Effects of stretching exercises on human gait: a systematic review and meta-analysis

Thomas Vialleron; Arnaud Delafontaine; Sebastien Ditcharles; Paul Fourcade; Eric Yiou

doi:10.12688/f1000research.25570.2

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Systematic Review

Revised

Effects of stretching exercises on human gait: a systematic review and meta-analysis

[version 2; peer review: 2 approved, 1 approved with reservations]

Thomas Vialleron^1,2, Arnaud Delafontaine ^1,2, Sebastien Ditcharles^1-3, Paul Fourcade^1,2, Eric Yiou^1,2

Thomas Vialleron^1,2, Arnaud Delafontaine ^1,2, [...] Sebastien Ditcharles^1-3, Paul Fourcade^1,2, Eric Yiou^1,2

PUBLISHED 30 Oct 2020

Author details Author details

¹ CIAMS, Univ. Paris-Sud., Université Paris-Saclay, Orsay, 91405, France
² CIAMS, Université d'Orléans, Orléans, Orléans, 45067, France
³ ENKRE, Saint Maurice, Ile de France, 94410, France

Thomas Vialleron
Roles: Conceptualization, Methodology, Writing – Original Draft Preparation

Arnaud Delafontaine
Roles: Conceptualization, Methodology, Writing – Original Draft Preparation

Sebastien Ditcharles
Roles: Writing – Review & Editing

Paul Fourcade
Roles: Writing – Review & Editing

Eric Yiou
Roles: Supervision, Writing – Review & Editing

OPEN PEER REVIEW

REVIEWER STATUS

Abstract

Background: Stretching is commonly used in physical therapy as a rehabilitation tool to improve range of motion and motor function. However, is stretching an efficient method to improve gait, and if so, for which patient category?
Methods: A systematic review of randomized and non-randomized controlled trials with meta-analysis was conducted using relevant databases. Every patient category and every type of stretching programs were included without multicomponent programs. Data were meta-analysed where possible. Estimates of effect sizes (reported as standard mean difference (SMD)) with their respective 95% confidence interval (95% CI) were reported for each outcome. The PEDro scale was used for the quality assessment.
Results: Twelve studies were included in the analysis. Stretching improved gait performance as assessed by walking speed and stride length only in a study with a frail elderly population, with small effect sizes (both SMD= 0.49; 95% CI: 0.03, 0.96; PEDro score: 3/10). The total distance and the continuous walking distance of the six-minute walking test were also improved only in a study in an elderly population who had symptomatic peripheral artery disease, with large effect sizes (SMD= 1.56; 95% CI: 0.66, 2.45 and SMD= 3.05; 95% CI: 1.86, 4.23, respectively; PEDro score: 5/10). The results were conflicting in healthy older adults or no benefit was found for most of the performance, spatiotemporal, kinetic and angular related variables. Only one study (PEDro score: 6/10) showed improvements in stance phase duration (SMD=-1.92; 95% CI: -3.04, -0.81), swing phase duration (SMD=1.92; 95 CI: 0.81, 3.04), double support phase duration (SMD= -1.69; 95% CI: -2.76, -0.62) and step length (SMD=1.37; 95% CI: 0.36, 2.38) with large effect sizes.
Conclusions: There is no strong evidence supporting the beneficial effect of using stretching to improve gait. Further randomized controlled trials are needed to understand the impact of stretching on human gait.

Keywords

stretching, gait, performance, balance, physical therapy

Corresponding author: Arnaud Delafontaine

Competing interests: No competing interests were disclosed.

Grant information: The author(s) declared that no grants were involved in supporting this work.

Copyright: © 2020 Vialleron T et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: Vialleron T, Delafontaine A, Ditcharles S et al. Effects of stretching exercises on human gait: a systematic review and meta-analysis [version 2; peer review: 2 approved, 1 approved with reservations]. F1000Research 2020, 9:984 (https://doi.org/10.12688/f1000research.25570.2) First published: 13 Aug 2020, 9:984 (https://doi.org/10.12688/f1000research.25570.1) Latest published: 30 Oct 2020, 9:984 (https://doi.org/10.12688/f1000research.25570.2)

Revised Amendments from Version 1

We have added a whole paragraph at the beginning of the introduction section to specify how gait can be related to the different variables seen in the review.
No article in children with cerebral palsy fitted our inclusion criteria during the systematic search of the literature. We have added a whole paragraph in a specific section “limitations of the study” for explain it.
We have added some precisions in the discussion section (healthy older adults paragraph) to specify how we have limited the risk of bias.
We have added some precisions in the discussion section (young adults paragraph) to specify why stretching is less interesting to improve gait parameters in young healthy adults.

See the authors' detailed response to the review by Xu Wei and Guoning Zhang
See the authors' detailed response to the review by Fabrice Mégrot

Introduction

Gait is the medical term used to describe the human whole body movement of walking¹. Gait involves internal and external forces that act on the body to move the center of mass (COM) across a given distance². It depends on many biomechanical features that can be observed during gait analysis such as center of mass shift, joint range of motion (ROM), forces, muscle activity, joint moments, and joint powers³. Spatiotemporal features (e.g. velocity, step length, stride length, step with, step variability) and kinematics parameters (ROM) can be observed subjectively with functional evaluations by clinicians (e.g. the Tinetti test⁴ or the timed up and go test⁵), but, it can be further objectified with biomechanical analysis in a laboratory². Kinetics variables (the forces that cause the body to move) must be collected in a laboratory environment with force plates (e.g. 6–9 for recent studies that used this technic).

Gait is a highly complex motor skill that is classically considered as an integrative measure and a predictor of health in older adults (e.g. 10; cf. 11 and also 12 for recent research topics on this matter). The loss of gait or its alteration with pathological conditions are known to be related to mortality, especially in the elderly (e.g. 13,14), stressing the importance of addressing gait disorders in physiotherapy. Gait requires body propulsion and balance control for safe progression, two “subtasks” that require the coordination of multiple skeletal muscles and the integration of sensory information arising from the vestibular, visual and somatosensory systems^15–17. As such, gait may expose populations with sensory or motor deficits to the risk of falling with serious consequences for health and autonomy. For these reasons, improving gait is a major aim in rehabilitation for most neurological/orthopaedic disorders, such as stroke or Parkinson’s disease, and for frail older adults. Various therapeutic methods have been used to improve gait, such as resistance training¹⁸, endurance training¹⁹, balance training²⁰, whole body vibrations (for a complete review, see Fischer et al., 2019²¹), multi-component exercise programs²² and stretching²³.

The successful completion of numerous daily life activities is conditioned by the ability to move efficiently through a sufficient ROM²⁴. Recent studies on gait initiation^25–27 and seat-to-stand task^28,29 showed that the experimental restriction of postural chain ROM induced by orthosis wear in young healthy adults led to instability and lower motor performance. It is well established that ROM significantly decreases with aging^30–35 and more generally with reduced functional demand (e.g. sedentarity, immobilization, disease etc.)²⁴. Consequently, stretching has become an important part of many sport and rehabilitation programs to maintain or improve ROM, reduce stiffness and promote physical activity. This method has been applied in older adults^36,37, patients with stroke³⁸, Parkinson’s disease³⁹, multiple sclerosis⁴⁰, plantar fasciitis⁴¹ and spastic paraplegia⁴², for example. In sport programs, the influence of stretching on motor performance remains an issue of debate, although recent reviews conclude that maximal muscle performance (e.g. force, power, jump height, reaction time, etc.) is impaired primarily immediately after long durations of stretch (>90 seconds)^43,44. To date, no review has collected results on the relationship between stretching and locomotor performance in rehabilitation programs.

Hence, the purpose of this article is to analyse the effects of a stretching program on gait in each patient category by means of a systematic literature review and meta-analysis, comparing the gait outcomes of the intervention groups with the control groups. It will contribute to provide evidence-based practice from scientific data in order to integrate stretching in rehabilitation programs in a reasoned manner.

Methods

Design and literature screening

The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) methodology was employed in this systematic review⁴⁵. A completed PRISMA checklist was submitted to an online repository (Reporting guidelines).

PubMed, Science Direct, Springer and Sage databases were used for a comprehensive systematic literature search for articles published prior to 28 April 2020 with no time limit. In addition, a manual search was conducted using the reference list of selected studies. The keywords used for the search strategy in PubMed were: “stretching” AND (gait OR walk). We included only articles published in English or French.

The selection procedure was conducted by two experts in rehabilitation (TV and AD). Disagreements were discussed with a third expert in a group until a mutual consensus was reached. First, a review was performed on all available titles obtained from the literature search with the selected keywords. All relevant or potentially relevant titles were included in the subsequent phase. Then, the abstracts were reviewed with all relevant or potential articles included in the following phase. Finally, full-text articles were reviewed to ensure that only relevant studies were included. In the same way, reference lists of all included articles were reviewed to possibly include articles through cross-referencing.

Inclusion and exclusion criteria

We included randomized controlled trials (RCT) and controlled clinical trials (CCT) published in peer-reviewed journals that aimed to explore the effects of stretching on gait parameters. We included all categories of subjects, all stretching techniques and different durations of treatment since standardized protocols are lacking in the purpose of the present study. Gait could be evaluated by functional tests, electromyographic (EMG) or biomechanical analysis. The following exclusion criteria were used: lack of gait assessment, non-application of muscle stretching, multimodal exercise programs, no control group, case report and review.

Data extraction and main measurements examined

Data were extracted from the selected articles by one of the authors (TV). The extracted data were checked by another author (AD) and disagreements were resolved with a third (EY).

The following data were extracted for each selected article: (1) the names of the authors and the date of publication; (2) the number of subjects involved in the experiment with their characteristics and breakdown in each group; (3) stretching training details (in the following order: number of participants, stretching technique, muscle groups stretched, number of sets, duration of stretch, frequency, protocol duration); (4) control group details; and (5) the main outcomes related to gait with the main results. When information could not be provided, it was indicated by a “?”.

Quality and risk of bias assessment

The PEDro scale was used to assess the risk of bias, and thus the methodological quality of the selected studies⁴⁶. This scale was chosen for its ability to provide an overview of the external (criterion 1), internal (criteria 2–9) and statistical (criteria 9 and 10) validity of clinical trials. The scale is divided into 11 criteria, but the first is not calculated in the total score. The output of each criterion could be either “yes” (y), “no” (n) or “do not know” (?). A “y” was given a score of one point, while an “n” or “?” was assigned zero points. Studies with a total score of 5–10/10 (≥ 50%) were considered to be of high quality, and scores of 0–4/10 (<50%) of low quality⁴⁷. Two evaluators independently assessed the quality of the included studies. In the event of disagreement, a group discussion was held with a third expert to reach a consensus.

Statistical analysis

Estimates of effect sizes (comparing the intervention group and the control group) accompanied with a measure of statistical uncertainty (95% confidence interval [95% CI]) were calculated for each outcome when sufficient data were reported. Estimates of effect sizes were reported by standard mean difference (SMD) and their respective 95% CI. In this way, the magnitude of the overall effect can be quantified as trivial (<0.2), small (0.2–0.49), moderate (0.5–0.79) or large (≥0.8)^48,49. When data were lacking to calculate estimates of effect sizes, exact p values were reported.

When at least two studies used the same outcome, meta-analysis was performed, comparing the intervention groups with the control groups. When outcomes were identified in only one study, no meta-analysis could be performed but the effect of intervention was still calculated, reporting the estimate of effect size and its 95% confidence interval. Statistical analysis and figures (i.e. forest plot to facilitate the visualization of values) were produced using a random-effect model in Review Manager software (RevMan, v 5.3, Cochrane Collaboration, Oxford UK). A random-effect model was used to take into account heterogeneity between study effects. Statistical heterogeneity was calculated using the I² and Cochrane Q statistic tests⁴⁸. Statistical significance was set at p<0.05.

