 3 .⎯ Hazard ratios (and 95%CI) of the standing balance tests and the 5STS with
time to transitioning according to ambulation class at baseline (adjusted by age and time
since stroke). *HRs could not be calculated because all patients did the test.

Rates of improvement in patients with good and poor balance performance


Figure 4a shows how those household non-ambulators able to stand >1s in semi-tandem

positions (the best discriminative test) transitioned to a higher ambulation class at a

significantly faster rate compared to these unable to perform this test (X2(1)=15.75 log rank;

P<0.001). At three months patients with a better performance in this test had higher rates of

improvements than patients with poor performance (77.8% vs 26.1%). Figure 4b shows how

limited community ambulators who were able to complete the 5STS test <14.8s required

significantly less time to transition to full community ambulators than those unable to do so

(X2(1)=15.98 log rank; P<0.001).

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Figure 4 .⎯ Cumulative percentage of transitioning to a higher ambulation class by months:


4a) household non-ambulators patients able (solid line) or not (dotted line) to standing in
the semi-tandem position ≥1s; 4b) limited community patients able (solid line) or not (dotted
line) to complete the 5STS in ≤14.8 s.

Discussion
We found that many patients from the household ambulators and limited community class

transitioned at around three months after admission to the physical rehabilitation, however,

only a quarter of household non-ambulators transitioned at that time. After three months,

only household non-ambulators increased their transition rates. For these patients, the semi-

tandem was the best test for discriminating patients who improve level of functional

ambulation at three months and again at discharge, but all standing balance tests showed an

association with transition time. The 5STS test also had good these discriminative and

predictive properties among limited community ambulators.

Balance, age and days since stroke onset were previously reported as key determinants of

certain gait recovery indicators after stroke.13,19,29–33 Our study confirmed that these factors

are also determinants for discriminative and predictive purposes with transitions of

functional ambulation. On the one hand, we found that by using a cut-off point in side-by-

side and semi-tandem stance positions it is possible to discriminate between household non-

ambulators who are able to transition at three months and at the discharge and those who

fail to transition. Our indicators of sensitivity and specificity at three months were similar

or higher than those reported for the Berg balance scale for discriminating non-ambulator

stroke patients who achieved unassisted walking.24,29

As expected, our study also found that the 5STS test was not relevant for household

ambulators and non-ambulators because many of these patients were not able to perform

the test on admission. In contrast, as expected, the 5STS had a greater discriminative

capacity among the limited community ambulators. To our knowledge, this is the first study

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that shows the discriminative value of the 5STS on the appearance of certain events over

time for stroke patients. Previous studies have only reported the cross-sectional ability for

discriminating patients with differing ambulatory capacity (e.g., discriminating limited or

full community ambulators), with similar values of sensitivity and specificity to our study.19

Another novelty of our study is that we found that the 5STS in the case of limited community

ambulators had a prognostic value for achieving earlier transitioning to a higher ambulation

class.

At three months, we found higher cumulative percentages of transitions to a higher

ambulation class for household ambulators and limited community ambulators compared to

those previously reported by Schmid et al.5 Beyond three months, our study showed that

hardly any transitions took place among both household ambulators and limited community

ambulators. Our results are consistent with previous studies that reported that the maximum

walking improvement after a stroke is achieved during the first three months.1,6,7

Previous studies showed that a quarter of non-ambulators can achieve unassisted walking at

three months.24,29,30 Because unassisted walking is theoretically a less difficult task for non-

ambulator stroke patients than transitioning to the limited community ambulation category,

we expected the cumulative percentage of transitions at three months to be lower than 25%.

Surprisingly, our study showed that a quarter of those patients were able to transition at

three months.

Implications for practice and research


Previous literature has reported that gait speed can continue to improve over the first six

months when undergoing a physical rehabilitation.6,30 In spite of this overall evidence, our

results added that it is unexpected for household ambulators and limited community patients

to attain a higher level of ambulation beyond the first three months.

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Furthermore, our findings reveal that the side-by-side and semi-tandem stance positions,

and the 5STS had prognostic value for household non-ambulators and limited community

ambulators, respectively. This supports the use of these tests. They are also very useful when

time and space is limited in clinical settings as they can be performed rapidly. Given the

prognostic relevance of these tests, future research is necessary to analyze whether they

could be incorporated into predictive models.

Strengths and limitations


This study has several strengths. First, we explored the prognostic value of multiple tests on

three groups with differing ambulatory abilities. One of the positive consequences of this

design was that it enabled us to observe how the tests had different prognostic values for

each group, which, to our knowledge is a novel finding to date. Second, we used different

indicators to analyze the discriminative ability of tests (AUCs, sensitivity, specificity and

positive and negative LRs).