Level of evidence

The strength of evidence of primary outcomes was established as described by Van Tulder et al. 2003⁵⁰ based on effect size estimates with a measure of statistical uncertainty (SMD; 95% CI), statistical heterogeneity (I²) when applicable (multiple studies) and risk of bias (PEDro scale). The level of evidence was considered strong with consistent findings among multiple high-quality RCT (at least two RCT with a PEDro score ≥5/10 that were statistically homogenous: I² p≥0.05). The level of evidence was considered moderate with consistent findings among multiple low-quality RCT and/or CCT (two trials with a PEDro score <5/10 that were statistically homogenous) and/or one high quality RCT. The level of evidence was considered limited when only one low quality RCT and/or CCT was identified. The level of evidence was conflicting when there was inconsistency among multiple trials (I² p < 0.05).

Results

Included studies

A total of 821 titles were screened in the first search stage, one more was included through cross-referencing, and 671 were excluded because they did not concern our research question. Following exclusion, 150 studies were considered for an abstract review. A further 105 were excluded in this second stage because they did not meet the inclusion criteria. Finally, 45 full-text articles were assessed for eligibility with 33 not accepted (Figure 1).

Figure 1. PRISMA flow chart of study selection process.

Thus, 12 articles were ultimately included in this systematic review. Six studies evaluated the effects of stretching in healthy older adults^23,51–55, one in a frail elderly population⁵⁶, one study in an elderly population with stable symptomatic peripheral artery disease⁵⁷, one in stroke patients⁵⁸, one study in adults with limited ankle ROM associated with a history of lower limb overuses injury⁵⁹, one study in healthy adults with limited ankle dorsiflexion ROM⁶⁰ and one in healthy young adults⁶¹. A summary of the studies selected is provided in Table 1, and their quality assessment is reported in Table 2. The results in different patient categories are reported below.

Table 1. Summary of the included studies.

Studies	Population	Stretching group	Control group	Outcomes and main results
Kerrigan et al., 2003⁵³	96 healthy older adults, ? (≥65 years)	n= 47, static stretching, hip flexors, 4 sets, 30 seconds, twice daily, 10 weeks	n=49, static shoulder deltoid-stretching, same protocol	No significant difference between groups for hip extension (SMD= 0.22; 95% CI: -0.18, 0.62), hip torque (SMD= 0.35; 95% CI: -0.06, 0.75), anterior pelvic tilt (SMD= -0.35 ; 95% CI : -0.76, 0.05), ankle plantar flexion ROM (SMD= -0.05, 95% CI : -0.45, 0.35), ankle plantar flexion power (SMD= 0.00 ; 95% CI : -0.40, 0.40), hip extension (SMD= 0.22 ; 95% CI : -0.19, 0.62) and hip torque (SMD= 0.35; 95% CI: -0.06, 0.75)
Gajdosik et al., 2005²³	19 community dwelling older women, ? (65–89 years)	n=10, static stretching, ankle plantar flexors, 10 sets, 15 seconds, 3 times per week, 8 weeks	n=9, no exercise.	No significant difference between groups for 10MWT (SMD= -0.76; 95% CI: -1.70, 0.18)
Christiansen, 2008⁵¹	40 healthy older adults, 72.10±4.70 years	N= 20, static stretching, hip flexors, 3 sets, 45 seconds, twice daily, 8 weeks	n=20, maintain their current level of physical activity	No significant difference between groups for gait speed (SMD= -0.32; 95% CI: -0.97, 0.33), hip extension (SMD= 0.22; 95% CI: -0.43, 0.86), stride length (SMD= - 0.14 ; 95% CI : -0.79, 0.50), ankle dorsiflexion (SMD= 0.29 ; 95% CI : -0.36, 0.94)
Cristopoliski et al., 2009⁵²	20 healthy elderly women, 65.90±4.20 years	n=12, static stretching, hip flexors and extensors, ankle plantar flexors, 4 sets, 60 seconds, 3 sessions per week, 12 sessions	n=8, no specific activity in this period	Significant improvement in favor of stretching group for gait speed (SMD= 1.32 ; 95% CI : 0.32, 2.32), anterior pelvic tilt (SMD= -2.52 ; 95% CI : -3.77, -1.27), stand phase duration (SMD= -1.92; 95% CI: -3.04, -0.81), swing phase duration (SMD= 1.92 ; 95% CI : 0.81, 3.04), double support phase duration (SMD= -1.69; 95% CI: -2.76, -0.62), step length (SMD= 1.37 ; 95% CI : 0.36, 2.38) and pelvic rotation (SMD= 1.37 ; 95% CI : 0.36, 2.38) No significant difference between groups for cycle duration (SMD= - 0.24 ; 95% CI : -1.14, 0.66), heel-contact velocity (SMD= -0.46 ; 95% CI : -1.37, 0.45), toe clearance (SMD= 0.91 ; 95% CI : -0.04, 1.86), lateral pelvic tilt (SMD= 0.93 ; 95% CI : -0.02, 1.88) and knee ROM (SMD= 0.23 ; 95% CI : -0.67, 1.12)
Watt et al., 2011⁵⁵	82 healthy elderly subjects, 72,6±6 years	n= 43, static stretching, hip flexors, 2 sets, 60 seconds, 2 sessions daily stretching, 10 weeks	N= 39, shoulder abductor static stretching, same protocol	Significant improvement in favor of stretching group for gait speed (SMD= 0.47; 95% CI: 0.03, 0.91) No significant difference between groups for hip extension (SMD= 0.18; 95% CI: -0.25, 0.62), anterior pelvic tilt (SMD=0.07 ; 95% CI : -0.36, 0.51), stride length (SMD= 0.54 ; 95% CI : -0.01, 1.08)
Locks et al., 2012⁵⁴	23 healthy older individuals, 67.5±2.12 years	n=10, static stretching, knee extensors, ankle dorsiflexor, knee flexors, ankle plantar flexors, 4 sets, 60 seconds, twice a week ,12 weeks	n=13 a one-hour seminar on healthy living every four weeks and did not perform any physical or therapeutic exercise.	No significant difference between groups for 6MWT (SMD= -0.04; 95% CI : -0.86, 0.79)
Watt et al., 2011⁵⁶	74 frail elderly subjects, 77.00±8.00 years	n=33, static stretching, hip flexors, 2 sets, 60 seconds, 2 sessions per day, 10 weeks	n=41, shoulder abductor stretching program, same protocol	No significant difference between groups in peak hip extension, (SMD= 0.22; 95% CI: -0.24, 0.68), anterior pelvic tilt (SMD= -0.05; 95% CI: -0.51, 0.41) and cadence (SMD= 0.13; 95% CI: -0.33, 0.59) Significant improvements in favor of the stretching group in walking speed and stride length (both SMD= 0.49; 95% CI: 0.03, 0.96)
Hotta et al., 2019⁵⁷	13 elderly patients with symptomatic peripheral artery disease, ?	n= 13, static stretching, ankle plantar flexor stretching, 1 set, 30 minutes, 5 sessions per week, 4 weeks	n= 13, no stretching intervention (cross- over intervention)	Significant improvements in favor of the stretching group for both total walking distance and continuous walking distance with large effect sizes (SMD= 1.56; 95% CI: 0.66, 2.45 and SMD= 3.05; 95% CI: 1.86, 4.23 respectively)
Kim et al., 2013⁵⁸	24 patients with stroke, 53.30±3.16 years	n=12, static stretching, ankle plantar flexors, 1 set, 20 minutes, 4 times a week, 4 times a week, 6 weeks	n= 12, conventional physical therapy as in the stretching group	No significant difference between groups in sway of the center of pressure (SMD=0.75; 95% CI: -0.09, 1.58)
Johanson et al., 2006⁵⁹	19 adults with limited passive ankle- dorsiflexion ROM (less than 8 degrees) and a history of lower limb overuse injury, 30.30± 9.80 years	n=11, static stretching, ankle plantar flexors, 5 sets, 30 seconds, 2 times daily, 3 weeks	n= 8, continue all of their usual activities	No significant difference between groups in ankle dorsiflexion during gait in both right and left ankle (SMD= 0.50; 95% CI: -0.42, 1.43 and SMD= 0.41; 95% CI: -0.52, 1.33 respectively) and for time-to-heel-off during the stance phase of gait in both right and left ankle (SMD= -0.50; 95% CI: -1.43, 0.43 and SMD= -0.48; 95% CI: -1.41, 0.45 respectively)
Johanson et al., 2009⁶⁰	16 healthy adults with limited passive ankle-dorsiflexion ROM (less than 5 degrees), 27.40±8.20 years	n=8, static stretching, ankle plantar flexors, 4 sets, 30 seconds, 2 times daily, 3 weeks	n=8, no physical activity or stretching programs involving the lower extremities for 3 weeks	No significant difference between groups in ankle dorsiflexion (SMD= 0.53; 95% CI: -0.48, 1.53), maximum knee extension (SMD= -0.07; 95% CI: -1.05, 0.91), medial and lateral gastrocnemius activities (SMD= 0.37; 95% CI: -0.62, 1.36 and SMD= 0.00; 95% CI=: -0.98, 0.98 respectively)
Godges et al., 1993⁶¹	16 healthy, athletic, male college students, 21.00±l.00 years	n=9, static stretching, hip flexors, 3 sets, 2 minutes, 2 sessions per week, 3 weeks	n=7, continue their current activity levels	No significant difference between groups in gait economy (SMD= 0.83; 95% CI: -0.21, 1.87)

SMD: standard mean difference, CI: confidence interval, 10MWT: 10-meter walk test, 6MWT: 6-minute walk test, ROM: ROM, ?: information not provided.

Table 2. Quality assessment of the included studies.

Study	Eligibility criteria specified	Random allocation	Concealed allocation	Groups similar at baseline	Participant blinding	Therapist blinding	Assessor blinding	<15% dropouts	Intention- to-treat analysis	Between- group difference reported	Point estimate and variability reported	Total score	Patient category
Kerrigan et al., 2003	y	y	n	y	n	n	y	y	n	y	y	6	Healthy older adults
Gajdosik et al., 2005	y	y	y	y	n	n	n	y	y	y	y	7
Christiansen, 2008	y	y	n	y	n	n	n	y	n	y	y	5
Cristopoliski et al., 2009	y	y	n	y	n	n	n	y	y	y	y	6
Watt et al., 2011	y	y	n	n	n	n	y	n	n	n	y	3
Locks et al., 2012	y	n	n	y	n	n	n	n	n	y	y	3
Watt et al., 2011	y	y	n	?	n	n	y	n	n	n	y	3	Frail older adults
Hotta et al., 2009	y	y	n	y	n	n	n	y	n	y	y	5	Peripheral artery disease
Kim et al., 2013	n	n	n	y	n	n	n	n	n	y	y	3	Stroke
Johanson et al., 2006	y	y	n	n	n	n	n	y	y	y	y	5	Lower limb overuse injury
Johanson et al., 2009	y	y	n	y	n	n	n	y	y	y	y	6	Limited ankle ROM
Godges et al., 1993	y	y	n	?	n	n	n	y	y	y	y	5	Healthy adults

n: criterion not fulfilled; y: criterion fulfilled; ?: criterion not mentioned; total score: each item (except the first) contributes 1 point to the total score, yielding a PEDro scale score that can range from 0 to 10.

Results in different patient categories

Healthy older adults

Description of the studies and quality assessment

Six studies examined the effects of stretching on healthy elderly subjects^23,51–55. Regarding the characteristics of the subjects, the average sample size was 46.6±33.9 subjects (ranging from 19²³ to 96 subjects⁵³) and the mean age was 70.1±3.6 years (ranging from 65.40⁵² to 75.30 years²³). Regarding the characteristics of the training programs, the average training duration was 8.6±2.7 weeks (ranging from 4⁵² to 12 weeks⁵⁴), with an average frequency of 8.3±6.2 sessions per week (ranging from 2⁵⁴ to 14 sessions^51,53,55). The average number of sets per session was 4.5±2.8 sets (ranging from 2⁵⁵ to 10 sets²³), with an average stretching time of 45.0±18.9 seconds (ranging from 15²³ to 60 seconds^52,54,55). Static stretching was provided in all studies. The muscle groups stretched were the hip flexors^51–55, ankle plantar flexors^23,51,52,54, ankle dorsiflexors⁵⁴, hip extensors⁵², knee extensors and flexors⁵⁴. There was great heterogeneity in gait outcomes. Angular variables during gait included peak hip extension^51,53,55, ankle plantar flexion during gait⁵³, ankle ROM during gait⁵², anterior pelvis tilt^52,55, knee ROM, pelvic rotation, lateral pelvic tilt and hip ROM⁵². Spatiotemporal variables were: gait speed^51,52,55, stance and swing duration, double support phases, step length⁵² and stride length^52,55. Kinetic variables were hip torque and ankle plantar flexion power⁵³. Finally, two functional tests were used: the 10-meter walk test (10MWT)²³ and the 6-minute walk test (6MWT)⁵⁴. Regarding the quality of the studies, the average PEDro score was 4.6±1.6 and one study was identified as a non-randomized trial⁵⁴. The range of score varied from 3^54,55 to 7²³.

Meta-analyses

Four meta-analysis were conducted for the following outcomes (Figure 2): gait speed, stride length, hip extension during gait and anterior pelvic tilt.

Figure 2.

Comparisons between intervention and control groups for gait speed (A), stride length (B), hip extension (C) and anterior pelvic tilt (D) in healthy older adults.

Gait speed: For gait speed (Figure 2A), two studies were included in the meta-analysis^51,52. One study was excluded because intervention and control groups were not similar at baseline⁵⁵. Statistical analysis showed no significant difference between groups (SMD= 0.45; 95% CI: -1.15, 2.06), with heterogeneous results (I²=86%, p=0.007). Thus, the level of evidence was conflicting.

Stride length: For stride length (Figure 2B), two studies were included in the meta-analysis^51,55. Statistical analysis showed no significant difference between groups (SMD= 0.22; 95% CI: -0.44, 0.88), with consistent results (I²=59%, p=0.12). Only one study was of high quality⁵¹, thus a moderate level of evidence supports the lack of beneficial effect of stretching to improve stride length in the elderly.

Hip extension: For hip extension during gait (kinematic data) (Figure 2C), three studies were included in the meta-analysis^51,53,55. Statistical analysis showed no significant difference between groups (SMD= 0.20; 95% CI: -0.06, 0.47), with consistent results (I²=0%, p=0.99). Two studies were of high quality^51,53, thus a strong level of evidence supports the lack of beneficial effect of stretching to improve hip ROM during gait in the elderly.

Anterior pelvic tilt: For anterior pelvic tilt (Figure 2D), three studies were included in the meta-analysis^52,53,55. Statistical analysis showed no significant difference between groups (SMD= -0.70; 95% CI: -1.60, 0.21), with heterogeneous results (I²=87%, p<0.01). Thus, the level of evidence was conflicting.

Effects of interventions in other outcomes

For the outcomes below, no meta-analysis could be performed because only one study was identified. Nevertheless, for each outcome, effect size estimates with a measure of statistical uncertainty (95% CI) were provided.

Angular variables during gait initiation: The study of Christiansen et al. (2008) showed no significant difference between stretching and control groups for ankle dorsiflexion during gait (SMD=0.29; 95% CI: -0.36, 0.94) with a moderate level of confidence (PEDro score: 5/10). The study of Kerrigan et al. (2003) showed no significant difference between groups for ankle plantar flexion (SMD=-0.05; 95% CI: -0.45, 0.35), with a moderate level of confidence (PEDro score: 6/10). The study of Cristopoliski et al. (2009) showed no significant difference between groups for lateral pelvic tilt (SMD= 0.93; 95% CI: -0.02, 1.88) and knee ROM (SMD= 0.23; 95% CI: -0.67, 1.12), with a moderate level of confidence (PEDro score: 6/10).

Kinetic variables: The study of Kerrigan et al. (2003) showed no significant difference between groups for hip torque (SMD= 0.35; 95% CI: -0.06, 0.75) and ankle plantar flexion power (SMD=0.00; 95% CI: -0.40, 0.40), with a moderate level of confidence (PEDro score: 6/10).

Spatiotemporal variables: The study of Cristopoliski et al. (2009) showed no significant difference between groups for cycle duration (SMD= -0.24; 95% CI: -1.14, 0.66), heel contact velocity (SMD= -0.46; 95% CI: -1.37, 0.45) and toe clearance (SMD= 0.91; 95% CI: -0.04, 1.86). However, the study showed significant decreases with large effect sizes in stance phase duration (SMD=-1.92; 95% CI: -3.04, -0.81), double support phase duration (SMD= -1.69; 95% CI: -2.76, -0.62) in favour of the stretching group as compared to the control group. Additionally, the authors found significant increases with large effect sizes of swing phase duration (SMD=1.92; 95 CI: 0.81, 3.04) and step length (SMD=1.37; 95% CI: 0.36, 2.38) in favour of the stretching group as compared to the control group. The study obtained a PEDro score of 6/10, thus, the level of evidence for these outcomes was moderate.

Functional tests: The study of Gajdosik et al. (2005) showed no significant difference between groups for the 10MWT (SMD= -0.76; 95% CI= -1.70, 0.18), with a moderate level of confidence (PEDro score: 7/10). The study of Locks et al. (2012) showed no significant improvement of the 6MWT in favour of the stretching group as compared to the control group (SMD= -0.04; 95% CI:-0.86, 0.79) with a limited level of confidence (low quality CCT with a PEDro score of 3/10).

Frail elderly

Description of the study and quality assessment

The study of Watt et al. 2011 examined the effects of stretching on frail elderly subjects⁵⁶. Regarding the characteristics of the subjects, 74 subjects were included, and the mean age was 77.0±8.0 years. Regarding the characteristics of the training programs, the stretching program lasted ten weeks, with a frequency of 14 sessions per week (two sessions per day). Participants performed two sets per session, holding the stretch for 60 seconds (static stretching), alternating the right and left limb (four minutes in total). The muscle group stretched was the hip flexors. The outcomes were cadence (steps/minute), walking speed (meters/second), stride length (meters) peak hip extension (degree) and peak anterior pelvic tilt (degree). Regarding the quality assessment, the study was identified as RCT and had an average PEDro score of 3 (low level of evidence).

Effects of intervention

The study of Watt et al. (2011) showed no significant difference between groups in angular variables, i.e. peak hip extension and anterior pelvic tilt (SMD= 0.22; 95% CI: -0.24, 0.68 and SMD= -0.05; 95% CI: -0.51, 0.41 respectively). There was also no significant difference for cadence (SMD= 0.13; 95% CI: -0.33, 0.59). However, the study showed significant improvements in favour of the stretching group with small effect sizes in some performance-related variables, i.e. walking speed and stride length (both SMD= 0.49; 95% CI: 0.03, 0.96).

Elderly with symptomatic peripheral artery disease

Description of the study and quality assessment

The study of Hotta et al. (2019) examined the effects of stretching in elderly with symptomatic peripheral artery disease⁵⁷. Regarding the characteristics of the subjects, 13 subjects were included and the mean age was not mentioned. Regarding the characteristics of the training programs, the stretching program lasted four weeks, with a frequency of five sessions per week. Participants performed one set daily, holding the stretch for 30 minutes (static stretching with splints). The muscle group stretched was ankle plantar flexors. The gait outcome was 6MWT. Regarding the quality assessment, the study was identified as RCT and had an average PEDro score of 5 (moderate level of evidence).

Effects of intervention

The study of Hotta et al. (2019) showed significant improvements in favour of the stretching group for both total walking distance and continuous walking distance with large effect sizes (SMD= 1.56; 95% CI: 0.66, 2.45 and SMD= 3.05; 95% CI: 1.86, 4.23 respectively).

Stroke

Description of the study and quality assessment

The study of Kim et al. (2013) examined the effects of stretching on stroke patients⁵⁸. Only a static muscle stretching training group and control group were included in the analysis. Regarding the characteristics of the subjects, 24 subjects were included, and the mean age was 53.3±3.1 years. Regarding the characteristics of the training programs, the stretching program lasted six weeks, with a frequency of four sessions per week. Participants performed one set per session, holding the stretch for 20 minutes (static stretching). The muscle group stretched was ankle plantar flexors. The outcome was the sway of the centre of pressure during the stance phase. Regarding the quality assessment, the study was identified as CCT and had an average PEDro score of 3 (low level of evidence).

Effects of intervention

The study of Kim et al. (2013) showed no significant difference between groups in the sway of the centre of pressure (SMD=0.75; 95% CI: -0.09, 1.58).

Young adults with limited ankle ROM and a history of lower limb overuse injury

Description of the study and quality assessment

The study of Johanson et al. (2006) examined the effects of stretching on healthy adults with limited passive ankle-dorsiflexion ROM (less than eight degrees) and a history of lower limb overuse injury⁵⁹. Regarding the characteristics of the subjects, 19 subjects were included and the mean age was 30.3±9.8 years. Regarding the characteristics of the training programs, the stretching program lasted three weeks, with a frequency of two sessions per day. Participants performed five sets per session, holding the stretch for 30 seconds (static stretching). The muscle group stretched was ankle plantar flexors. The outcomes were ankle dorsiflexion and time-to-heel-off during the stance phase of gait. Regarding the quality assessment, the study was identified as RCT and had an average PEDro score of 5 (moderate level of evidence).

Effects of intervention

The study of Johanson et al. (2006) showed no significant difference between groups in ankle dorsiflexion during gait in both the right and left ankle (SMD= 0.50; 95% CI: -0.42, 1.43 and SMD= 0.41; 95% CI: -0.52, 1.33 respectively). There was also no significant difference between groups for time-to-heel-off during the stance phase of gait in both the right and left ankle (SMD= -0.50; 95% CI: -1.43, 0.43 and SMD= -0.48; 95% CI: -1.41, 0.45 respectively).

Young adults with limited ankle ROM

Description of the study and quality assessment

The study of Johanson et al. (2009) examined the effects of stretching on young adults with limited passive ankle-dorsiflexion ROM (less than 5 degrees)⁶⁰. It is worth noticed that these participants were not the same than in the study of Johanson et al. (2006). In contrast, the characteristics of the training programs were the same as in Johanson et al. (2006). In the current study, 16 subjects were included, and the mean age was 27.4±8.2 years. The muscle group stretched was the ankle plantar flexors. The outcomes were maximum ankle dorsiflexion, maximum knee extension and EMG amplitude of the gastrocnemius during the stance phase of gait. Regarding the quality assessment, the study was identified as RCT and had an average PEDro score of 6 (moderate level of evidence).

Effects of intervention

The study of Johanson et al. (2009) showed no significant difference between groups in angular variables during gait, i.e. maximum ankle dorsiflexion and maximum knee extension (SMD= 0.53; 95% CI: -0.48, 1.53 and SMD= -0.07; 95% CI: -1.05, 0.91 respectively). There was also no significant difference between groups for EMG variables, i.e. medial and lateral gastrocnemius activity (SMD= 0.37; 95% CI: -0.62, 1.36 and SMD= 0.00; 95% CI=: -0.98, 0.98 respectively).

Healthy young adults

Description of the study and quality assessment

The study of Godges et al. (1993) examined the effects of stretching on healthy young adults⁶¹. Only a static hip extension stretching group and control group were included in the analysis. Regarding the characteristics of the subjects, 16 subjects were included, and the mean age was 21.0±1.0 years. Regarding the characteristics of the training programs, the stretching program lasted three weeks, with a frequency of two sessions per week. Participants performed three sets per session, holding the stretch for two minutes (static stretching). The muscle group stretched was the hip flexors. The outcome was walking economy (ml/kg/min). Regarding the quality assessment, the study was identified as RCT and had an average PEDro score of 5 (moderate level of evidence).