This study also has some limitations. First, as our study was developed at a single hospital
and included a small number of patients, generalizations should be made with caution.
Second, we imputed times for patients who failed to complete the 5STS. Thus, we did not
compare unable vs. able to complete the 5STS. Third, other measures that may impact
improvement during rehabilitation and overall walking function were not included as
covariates. For example, lower extremity impairment (somatosensorial, spasticity) was not
specifically measured yet may impact balance and walking ability.29 Finally, the lack of a
validation of our results in other independent sample of stroke patients and/or with another
additional method for measuring gait speed. While other researchers used the 10 m walking
test timed with a stopwatch for analyzing transition to a higher class of ambulation,5 we
used the 4-m gait speed test. Until that validation, our results should be considered
provisional. Given our current good results and the reasons for our test selection, we would
expect that new studies will provide validity and enough adequacy of the 4-m gait speed
test to sub-acute patients. On the one hand, we selected this test because shorter distances
(e.g., 5m) are more recommended to detect longitudinal change over time than longer
distances (e.g., 10m) in sub-acute stroke patients,34 which were our study aim and study

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population, respectively. Reasons for a lower responsiveness of the 10m walking test may
be due to the fact that some of these patients were unable to maintain speed over those
distances because of reduced active movement or muscular endurance.34 On the other hand,
instead of the frequently used 5-m gait speed test,27,34 the 4-m test was chosen because it is
a component of the SPPB, which includes the balance test and the 5-STS test as components
as well.17
Conclusions
In summary, only a few of the household non-ambulators transitioned beyond the three

months. Semi-tandem and the 5STS tests can discriminate patients who improve level of

functional ambulation and predict transition times within three months in non-ambulators

and limited community ambulation patients, respectively. However, further studies are

required to determine the prognostic value of these tests for household ambulators.

REFERENCES

1. Lord SE, McPherson K, McNaughton HK, Rochester L, Weatherall M. Community ambulation


after stroke: how important and obtainable is it and what measures appear predictive? Arch Phys
Med Rehabil. 2004;85:234–9.
2. Bohannon RW, Horton MG, Wikholm JB. Importance of four variables of walking to patients
with stroke. Int J Rehabil Res. 1991;14:246–50.
3. Perry J, Garrett M, Gronley JK, Mulroy SJ. Classification of Walking Handicap in the Stroke
Population. Stroke. 1995;26:982–9.
4. Viosca E, Lafuente R, Martínez JL, Almagro PL, Gracia A, González C. Walking recovery after
an acute stroke: assessment with a new functional classification and the Barthel Index. Arch Phys
Med Rehabil. 2005;86:1239–44.
5. Schmid A, Duncan PW, Studenski S, Lai SM, Richards L, Perera S, et al. Improvements in speed-
based gait classifications are meaningful. Stroke. 2007;38:2096–100.
6. Jørgensen HS, Nakayama H, Raaschou HO, Vive-Larsen J, Støier M, Olsen TS. Outcome and
time course of recovery in stroke. Part II: Time course of recovery. The Copenhagen Stroke Study.
Arch Phys Med Rehabil. 1995;76:406–12.
7. Buvarp D, Rafsten L, Sunnerhagen KS. Predicting Longitudinal Progression in Functional
Mobility After Stroke: A Prospective Cohort Study. Stroke. 2020;51:2179–87.

This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one
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the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other means which may allow access to the Article. The use of all or any
part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is not
permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to
frame or use framing techniques to enclose any trademark, logo, or other proprietary information of the Publisher.
COPYRIGHT© EDIZIONI MINERVA MEDICA