Effects of intervention

The study of Godges et al. (1993) showed no significant difference between groups in gait economy in terms of oxygen consumption (SMD= 0.83; 95% CI: -0.21, 1.87).

Discussion

The aim of this systematic review was to determine the effects of a stretching program on human gait by means of a systematic literature review and meta-analysis. Twelves studies were identified in six different patient categories. Statistical analyses showed no strong level of evidence supporting the beneficial effect of a stretching program to improve any gait outcome. The major issue in conducting meta-analyses and establishing strong level of evidences was the great heterogeneity in gait variables. The results obtained in the different patient categories are discussed in detail below.

Healthy older adults

The healthy older adult population was the most studied. Two muscle groups were systematically stretched in the six identified studies: hip flexors^{23,51–53,55} and ankle plantar flexors^23,51–53. Hip flexor stiffness, associated with reduced hip extension during gait has been demonstrated in the elderly and may alter gait^62,63. In the same way, decreased calf muscle length associated with restricted dorsiflexion ROM is well documented in older adults^35,64. A decreased ankle dorsiflexion ROM has been correlated with poorer balance test scores in the elderly⁶⁵ and may contribute to an increased risk of falls⁶⁶. All the studies included in the present analysis showed that specific stretching programs were efficient to improve passive ROM of the targeted joints, but results are more heterogeneous regarding gait performance and dynamic ROM. This led to inconsistency in the results or the impossibility to conclude with a strong level of evidence that a stretching program improves gait in healthy older adults. Moreover, when improvement in ROM or gait performance occurred, it was not associated with a significant increase in dynamic hip extension or ankle dorsiflexion. Only trends toward increased dynamic ROM after stretching interventions were observed^51,53,55. This observation was consistent in young adults.

When data were meta-analyzed, we ensured that the groups and the training characteristics were similar to limit the risk of bias. This explains that a limited number of studies was included in the meta-analysis. It is worth noticed that the stretching technic was the same (i.e. static stretching), but that details of interventions varied across these studies. For example, both studies selected for the meta-analysis of gait speed included hip flexors and plantar flexors stretching, but, one study included hip extensor stretching⁵² whereas the other did not⁵¹. This difference may partially explain the heterogenous results in the meta-analysis (I²=86%, p=0.007). In the same way, the heterogenous results observed in the meta-analysis of anterior pelvic tilt (I²=87%, <0.01) may be explained by the stretching of additional muscle groups (hip extensors and plantar flexors) in the study of Cristopoliski et al. (2009) compared to the other studies (in which only hip flexors were stretched)^53,55. Nevertheless, heterogeneity in the results was not systematically observed between studies that used slight different protocols, as showed by the consistent results int the meta-analyses of stride length (I²=59%, p=0.12) and hip extension (I²=0%, p=0.99). Thus, we assume that we have limited the risk of bias in the meta-analyses.

Stroke patients

In stroke patients, ankle plantar flexor stretching has been successfully used to improve ankle stiffness^67–70. Decreased plantar flexors stiffness may have a beneficial effect on postural control during gait because triceps surae is known to play an important role during gait^71–73 and an increase in muscle stiffness might alter synergistic muscle activities during human gait. However, only one non-randomized study⁵⁸ was identified and included in the current systematic review. Other studies that used stretching in multicomponent programs^74–76 or in control groups^77,78 were identified but excluded because of the addition of resistance training or the lack of a control group. Nevertheless, it should be noted that some studies showed improvements between pre- and post-stretching conditions. Forrester et al. (2014) showed that both robotic ankle mobilizations and manual ankle stretching improved gait velocity in stroke patients at hospital discharge compared to baseline. Similarly, Park et al. (2018) showed that both static ankle stretching and ankle mobilizations improved gait speed after four weeks of treatment compared to baseline. Other authors showed that one week of immobilization in dorsiflexed position (casting) followed by one week of plantar flexor stretching and gait training improved gait performances in 10MWT and 6MWT⁷⁴. Hence, these encouraging results suggest that further randomized controlled trials of good quality are needed to explore the ability of ankle stretching to improve gait parameters in stroke or in other neurological diseases exposing patients to joint stiffness, e.g. Parkinson’s disease⁷⁹.

Young adults

In healthy adults, the interest of practicing stretching to improve gait seems limited as they are assumed to have sufficient mobility for walking. Moreover, the included study involved athletic males⁶¹, a population that is known to be more flexible than inactive persons⁸⁰. Stretching should be more indicated when ROM is limited²⁴. However, even in young adults with limited ankle ROM, stretching did not improve dynamic dorsiflexion during gait^59,60. Stretching programs in apparently healthy adults should be more indicated after a prolonged period of reduced functional demand (e.g. immobilization, sedentarity), when ROM is insufficient to practice a specific activity or when high levels of flexibility are required for sport performance (e.g. gymnastics or dance) and in sports that involve stretch-shortening cycles (e.g. basketball, volleyball)²⁴.

Limitations of the study

Some patient categories were not included in the present review, although muscle stretching is commonly indicated in their clinical care to reduce spasticity⁸¹. This is for example the case for children with cerebral palsy⁸². In fact, we were able to identify studies in the literature focusing on the effects of stretching on gait in this population during the first phase of the present review, but the protocol of these studies combined stretching with another form of training (e.g. 83,84) or there was no control group (e.g. 85). These studies therefore did not fit with the inclusion criteria of the present systematic review and were consequently excluded. Now, it should be stressed that the effectiveness of static stretching to improve motor function in children with cerebral palsy is still controversial⁸⁶, although some authors showed that functional stretching exercises may be effective to improve gait⁸⁵. Further randomized controlled trials are needed to explore the impact of stretching on gait in this population.

To reduce the risk of bias, data were meta-analyzed when at least 2 studies with similar populations and training characteristics were found. Considering these constraints and the great heterogeneity in the gait outcomes, we only performed meta-analyses in healthy older adults for 4 outcomes. The Cochrane Qualitative and Implementation Methods Group recommends the application of Grades of Recommendation, Assessment, Development, and Evaluation (GRADE) in the Evidence from Qualitative Reviews to assess the level of confidence in systematic review with meta-analyses⁸⁷. However, the GRADE necessitates assessing the risk of publication bias with a funnel plot, determining its asymmetry, which can be performed with at least 10 studies⁸⁸. In the present study, the meta-analyses included less that 10 randomized controlled trials, so, we chose to implement other guidelines described by a Cochrane collaboration group to assess the level of evidence⁵⁰. Because this method includes fewer criteria, our confidence in the results must be taken with caution

Conclusion

Twelve studies were identified, involving a total of 442 subjects. Despite some improvements in isolated studies, statistical analyses showed no strong level of evidence supporting the beneficial effect of using stretching alone to improve gait outcomes in rehabilitation programs. The major obstacle in conducting meta-analyses and establishing strong levels of evidence were the great heterogeneity in gait variables and the low quality of the included studies. Because the effects of stretching are not clear, further randomized controlled trials of good quality are needed to understand the impact of stretching on human gait. Currently, stretching is more recommended to maintain and improve ROM rather than improve gait parameters and should be integrated in multicomponent programs.

Data availability

Underlying data

All data underlying the results are available as part of the article and no additional source data are required.

Reporting guidelines

Harvard Dataverse: PRISMA checklist and PRISMA flow diagram for ‘Effects of stretching exercises on human gait: a systematic review and meta-analysis’, https://doi.org/10.7910/DVN/N8ZXNB⁸⁹.

Data are available under the terms of the Creative Commons Zero “No rights reserved” data waiver (CC0 1.0 Public domain dedication).

Faculty Opinions recommended

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Author details Author details

¹ CIAMS, Univ. Paris-Sud., Université Paris-Saclay, Orsay, 91405, France
² CIAMS, Université d'Orléans, Orléans, Orléans, 45067, France
³ ENKRE, Saint Maurice, Ile de France, 94410, France

Thomas Vialleron
Roles: Conceptualization, Methodology, Writing – Original Draft Preparation

Arnaud Delafontaine
Roles: Conceptualization, Methodology, Writing – Original Draft Preparation

Sebastien Ditcharles
Roles: Writing – Review & Editing

Paul Fourcade
Roles: Writing – Review & Editing

Eric Yiou
Roles: Supervision, Writing – Review & Editing

Competing interests

No competing interests were disclosed.

Grant information

The author(s) declared that no grants were involved in supporting this work.

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https://doi.org/10.12688/f1000research.25570.2

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© 2020 Vialleron T et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Vialleron T, Delafontaine A, Ditcharles S et al. Effects of stretching exercises on human gait: a systematic review and meta-analysis [version 2; peer review: 2 approved, 1 approved with reservations]. F1000Research 2020, 9:984 (https://doi.org/10.12688/f1000research.25570.2)

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ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested

Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.

Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions

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Reviewer Report 26 Feb 2021

Maria Garcia Escudero, School of Medicine and Health Sciencies, Universidad Católica de Valencia San Vicente Mártir, Valencia, Spain

Approved

https://doi.org/10.5256/f1000research.30366.r79222

I believe that the idea of this research study was necessary to carry it out because of the need to clarify stretch treatments and clear protocols to improve the progress of patients.

I think the methodology used is appropriate although after reviewing the results it is concluded that further randomized controlled trials of good quality are necessary even to offer this line of research to carry out new studies and improve the cohort of patients by categories and sample number.

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

Yes
Are the conclusions drawn adequately supported by the results presented in the review?

Yes

Competing Interests: No competing interests were disclosed.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

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Reviewer Report 09 Nov 2020

Fabrice Mégrot, Unité Clinique d’Analyse de la Marche et du Mouvement, Centre de Médecine Physique et de Réadaptation pour Enfants Bois-Larris, Croix-rouge française, Lamorlaye, France; BioMécanique et BioIngénierie (BMBI) - UMR 7338, Université de Technologie de Compiègne, Sorbonnes Université, Compiègne, France

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https://doi.org/10.5256/f1000research.30366.r74039

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Reviewer Report 09 Oct 2020

Xu Wei, Department of Orthopaedic Surgery, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

Guoning Zhang, Department of Orthopaedic Surgery, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

Approved with Reservations

https://doi.org/10.5256/f1000research.28219.r69875

The purpose of this article is to analyse the effects of a stretching program on gait in each patient category by means of a systematic literature review and meta-analysis, comparing the gait outcomes of the intervention groups

The purpose of this article is to analyse the effects of a stretching program on gait in each patient category by means of a systematic literature review and meta-analysis, comparing the gait outcomes of the intervention groups with the control groups. This is a very interesting research direction and it has good innovation. But different ages and diseases have different gait results and different stretching training modes and intervention methods. How to eliminate the bias caused by these differences in meta-analysis and comparison?
Four meta-analysis were conducted for the following outcomes (Figure 2): gait speed, stride length, hip extension during gait and anterior pelvic tilt. Why choose these four dimensions? Is there any theoretical basis?
Kinetic variables: The study of Kerrigan et al. (2003)44 showed no significant difference between groups for hip torque (SMD= 0.35; 95% CI: -0.06, 0.75) and ankle plantar flexion power (SMD=0.00; 95% CI: -0.40, 0.40), with a moderate level of confidence (PEDro score: 6/10).: It seems that gait analysis cannot directly measure muscle power. sEMG can only evaluate muscle recruitment signals to evaluate muscle fiber contraction. Therefore, how is ankle flexion power measured by gait analysis?
Twelve studies were included in the analysis. Stretching improved gait performance as assessed by walking speed and stride length only in a study with a frail elderly population, with small effect sizes. There is no strong evidence supporting the beneficial effect of using stretching to improve gait. I think that since stretching can improve gait parameters for adults with special weakness, the effect of stretching on gait is significant, although it has little effect on healthy adults or young adults. Should it be explained? In general, this study made a meta-analysis on the effect of stretching on gait, which has good innovation. However, whether gait analysis has guiding significance for different groups of rehabilitation training is still controversial especially for healthy adults, so the research conclusion of this paper has practical significance in clinical guidance.

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

Partly
Are the conclusions drawn adequately supported by the results presented in the review?

Partly

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Sports medicine; osteoporosis; osteosarcoma; Spine surgery; Scoliosis

We confirm that we have read this submission and believe that we have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however we have significant reservations, as outlined above.

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Author Response 30 Oct 2020

ARNAUD DELAFONTAINE, CIAMS, Université d'Orléans, Orléans, 45067, France

30 Oct 2020

Author Response

Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. Different ages and diseases have different gait results and different ... Continue reading Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. Different ages and diseases have different gait results and different stretching training modes and intervention methods. How to eliminate the bias caused by these differences in meta-analysis and comparison?

Reply: We add some precisions in the discussion section (healthy older adults paragraph) to specify how we have limited the risk of bias:
Please see L353-366: When data were meta-analyzed, we ensured that the groups and the training characteristics were similar to limit the risk of bias. This explains that a limited number of studies was included in the meta-analysis. It is worth noticing that the stretching technic was the same (i.e. static stretching), but that details of interventions varied across these studies. For example, both studies selected for the meta-analysis of gait speed included hip flexors and plantar flexors stretching, but, one study included hip extensor stretching⁵² whereas the other did not⁵¹. This difference may partially explain the heterogenous results in the meta-analysis (I²=86%, p=0.007). In the same way, the heterogenous results observed in the meta-analysis of anterior pelvic tilt (I²=87%, p<0.01) may be explained by the stretching of additional muscle groups (hip extensors and plantar flexors) in the study of Cristopoliski et al. (2009) compared to the other studies (in which only hip flexors were stretched)^53,55. Nevertheless, heterogeneity in the results was not systematically observed between studies that used slight different protocols, as showed by the consistent results in the meta-analyses of stride length (I²=59%, p=0.12) and hip extension (I²=0%, p=0.99). Thus, we assume that we have limited the risk of bias in the meta-analyses.

Comment 2. Four meta-analysis were conducted for the following outcomes (Figure 2): gait speed, stride length, hip extension during gait and anterior pelvic tilt. Why choose these four dimensions? Is there any theoretical basis?

Reply: Only these four outcomes fitted with the inclusion criteria for meta-analysis. Meta-analyses were performed only when more than one trial was identified for each outcome. Additionally, to reduce the risk of bias, we ensured that the groups were similar. For example, in the study of Watt et al. (2011), the intervention group had a significantly higher gait speed than the control group, so the trial was excluded of the meta-analysis.

Comment 3. Kinetic variables: The study of Kerrigan et al. (2003)44 showed no significant difference between groups for hip torque (SMD= 0.35; 95% CI: -0.06, 0.75) and ankle plantar flexion power (SMD=0.00; 95% CI: -0.40, 0.40), with a moderate level of confidence (PEDro score: 6/10).: It seems that gait analysis cannot directly measure muscle power. sEMG can only evaluate muscle recruitment signals to evaluate muscle fiber contraction. Therefore, how is ankle flexion power measured by gait analysis?

Reply: In the study of Kerrigan et al. (2003), “joint torque and power calculations were based on the mass and inertial characteristics of each lower-extremity segment, the derived linear and angular velocities and accelerations of each lower-extremity segment, and the ground reaction force and joint center position estimates. Joint torques and powers were normalized for body weight and height and were reported as external in newton meters per kilogram meters (N.m/kg.m) and watts per kilogram meters (W/kg.m), respectively”.
Unless special recommendation of the reviewer or the Editor, we feel it is not necessary to add how the ankle flexion power was measured in the study of Kerrigan et al. (2003).

Comment 4. I think that since stretching can improve gait parameters for adults with special weakness, the effect of stretching on gait is significant, although it has little effect on healthy adults or young adults. Should it be explained?

Reply: We add some precisions in the discussion section (young adults paragraph) to specify why stretching is less interesting to improve gait parameters in young healthy adults:

Please see L387-390: In healthy adults, the interest of practicing stretching to improve gait seems limited as they are assumed to have sufficient mobility for walking. Moreover, the included study involved athletic males ⁶¹, a population that is known to be more flexible than inactive persons ⁸¹. Stretching should be more indicated when range of motion is limited²⁴.

Best regards
Arnaud Delafontaine
on behalf of all the authors
Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. Different ages and diseases have different gait results and different stretching training modes and intervention methods. How to eliminate the bias caused by these differences in meta-analysis and comparison?

Reply: We add some precisions in the discussion section (healthy older adults paragraph) to specify how we have limited the risk of bias:
Please see L353-366: When data were meta-analyzed, we ensured that the groups and the training characteristics were similar to limit the risk of bias. This explains that a limited number of studies was included in the meta-analysis. It is worth noticing that the stretching technic was the same (i.e. static stretching), but that details of interventions varied across these studies. For example, both studies selected for the meta-analysis of gait speed included hip flexors and plantar flexors stretching, but, one study included hip extensor stretching⁵² whereas the other did not⁵¹. This difference may partially explain the heterogenous results in the meta-analysis (I²=86%, p=0.007). In the same way, the heterogenous results observed in the meta-analysis of anterior pelvic tilt (I²=87%, p<0.01) may be explained by the stretching of additional muscle groups (hip extensors and plantar flexors) in the study of Cristopoliski et al. (2009) compared to the other studies (in which only hip flexors were stretched)^53,55. Nevertheless, heterogeneity in the results was not systematically observed between studies that used slight different protocols, as showed by the consistent results in the meta-analyses of stride length (I²=59%, p=0.12) and hip extension (I²=0%, p=0.99). Thus, we assume that we have limited the risk of bias in the meta-analyses.

Comment 2. Four meta-analysis were conducted for the following outcomes (Figure 2): gait speed, stride length, hip extension during gait and anterior pelvic tilt. Why choose these four dimensions? Is there any theoretical basis?

Reply: Only these four outcomes fitted with the inclusion criteria for meta-analysis. Meta-analyses were performed only when more than one trial was identified for each outcome. Additionally, to reduce the risk of bias, we ensured that the groups were similar. For example, in the study of Watt et al. (2011), the intervention group had a significantly higher gait speed than the control group, so the trial was excluded of the meta-analysis.

Comment 3. Kinetic variables: The study of Kerrigan et al. (2003)44 showed no significant difference between groups for hip torque (SMD= 0.35; 95% CI: -0.06, 0.75) and ankle plantar flexion power (SMD=0.00; 95% CI: -0.40, 0.40), with a moderate level of confidence (PEDro score: 6/10).: It seems that gait analysis cannot directly measure muscle power. sEMG can only evaluate muscle recruitment signals to evaluate muscle fiber contraction. Therefore, how is ankle flexion power measured by gait analysis?

Reply: In the study of Kerrigan et al. (2003), “joint torque and power calculations were based on the mass and inertial characteristics of each lower-extremity segment, the derived linear and angular velocities and accelerations of each lower-extremity segment, and the ground reaction force and joint center position estimates. Joint torques and powers were normalized for body weight and height and were reported as external in newton meters per kilogram meters (N.m/kg.m) and watts per kilogram meters (W/kg.m), respectively”.
Unless special recommendation of the reviewer or the Editor, we feel it is not necessary to add how the ankle flexion power was measured in the study of Kerrigan et al. (2003).

Comment 4. I think that since stretching can improve gait parameters for adults with special weakness, the effect of stretching on gait is significant, although it has little effect on healthy adults or young adults. Should it be explained?

Reply: We add some precisions in the discussion section (young adults paragraph) to specify why stretching is less interesting to improve gait parameters in young healthy adults:

Please see L387-390: In healthy adults, the interest of practicing stretching to improve gait seems limited as they are assumed to have sufficient mobility for walking. Moreover, the included study involved athletic males ⁶¹, a population that is known to be more flexible than inactive persons ⁸¹. Stretching should be more indicated when range of motion is limited²⁴.

Best regards
Arnaud Delafontaine
on behalf of all the authors
Competing Interests: None Close
Report a concern
Respond or Comment

COMMENTS ON THIS REPORT

Author Response 30 Oct 2020

ARNAUD DELAFONTAINE, CIAMS, Université d'Orléans, Orléans, 45067, France

30 Oct 2020

Author Response

Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. Different ages and diseases have different gait results and different ... Continue reading Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. Different ages and diseases have different gait results and different stretching training modes and intervention methods. How to eliminate the bias caused by these differences in meta-analysis and comparison?

Reply: We add some precisions in the discussion section (healthy older adults paragraph) to specify how we have limited the risk of bias:
Please see L353-366: When data were meta-analyzed, we ensured that the groups and the training characteristics were similar to limit the risk of bias. This explains that a limited number of studies was included in the meta-analysis. It is worth noticing that the stretching technic was the same (i.e. static stretching), but that details of interventions varied across these studies. For example, both studies selected for the meta-analysis of gait speed included hip flexors and plantar flexors stretching, but, one study included hip extensor stretching⁵² whereas the other did not⁵¹. This difference may partially explain the heterogenous results in the meta-analysis (I²=86%, p=0.007). In the same way, the heterogenous results observed in the meta-analysis of anterior pelvic tilt (I²=87%, p<0.01) may be explained by the stretching of additional muscle groups (hip extensors and plantar flexors) in the study of Cristopoliski et al. (2009) compared to the other studies (in which only hip flexors were stretched)^53,55. Nevertheless, heterogeneity in the results was not systematically observed between studies that used slight different protocols, as showed by the consistent results in the meta-analyses of stride length (I²=59%, p=0.12) and hip extension (I²=0%, p=0.99). Thus, we assume that we have limited the risk of bias in the meta-analyses.

Comment 2. Four meta-analysis were conducted for the following outcomes (Figure 2): gait speed, stride length, hip extension during gait and anterior pelvic tilt. Why choose these four dimensions? Is there any theoretical basis?

Reply: Only these four outcomes fitted with the inclusion criteria for meta-analysis. Meta-analyses were performed only when more than one trial was identified for each outcome. Additionally, to reduce the risk of bias, we ensured that the groups were similar. For example, in the study of Watt et al. (2011), the intervention group had a significantly higher gait speed than the control group, so the trial was excluded of the meta-analysis.

Comment 3. Kinetic variables: The study of Kerrigan et al. (2003)44 showed no significant difference between groups for hip torque (SMD= 0.35; 95% CI: -0.06, 0.75) and ankle plantar flexion power (SMD=0.00; 95% CI: -0.40, 0.40), with a moderate level of confidence (PEDro score: 6/10).: It seems that gait analysis cannot directly measure muscle power. sEMG can only evaluate muscle recruitment signals to evaluate muscle fiber contraction. Therefore, how is ankle flexion power measured by gait analysis?

Reply: In the study of Kerrigan et al. (2003), “joint torque and power calculations were based on the mass and inertial characteristics of each lower-extremity segment, the derived linear and angular velocities and accelerations of each lower-extremity segment, and the ground reaction force and joint center position estimates. Joint torques and powers were normalized for body weight and height and were reported as external in newton meters per kilogram meters (N.m/kg.m) and watts per kilogram meters (W/kg.m), respectively”.
Unless special recommendation of the reviewer or the Editor, we feel it is not necessary to add how the ankle flexion power was measured in the study of Kerrigan et al. (2003).

Comment 4. I think that since stretching can improve gait parameters for adults with special weakness, the effect of stretching on gait is significant, although it has little effect on healthy adults or young adults. Should it be explained?