8. Patterson KK, Mansfield A, Biasin L, Brunton K, Inness EL, McIlroy WE. Longitudinal changes
in poststroke spatiotemporal gait asymmetry over inpatient rehabilitation. Neurorehabil Neural
Repair. 2015;29:153–62.
9. Duncan P, Studenski S, Richards L, Gollub S, Lai SM, Reker D, et al. Randomized clinical trial
of therapeutic exercise in subacute stroke. Stroke. 2003;34:2173–80.
10. da Cunha IT, Lim PA, Qureshy H, Henson H, Monga T, Protas EJ. Gait outcomes after acute
stroke rehabilitation with supported treadmill ambulation training: a randomized controlled pilot
study. Arch Phys Med Rehabil. 2002;83:1258–65.
11. Green J, Forster A, Young J. Reliability of gait speed measured by a timed walking test in
patients one year after stroke. Clin Rehabil. 2002;16:306–14.
12. Kollen B, Kwakkel G, Lindeman E. Longitudinal robustness of variables predicting independent
gait following severe middle cerebral artery stroke: a prospective cohort study. Clin Rehabil.
2006;20:262–8.
13. Bland MD, Sturmoski A, Whitson M, Connor LT, Fucetola R, Huskey T, et al. Prediction of
Discharge Walking Ability From Initial Assessment in a Stroke Inpatient Rehabilitation Facility
Population. Arch Phys Med Rehabil. 2012;93:1441–7.
14. Kluding P, Gajewski B. Lower-extremity strength differences predict activity limitations in
people with chronic stroke. Phys Ther. 2009;89:73–81.
15. Goldie PA, Matyas TA, Kinsella GJ, Galea MP, Evans OM, Bach TM. Prediction of gait velocity
in ambulatory stroke patients during rehabilitation. Arch Phys Med Rehabil. 1999;80:415–20.
16. Kuys SS, Bew PG, Lynch MR, Morrison G, Brauer SG. Measures of activity limitation on
admission to rehabilitation after stroke predict walking speed at discharge: an observational study.
Aust J Physiother. 2009;55:265–8.
17. Rantanen T, Guralnik JM, Ferrucci L, Leveille S, Fried LP. Coimpairments: strength and balance
as predictors of severe walking disability. J Gerontol A Biol Sci Med Sci. 1999;54:M172-176.
18. Mentiplay BF, Clark RA, Bower KJ, Williams G, Pua Y-H. Five times sit-to-stand following
stroke: Relationship with strength and balance. Gait & Posture. 2020;78:35–9.
19. Lee G, An S, Lee Y, Park D-S. Clinical measures as valid predictors and discriminators of the
level of community ambulation of hemiparetic stroke survivors. J Phys Ther Sci. 2016;28:2184–9.
20. Schenkman M, Hughes MA, Samsa G, Studenski S. The relative importance of strength and
balance in chair rise by functionally impaired older individuals. J Am Geriatr Soc. 1996;44:1441-6.
21. Ng S. Balance ability, not muscle strength and exercise endurance, determines the performance
of hemiparetic subjects on the timed-sit-to-stand test. Am J Phys Med Rehabil. 2010;89:497–504.
22. Blum L, Korner-Bitensky N. Usefulness of the Berg Balance Scale in stroke rehabilitation: a
systematic review. Phys Ther. 2008;88:559–66.

This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one
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COPYRIGHT© EDIZIONI MINERVA MEDICA

23. Fulk GD, Ludwig M, Dunning K, Golden S, Boyne P, West T. Estimating clinically important
change in gait speed in people with stroke undergoing outpatient rehabilitation. J Neurol Phys Ther.
2011;35:82–9.
24. Louie DR, Eng JJ. Berg Balance Scale score at admission can predict walking suitable for
community ambulation at discharge from inpatient stroke rehabilitation. J Rehabil Med.
2018;50:37–44.
25. Jones SE, Kon SSC, Canavan JL, Patel MS, Clark AL, Nolan CM, et al. The five-repetition sit-
to-stand test as a functional outcome measure in COPD. Thorax. 2013;68:1015–20.
26. Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF, Blazer DG, et al. A short
physical performance battery assessing lower extremity function: association with self-reported
disability and prediction of mortality and nursing home admission. J Gerontol. 1994;49:M85-94.
27. van Bloemendaal M, van de Water ATM, van de Port IGL. Walking tests for stroke survivors: a
systematic review of their measurement properties. Disabil Rehabil. 2012;34:2207–21.
28. Herbert RD. Cohort studies of aetiology and prognosis: they’re different. J Physiother.
2014;60:241–4.
29. Makizako H, Kabe N, Takano A, Isobe K. Use of the Berg Balance Scale to predict independent
gait after stroke: a study of an inpatient population in Japan. PM R. 2015;7:392–9.
30. Kollen B, van de Port I, Lindeman E, Twisk J, Kwakkel G. Predicting improvement in gait after
stroke: a longitudinal prospective study. Stroke. 2005;36:2676–80.
31. Kwakkel G, Kollen B, Twisk J. Impact of time on improvement of outcome after stroke. Stroke.
2006;37:2348–53.
32. Tsang YL, Mak MK. Sit-and-reach test can predict mobility of patients recovering from acute
stroke. Arch Phys Med Rehabil. 2004;85:94–8.
33. Park C, Son H, Yeo B. The effects of lower extremity cross-training on gait and balance in stroke
patients: a double-blinded randomized controlled trial. Eur J Phys Rehabil Med. 2021 Feb;57(1):4-
12.
34. Salbach NM, Mayo NE, Higgins J, Ahmed S, Finch LE, Richards CL. Responsiveness and
predictability of gait speed and other disability measures in acute stroke. Arch Phys Med Rehabil
2001;82:1204–1212

Conflicts of interest.⎯ The authors certify that there is no conflict of interest with any
financial organization regarding the material discussed in the manuscript.

Funding.⎯ The authors report no involvement in the research by the sponsor that could
have influenced the outcome of this work.

Authors’ contributions.⎯ Author F.M.-M. and author M.J.C have given substantial
contributions to the conception or the design of the manuscript, author M.P.S.M and author

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R.M.-S to acquisition, analysis and interpretation of the data. All authors have participated
to drafting the manuscript, author F.M.-M. revised it critically. All authors read and
approved the final version of the manuscript.

Acknowledgements.⎯ The authors acknowledge the neurology team of the Rehabilitation


Service of the Jerez Hospital for proofreading activity.

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