Reply: We add some precisions in the discussion section (young adults paragraph) to specify why stretching is less interesting to improve gait parameters in young healthy adults:

Please see L387-390: In healthy adults, the interest of practicing stretching to improve gait seems limited as they are assumed to have sufficient mobility for walking. Moreover, the included study involved athletic males ⁶¹, a population that is known to be more flexible than inactive persons ⁸¹. Stretching should be more indicated when range of motion is limited²⁴.

Best regards
Arnaud Delafontaine
on behalf of all the authors
Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. Different ages and diseases have different gait results and different stretching training modes and intervention methods. How to eliminate the bias caused by these differences in meta-analysis and comparison?

Reply: We add some precisions in the discussion section (healthy older adults paragraph) to specify how we have limited the risk of bias:
Please see L353-366: When data were meta-analyzed, we ensured that the groups and the training characteristics were similar to limit the risk of bias. This explains that a limited number of studies was included in the meta-analysis. It is worth noticing that the stretching technic was the same (i.e. static stretching), but that details of interventions varied across these studies. For example, both studies selected for the meta-analysis of gait speed included hip flexors and plantar flexors stretching, but, one study included hip extensor stretching⁵² whereas the other did not⁵¹. This difference may partially explain the heterogenous results in the meta-analysis (I²=86%, p=0.007). In the same way, the heterogenous results observed in the meta-analysis of anterior pelvic tilt (I²=87%, p<0.01) may be explained by the stretching of additional muscle groups (hip extensors and plantar flexors) in the study of Cristopoliski et al. (2009) compared to the other studies (in which only hip flexors were stretched)^53,55. Nevertheless, heterogeneity in the results was not systematically observed between studies that used slight different protocols, as showed by the consistent results in the meta-analyses of stride length (I²=59%, p=0.12) and hip extension (I²=0%, p=0.99). Thus, we assume that we have limited the risk of bias in the meta-analyses.

Comment 2. Four meta-analysis were conducted for the following outcomes (Figure 2): gait speed, stride length, hip extension during gait and anterior pelvic tilt. Why choose these four dimensions? Is there any theoretical basis?

Reply: Only these four outcomes fitted with the inclusion criteria for meta-analysis. Meta-analyses were performed only when more than one trial was identified for each outcome. Additionally, to reduce the risk of bias, we ensured that the groups were similar. For example, in the study of Watt et al. (2011), the intervention group had a significantly higher gait speed than the control group, so the trial was excluded of the meta-analysis.

Comment 3. Kinetic variables: The study of Kerrigan et al. (2003)44 showed no significant difference between groups for hip torque (SMD= 0.35; 95% CI: -0.06, 0.75) and ankle plantar flexion power (SMD=0.00; 95% CI: -0.40, 0.40), with a moderate level of confidence (PEDro score: 6/10).: It seems that gait analysis cannot directly measure muscle power. sEMG can only evaluate muscle recruitment signals to evaluate muscle fiber contraction. Therefore, how is ankle flexion power measured by gait analysis?

Reply: In the study of Kerrigan et al. (2003), “joint torque and power calculations were based on the mass and inertial characteristics of each lower-extremity segment, the derived linear and angular velocities and accelerations of each lower-extremity segment, and the ground reaction force and joint center position estimates. Joint torques and powers were normalized for body weight and height and were reported as external in newton meters per kilogram meters (N.m/kg.m) and watts per kilogram meters (W/kg.m), respectively”.
Unless special recommendation of the reviewer or the Editor, we feel it is not necessary to add how the ankle flexion power was measured in the study of Kerrigan et al. (2003).

Comment 4. I think that since stretching can improve gait parameters for adults with special weakness, the effect of stretching on gait is significant, although it has little effect on healthy adults or young adults. Should it be explained?

Reply: We add some precisions in the discussion section (young adults paragraph) to specify why stretching is less interesting to improve gait parameters in young healthy adults:

Please see L387-390: In healthy adults, the interest of practicing stretching to improve gait seems limited as they are assumed to have sufficient mobility for walking. Moreover, the included study involved athletic males ⁶¹, a population that is known to be more flexible than inactive persons ⁸¹. Stretching should be more indicated when range of motion is limited²⁴.

Best regards
Arnaud Delafontaine
on behalf of all the authors
Competing Interests: None Close
Report a concern

Views

Reviewer Report 14 Sep 2020

Approved with Reservations

https://doi.org/10.5256/f1000research.28219.r69874

Authors propose a systematic review and meta-analysis to investigate the effects of stretching programs on gait and to determine how stretching might be valuable for rehabilitation. From 150 studies identified through systematic searches and critical appraisal of the literature, 12 articles were considered by the authors.

The various demographics of the participants in the reported studies implied a mixed range of age and aetiology, even if old persons, either with an asymptomatic or a pathological health status, were the most represented individuals.

In young adults, two studies by Johanson are reported. Is it not clear if both groups of young adults with limited range of motion were identical in both studies and had the same characteristics? If yes, merging the two studies should make the deal, if not please provide specification about the second group.

Overall, the methodology is correct, and the meta-analysis well described. The results show weak effects of stretching on gait parameters.

The main issue arises from the various parameters which are considered in all the studies, both during gait initiation and straight walking (spatiotemporal parameters, kinematics, joint strength and dynamics, muscle activity, etc…). Therefore, in the results and the discussion, grouping the types of parameters according to their role in the process of walking would add value to this manuscript. The effects, demonstrated or not, have not all the same meaning depending on whether functional parameters or kinematics angles or even muscle strength and activity are considered.

Gait should be defined in a better way, especially how it is related to the different measures in terms of processes, even if there is anyway no real benefit demonstrated by stretching used as a unique therapy. Surprisingly, no article in children with cerebral palsy has been uncovered, while the clinical care of these children is mostly based on muscle stretching.

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

Yes
Are the conclusions drawn adequately supported by the results presented in the review?

Partly

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: motor control, biomechanics, neurosciences, nonlinear dynamics, clinical gait/movement analysis and gross motor function of children with cerebral palsy

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

CITE

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Author Response 30 Oct 2020

ARNAUD DELAFONTAINE, CIAMS, Université d'Orléans, Orléans, 45067, France

30 Oct 2020

Author Response

Reviewer 1 :

Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. In young adults, two studies by Johanson are ... Continue reading Reviewer 1 :

Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. In young adults, two studies by Johanson are reported. Is it not clear if both groups of young adults with limited range of motion were identical in both studies and had the same characteristics? If yes, merging the two studies should make the deal, if not please provide specification about the second group.The participants in both studies were different. In the study of Johanson et al. (2006), the participants were healthy adults with limited passive ankle-dorsiflexion range of motion (less than 8 degrees) and a history of lower limb overuse injury. In the study Johanson et al. (2009), the characteristics of the stretching program were the same as in Joahnson et al. (2006), but the participants did not have any history of lower limb overuse injury.

Reply: To make this difference clearer, precisions were added in the “included studies” and “results” sections:
Please see L158-163 Thus, 12 articles were ultimately included in this systematic review. Six studies evaluated the effects of stretching in healthy older adults ^23,51–55, one in a frail elderly population ⁵⁶, one study in an elderly population with stable symptomatic peripheral artery disease⁵⁷, one in stroke patients ⁵⁸, one study in adults with limited ankle range of motion (less than 8 degrees) associated with a history of lower limb overuse injury ⁵⁹, one study in healthy adults with limited ankle dorsiflexion range of motion (less than 5 degrees) ⁶⁰ and one in healthy young adults ⁶¹

Please see L285-288: “The study of Johanson et al. (2006) examined the effects of stretching on healthy adults with limited passive ankle-dorsiflexion range of motion (less than 8 degrees) and a history of lower limb overuse injury⁵⁰. Regarding the characteristics of the subjects, 19 subjects were included and the mean age was 30.3±9.8 years.”

Please see L302-306: “The study of Johanson et al. (2009) examined the effects of stretching on young adults with limited passive ankle-dorsiflexion range of motion (less than 5 degrees) ⁵¹. It is worth noticed that these participants were not the same than in the study of Johanson et al. (2006). In contrast, the characteristics of the training programs were the same as in Johanson et al. (2006)”.

Comment 2. In the results and the discussion, grouping the types of parameters according to their role in the process of walking would add value to this manuscript. The effects, demonstrated or not, have not all the same meaning depending on whether functional parameters or kinematics angles or even muscle strength and activity are considered.

Reply: In the results and the discussion, we chose to group the participants by patient categories because differences in ages and health parameters may result in different training effects. However, in each patient category, each variable was considered separately in an organized way.

Comment 3. Gait should be defined in a better way, especially how it is related to the different measures in terms of processes, even if there is anyway no real benefit demonstrated by stretching used as a unique therapy.

Reply: We agree. We add a whole paragraph at the beginning of the introduction section to specify how gait can be related to the different variables seen in the review:

Please see L35-44: “Gait is the medical term used to describe the human whole body movement of walking¹. Gait involves internal and external forces that act on the body to move the center of mass (COM) across a given distance². It depends on many biomechanical features that can be observed during gait analysis such as center of mass shifts, joint range of motion, forces, muscle activity, joint moments, and joint powers³. Spatiotemporal features (e.g. velocity, step length, stride length, step with, step variability) and kinematics parameters (range of motion) can be observed subjectively with functional evaluations by clinicians(e.g. the Tinetti test⁴ or the timed up and go test⁵), but, it can be further objectified with biomechanical analysis in a laboratory². Kinetics variables (the forces that cause the body to move) must be collected in a laboratory environment with force plates (e.g.^6–9 for recent studies that used this technic)”.

Comment 4. Surprisingly, no article in children with cerebral palsy has been uncovered, while the clinical care of these children is mostly based on muscle stretching.

Reply: We agree. However, no article in children with cerebral palsy fitted our inclusion criteria during the systematic search of the literature. We add a whole paragraph in a specific section “limitations of the study”:

Please see L397-406: Some patient categories were not included in the present review, although muscle stretching is commonly indicated in their clinical care to reduce spasticity⁸². This is for example the case for children with cerebral palsy⁸³. In fact, we were able to identify studies in the literature focusing on the effects of stretching on gait in this population during the first phase of the present review, but the protocol of these studies combined stretching with another form of training (e.g.^84,85) or there was no control group (e.g.⁸⁶). These studies therefore did not fit with the inclusion criteria of the present systematic review and were consequently excluded. Now, it should be stressed that the effectiveness of static stretching to improve motor function in children with cerebral palsy is still controversial⁸⁷, although some authors showed that functional stretching exercises may be effective to improve gait⁸⁶. Further randomized controlled trials are needed to explore the impact of stretching on gait in this population.

Best regards
Arnaud Delafontaine
on behalf of all the authors
Reviewer 1 :

Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. In young adults, two studies by Johanson are reported. Is it not clear if both groups of young adults with limited range of motion were identical in both studies and had the same characteristics? If yes, merging the two studies should make the deal, if not please provide specification about the second group.The participants in both studies were different. In the study of Johanson et al. (2006), the participants were healthy adults with limited passive ankle-dorsiflexion range of motion (less than 8 degrees) and a history of lower limb overuse injury. In the study Johanson et al. (2009), the characteristics of the stretching program were the same as in Joahnson et al. (2006), but the participants did not have any history of lower limb overuse injury.

Reply: To make this difference clearer, precisions were added in the “included studies” and “results” sections:
Please see L158-163 Thus, 12 articles were ultimately included in this systematic review. Six studies evaluated the effects of stretching in healthy older adults ^23,51–55, one in a frail elderly population ⁵⁶, one study in an elderly population with stable symptomatic peripheral artery disease⁵⁷, one in stroke patients ⁵⁸, one study in adults with limited ankle range of motion (less than 8 degrees) associated with a history of lower limb overuse injury ⁵⁹, one study in healthy adults with limited ankle dorsiflexion range of motion (less than 5 degrees) ⁶⁰ and one in healthy young adults ⁶¹

Please see L285-288: “The study of Johanson et al. (2006) examined the effects of stretching on healthy adults with limited passive ankle-dorsiflexion range of motion (less than 8 degrees) and a history of lower limb overuse injury⁵⁰. Regarding the characteristics of the subjects, 19 subjects were included and the mean age was 30.3±9.8 years.”

Please see L302-306: “The study of Johanson et al. (2009) examined the effects of stretching on young adults with limited passive ankle-dorsiflexion range of motion (less than 5 degrees) ⁵¹. It is worth noticed that these participants were not the same than in the study of Johanson et al. (2006). In contrast, the characteristics of the training programs were the same as in Johanson et al. (2006)”.

Comment 2. In the results and the discussion, grouping the types of parameters according to their role in the process of walking would add value to this manuscript. The effects, demonstrated or not, have not all the same meaning depending on whether functional parameters or kinematics angles or even muscle strength and activity are considered.

Reply: In the results and the discussion, we chose to group the participants by patient categories because differences in ages and health parameters may result in different training effects. However, in each patient category, each variable was considered separately in an organized way.

Comment 3. Gait should be defined in a better way, especially how it is related to the different measures in terms of processes, even if there is anyway no real benefit demonstrated by stretching used as a unique therapy.

Reply: We agree. We add a whole paragraph at the beginning of the introduction section to specify how gait can be related to the different variables seen in the review:

Please see L35-44: “Gait is the medical term used to describe the human whole body movement of walking¹. Gait involves internal and external forces that act on the body to move the center of mass (COM) across a given distance². It depends on many biomechanical features that can be observed during gait analysis such as center of mass shifts, joint range of motion, forces, muscle activity, joint moments, and joint powers³. Spatiotemporal features (e.g. velocity, step length, stride length, step with, step variability) and kinematics parameters (range of motion) can be observed subjectively with functional evaluations by clinicians(e.g. the Tinetti test⁴ or the timed up and go test⁵), but, it can be further objectified with biomechanical analysis in a laboratory². Kinetics variables (the forces that cause the body to move) must be collected in a laboratory environment with force plates (e.g.^6–9 for recent studies that used this technic)”.

Comment 4. Surprisingly, no article in children with cerebral palsy has been uncovered, while the clinical care of these children is mostly based on muscle stretching.

Reply: We agree. However, no article in children with cerebral palsy fitted our inclusion criteria during the systematic search of the literature. We add a whole paragraph in a specific section “limitations of the study”:

Please see L397-406: Some patient categories were not included in the present review, although muscle stretching is commonly indicated in their clinical care to reduce spasticity⁸². This is for example the case for children with cerebral palsy⁸³. In fact, we were able to identify studies in the literature focusing on the effects of stretching on gait in this population during the first phase of the present review, but the protocol of these studies combined stretching with another form of training (e.g.^84,85) or there was no control group (e.g.⁸⁶). These studies therefore did not fit with the inclusion criteria of the present systematic review and were consequently excluded. Now, it should be stressed that the effectiveness of static stretching to improve motor function in children with cerebral palsy is still controversial⁸⁷, although some authors showed that functional stretching exercises may be effective to improve gait⁸⁶. Further randomized controlled trials are needed to explore the impact of stretching on gait in this population.

Best regards
Arnaud Delafontaine
on behalf of all the authors
Competing Interests: None Close
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COMMENTS ON THIS REPORT

Author Response 30 Oct 2020

ARNAUD DELAFONTAINE, CIAMS, Université d'Orléans, Orléans, 45067, France

30 Oct 2020

Author Response

Reviewer 1 :

Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. In young adults, two studies by Johanson are ... Continue reading Reviewer 1 :

Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. In young adults, two studies by Johanson are reported. Is it not clear if both groups of young adults with limited range of motion were identical in both studies and had the same characteristics? If yes, merging the two studies should make the deal, if not please provide specification about the second group.The participants in both studies were different. In the study of Johanson et al. (2006), the participants were healthy adults with limited passive ankle-dorsiflexion range of motion (less than 8 degrees) and a history of lower limb overuse injury. In the study Johanson et al. (2009), the characteristics of the stretching program were the same as in Joahnson et al. (2006), but the participants did not have any history of lower limb overuse injury.

Reply: To make this difference clearer, precisions were added in the “included studies” and “results” sections:
Please see L158-163 Thus, 12 articles were ultimately included in this systematic review. Six studies evaluated the effects of stretching in healthy older adults ^23,51–55, one in a frail elderly population ⁵⁶, one study in an elderly population with stable symptomatic peripheral artery disease⁵⁷, one in stroke patients ⁵⁸, one study in adults with limited ankle range of motion (less than 8 degrees) associated with a history of lower limb overuse injury ⁵⁹, one study in healthy adults with limited ankle dorsiflexion range of motion (less than 5 degrees) ⁶⁰ and one in healthy young adults ⁶¹

Please see L285-288: “The study of Johanson et al. (2006) examined the effects of stretching on healthy adults with limited passive ankle-dorsiflexion range of motion (less than 8 degrees) and a history of lower limb overuse injury⁵⁰. Regarding the characteristics of the subjects, 19 subjects were included and the mean age was 30.3±9.8 years.”

Please see L302-306: “The study of Johanson et al. (2009) examined the effects of stretching on young adults with limited passive ankle-dorsiflexion range of motion (less than 5 degrees) ⁵¹. It is worth noticed that these participants were not the same than in the study of Johanson et al. (2006). In contrast, the characteristics of the training programs were the same as in Johanson et al. (2006)”.

Comment 2. In the results and the discussion, grouping the types of parameters according to their role in the process of walking would add value to this manuscript. The effects, demonstrated or not, have not all the same meaning depending on whether functional parameters or kinematics angles or even muscle strength and activity are considered.

Reply: In the results and the discussion, we chose to group the participants by patient categories because differences in ages and health parameters may result in different training effects. However, in each patient category, each variable was considered separately in an organized way.

Comment 3. Gait should be defined in a better way, especially how it is related to the different measures in terms of processes, even if there is anyway no real benefit demonstrated by stretching used as a unique therapy.

Reply: We agree. We add a whole paragraph at the beginning of the introduction section to specify how gait can be related to the different variables seen in the review:

Please see L35-44: “Gait is the medical term used to describe the human whole body movement of walking¹. Gait involves internal and external forces that act on the body to move the center of mass (COM) across a given distance². It depends on many biomechanical features that can be observed during gait analysis such as center of mass shifts, joint range of motion, forces, muscle activity, joint moments, and joint powers³. Spatiotemporal features (e.g. velocity, step length, stride length, step with, step variability) and kinematics parameters (range of motion) can be observed subjectively with functional evaluations by clinicians(e.g. the Tinetti test⁴ or the timed up and go test⁵), but, it can be further objectified with biomechanical analysis in a laboratory². Kinetics variables (the forces that cause the body to move) must be collected in a laboratory environment with force plates (e.g.^6–9 for recent studies that used this technic)”.

Comment 4. Surprisingly, no article in children with cerebral palsy has been uncovered, while the clinical care of these children is mostly based on muscle stretching.

Reply: We agree. However, no article in children with cerebral palsy fitted our inclusion criteria during the systematic search of the literature. We add a whole paragraph in a specific section “limitations of the study”:

Please see L397-406: Some patient categories were not included in the present review, although muscle stretching is commonly indicated in their clinical care to reduce spasticity⁸². This is for example the case for children with cerebral palsy⁸³. In fact, we were able to identify studies in the literature focusing on the effects of stretching on gait in this population during the first phase of the present review, but the protocol of these studies combined stretching with another form of training (e.g.^84,85) or there was no control group (e.g.⁸⁶). These studies therefore did not fit with the inclusion criteria of the present systematic review and were consequently excluded. Now, it should be stressed that the effectiveness of static stretching to improve motor function in children with cerebral palsy is still controversial⁸⁷, although some authors showed that functional stretching exercises may be effective to improve gait⁸⁶. Further randomized controlled trials are needed to explore the impact of stretching on gait in this population.

Best regards
Arnaud Delafontaine
on behalf of all the authors
Reviewer 1 :

Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. In young adults, two studies by Johanson are reported. Is it not clear if both groups of young adults with limited range of motion were identical in both studies and had the same characteristics? If yes, merging the two studies should make the deal, if not please provide specification about the second group.The participants in both studies were different. In the study of Johanson et al. (2006), the participants were healthy adults with limited passive ankle-dorsiflexion range of motion (less than 8 degrees) and a history of lower limb overuse injury. In the study Johanson et al. (2009), the characteristics of the stretching program were the same as in Joahnson et al. (2006), but the participants did not have any history of lower limb overuse injury.

Reply: To make this difference clearer, precisions were added in the “included studies” and “results” sections:
Please see L158-163 Thus, 12 articles were ultimately included in this systematic review. Six studies evaluated the effects of stretching in healthy older adults ^23,51–55, one in a frail elderly population ⁵⁶, one study in an elderly population with stable symptomatic peripheral artery disease⁵⁷, one in stroke patients ⁵⁸, one study in adults with limited ankle range of motion (less than 8 degrees) associated with a history of lower limb overuse injury ⁵⁹, one study in healthy adults with limited ankle dorsiflexion range of motion (less than 5 degrees) ⁶⁰ and one in healthy young adults ⁶¹

Please see L285-288: “The study of Johanson et al. (2006) examined the effects of stretching on healthy adults with limited passive ankle-dorsiflexion range of motion (less than 8 degrees) and a history of lower limb overuse injury⁵⁰. Regarding the characteristics of the subjects, 19 subjects were included and the mean age was 30.3±9.8 years.”

Please see L302-306: “The study of Johanson et al. (2009) examined the effects of stretching on young adults with limited passive ankle-dorsiflexion range of motion (less than 5 degrees) ⁵¹. It is worth noticed that these participants were not the same than in the study of Johanson et al. (2006). In contrast, the characteristics of the training programs were the same as in Johanson et al. (2006)”.

Comment 2. In the results and the discussion, grouping the types of parameters according to their role in the process of walking would add value to this manuscript. The effects, demonstrated or not, have not all the same meaning depending on whether functional parameters or kinematics angles or even muscle strength and activity are considered.

Reply: In the results and the discussion, we chose to group the participants by patient categories because differences in ages and health parameters may result in different training effects. However, in each patient category, each variable was considered separately in an organized way.

Comment 3. Gait should be defined in a better way, especially how it is related to the different measures in terms of processes, even if there is anyway no real benefit demonstrated by stretching used as a unique therapy.

Reply: We agree. We add a whole paragraph at the beginning of the introduction section to specify how gait can be related to the different variables seen in the review:

Please see L35-44: “Gait is the medical term used to describe the human whole body movement of walking¹. Gait involves internal and external forces that act on the body to move the center of mass (COM) across a given distance². It depends on many biomechanical features that can be observed during gait analysis such as center of mass shifts, joint range of motion, forces, muscle activity, joint moments, and joint powers³. Spatiotemporal features (e.g. velocity, step length, stride length, step with, step variability) and kinematics parameters (range of motion) can be observed subjectively with functional evaluations by clinicians(e.g. the Tinetti test⁴ or the timed up and go test⁵), but, it can be further objectified with biomechanical analysis in a laboratory². Kinetics variables (the forces that cause the body to move) must be collected in a laboratory environment with force plates (e.g.^6–9 for recent studies that used this technic)”.

Comment 4. Surprisingly, no article in children with cerebral palsy has been uncovered, while the clinical care of these children is mostly based on muscle stretching.

Reply: We agree. However, no article in children with cerebral palsy fitted our inclusion criteria during the systematic search of the literature. We add a whole paragraph in a specific section “limitations of the study”:

Please see L397-406: Some patient categories were not included in the present review, although muscle stretching is commonly indicated in their clinical care to reduce spasticity⁸². This is for example the case for children with cerebral palsy⁸³. In fact, we were able to identify studies in the literature focusing on the effects of stretching on gait in this population during the first phase of the present review, but the protocol of these studies combined stretching with another form of training (e.g.^84,85) or there was no control group (e.g.⁸⁶). These studies therefore did not fit with the inclusion criteria of the present systematic review and were consequently excluded. Now, it should be stressed that the effectiveness of static stretching to improve motor function in children with cerebral palsy is still controversial⁸⁷, although some authors showed that functional stretching exercises may be effective to improve gait⁸⁶. Further randomized controlled trials are needed to explore the impact of stretching on gait in this population.

Best regards
Arnaud Delafontaine
on behalf of all the authors
Competing Interests: None Close
Report a concern

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VERSION 2 PUBLISHED 13 Aug 2020

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Fabrice Mégrot, Centre de Médecine Physique et de Réadaptation pour Enfants Bois-Larris, Croix-rouge française, Lamorlaye, France; Université de Technologie de Compiègne, Sorbonnes Université, Compiègne, France
Xu Wei, Shanghai Jiao Tong University School of Medicine, Shanghai, China

Guoning Zhang, Shanghai Jiao Tong University School of Medicine, Shanghai, China
Maria Garcia Escudero, School of Medicine and Health Sciencies, Universidad Católica de Valencia San Vicente Mártir, Valencia, Spain

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26 Feb 2021 | for Version 2

Maria Garcia Escudero, School of Medicine and Health Sciencies, Universidad Católica de Valencia San Vicente Mártir, Valencia, Spain

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Approved

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

Yes
Are the conclusions drawn adequately supported by the results presented in the review?

Yes

Competing Interests

No competing interests were disclosed.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

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09 Nov 2020 | for Version 2

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Approved

Thanks for the corrections. That works.

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

motor control, biomechanics, neurosciences, nonlinear dynamics, clinical gait/movement analysis and gross motor function of children with cerebral palsy

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

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23 Views

09 Oct 2020 | for Version 1

Xu Wei, Department of Orthopaedic Surgery, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

Guoning Zhang, Department of Orthopaedic Surgery, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

23 Views Cite this report Responses(1)

Approved With Reservations

The purpose of this article is to analyse the effects of a stretching program on gait in each patient category by means of a systematic literature review and meta-analysis, comparing the gait outcomes of the intervention groups with the control groups. This is a very interesting research direction and it has good innovation. But different ages and diseases have different gait results and different stretching training modes and intervention methods. How to eliminate the bias caused by these differences in meta-analysis and comparison?
Four meta-analysis were conducted for the following outcomes (Figure 2): gait speed, stride length, hip extension during gait and anterior pelvic tilt. Why choose these four dimensions? Is there any theoretical basis?
Kinetic variables: The study of Kerrigan et al. (2003)44 showed no significant difference between groups for hip torque (SMD= 0.35; 95% CI: -0.06, 0.75) and ankle plantar flexion power (SMD=0.00; 95% CI: -0.40, 0.40), with a moderate level of confidence (PEDro score: 6/10).: It seems that gait analysis cannot directly measure muscle power. sEMG can only evaluate muscle recruitment signals to evaluate muscle fiber contraction. Therefore, how is ankle flexion power measured by gait analysis?
Twelve studies were included in the analysis. Stretching improved gait performance as assessed by walking speed and stride length only in a study with a frail elderly population, with small effect sizes. There is no strong evidence supporting the beneficial effect of using stretching to improve gait. I think that since stretching can improve gait parameters for adults with special weakness, the effect of stretching on gait is significant, although it has little effect on healthy adults or young adults. Should it be explained? In general, this study made a meta-analysis on the effect of stretching on gait, which has good innovation. However, whether gait analysis has guiding significance for different groups of rehabilitation training is still controversial especially for healthy adults, so the research conclusion of this paper has practical significance in clinical guidance.

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

Partly
Are the conclusions drawn adequately supported by the results presented in the review?

Partly

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Sports medicine; osteoporosis; osteosarcoma; Spine surgery; Scoliosis

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30 Oct 2020

ARNAUD DELAFONTAINE, CIAMS, Université d'Orléans, Orléans, 45067, France

Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. Different ages and diseases have different gait results and different stretching training modes and intervention methods. How to eliminate the bias caused by these differences in meta-analysis and comparison?

Reply: We add some precisions in the discussion section (healthy older adults paragraph) to specify how we have limited the risk of bias:
Please see L353-366: When data were meta-analyzed, we ensured that the groups and the training characteristics were similar to limit the risk of bias. This explains that a limited number of studies was included in the meta-analysis. It is worth noticing that the stretching technic was the same (i.e. static stretching), but that details of interventions varied across these studies. For example, both studies selected for the meta-analysis of gait speed included hip flexors and plantar flexors stretching, but, one study included hip extensor stretching⁵² whereas the other did not⁵¹. This difference may partially explain the heterogenous results in the meta-analysis (I²=86%, p=0.007). In the same way, the heterogenous results observed in the meta-analysis of anterior pelvic tilt (I²=87%, p<0.01) may be explained by the stretching of additional muscle groups (hip extensors and plantar flexors) in the study of Cristopoliski et al. (2009) compared to the other studies (in which only hip flexors were stretched)^53,55. Nevertheless, heterogeneity in the results was not systematically observed between studies that used slight different protocols, as showed by the consistent results in the meta-analyses of stride length (I²=59%, p=0.12) and hip extension (I²=0%, p=0.99). Thus, we assume that we have limited the risk of bias in the meta-analyses.

Comment 2. Four meta-analysis were conducted for the following outcomes (Figure 2): gait speed, stride length, hip extension during gait and anterior pelvic tilt. Why choose these four dimensions? Is there any theoretical basis?

Reply: Only these four outcomes fitted with the inclusion criteria for meta-analysis. Meta-analyses were performed only when more than one trial was identified for each outcome. Additionally, to reduce the risk of bias, we ensured that the groups were similar. For example, in the study of Watt et al. (2011), the intervention group had a significantly higher gait speed than the control group, so the trial was excluded of the meta-analysis.

Comment 3. Kinetic variables: The study of Kerrigan et al. (2003)44 showed no significant difference between groups for hip torque (SMD= 0.35; 95% CI: -0.06, 0.75) and ankle plantar flexion power (SMD=0.00; 95% CI: -0.40, 0.40), with a moderate level of confidence (PEDro score: 6/10).: It seems that gait analysis cannot directly measure muscle power. sEMG can only evaluate muscle recruitment signals to evaluate muscle fiber contraction. Therefore, how is ankle flexion power measured by gait analysis?

Reply: In the study of Kerrigan et al. (2003), “joint torque and power calculations were based on the mass and inertial characteristics of each lower-extremity segment, the derived linear and angular velocities and accelerations of each lower-extremity segment, and the ground reaction force and joint center position estimates. Joint torques and powers were normalized for body weight and height and were reported as external in newton meters per kilogram meters (N.m/kg.m) and watts per kilogram meters (W/kg.m), respectively”.
Unless special recommendation of the reviewer or the Editor, we feel it is not necessary to add how the ankle flexion power was measured in the study of Kerrigan et al. (2003).

Comment 4. I think that since stretching can improve gait parameters for adults with special weakness, the effect of stretching on gait is significant, although it has little effect on healthy adults or young adults. Should it be explained?

Reply: We add some precisions in the discussion section (young adults paragraph) to specify why stretching is less interesting to improve gait parameters in young healthy adults:

Please see L387-390: In healthy adults, the interest of practicing stretching to improve gait seems limited as they are assumed to have sufficient mobility for walking. Moreover, the included study involved athletic males ⁶¹, a population that is known to be more flexible than inactive persons ⁸¹. Stretching should be more indicated when range of motion is limited²⁴.

Best regards
Arnaud Delafontaine
on behalf of all the authors

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14 Sep 2020 | for Version 1

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Approved With Reservations

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

Yes
Are the conclusions drawn adequately supported by the results presented in the review?

Partly

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

motor control, biomechanics, neurosciences, nonlinear dynamics, clinical gait/movement analysis and gross motor function of children with cerebral palsy

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Responses (1)

Author Response

30 Oct 2020

ARNAUD DELAFONTAINE, CIAMS, Université d'Orléans, Orléans, 45067, France

Reviewer 1 :

Dear Reviewer
We greatly you for scrutinizing our manuscript and for his relevant comments. We feel that the manuscript has improved.

Comment 1. In young adults, two studies by Johanson are reported. Is it not clear if both groups of young adults with limited range of motion were identical in both studies and had the same characteristics? If yes, merging the two studies should make the deal, if not please provide specification about the second group.The participants in both studies were different. In the study of Johanson et al. (2006), the participants were healthy adults with limited passive ankle-dorsiflexion range of motion (less than 8 degrees) and a history of lower limb overuse injury. In the study Johanson et al. (2009), the characteristics of the stretching program were the same as in Joahnson et al. (2006), but the participants did not have any history of lower limb overuse injury.

Reply: To make this difference clearer, precisions were added in the “included studies” and “results” sections:
Please see L158-163 Thus, 12 articles were ultimately included in this systematic review. Six studies evaluated the effects of stretching in healthy older adults ^23,51–55, one in a frail elderly population ⁵⁶, one study in an elderly population with stable symptomatic peripheral artery disease⁵⁷, one in stroke patients ⁵⁸, one study in adults with limited ankle range of motion (less than 8 degrees) associated with a history of lower limb overuse injury ⁵⁹, one study in healthy adults with limited ankle dorsiflexion range of motion (less than 5 degrees) ⁶⁰ and one in healthy young adults ⁶¹

Please see L285-288: “The study of Johanson et al. (2006) examined the effects of stretching on healthy adults with limited passive ankle-dorsiflexion range of motion (less than 8 degrees) and a history of lower limb overuse injury⁵⁰. Regarding the characteristics of the subjects, 19 subjects were included and the mean age was 30.3±9.8 years.”

Please see L302-306: “The study of Johanson et al. (2009) examined the effects of stretching on young adults with limited passive ankle-dorsiflexion range of motion (less than 5 degrees) ⁵¹. It is worth noticed that these participants were not the same than in the study of Johanson et al. (2006). In contrast, the characteristics of the training programs were the same as in Johanson et al. (2006)”.

Comment 2. In the results and the discussion, grouping the types of parameters according to their role in the process of walking would add value to this manuscript. The effects, demonstrated or not, have not all the same meaning depending on whether functional parameters or kinematics angles or even muscle strength and activity are considered.

Reply: In the results and the discussion, we chose to group the participants by patient categories because differences in ages and health parameters may result in different training effects. However, in each patient category, each variable was considered separately in an organized way.

Comment 3. Gait should be defined in a better way, especially how it is related to the different measures in terms of processes, even if there is anyway no real benefit demonstrated by stretching used as a unique therapy.

Reply: We agree. We add a whole paragraph at the beginning of the introduction section to specify how gait can be related to the different variables seen in the review:

Please see L35-44: “Gait is the medical term used to describe the human whole body movement of walking¹. Gait involves internal and external forces that act on the body to move the center of mass (COM) across a given distance². It depends on many biomechanical features that can be observed during gait analysis such as center of mass shifts, joint range of motion, forces, muscle activity, joint moments, and joint powers³. Spatiotemporal features (e.g. velocity, step length, stride length, step with, step variability) and kinematics parameters (range of motion) can be observed subjectively with functional evaluations by clinicians(e.g. the Tinetti test⁴ or the timed up and go test⁵), but, it can be further objectified with biomechanical analysis in a laboratory². Kinetics variables (the forces that cause the body to move) must be collected in a laboratory environment with force plates (e.g.^6–9 for recent studies that used this technic)”.

Comment 4. Surprisingly, no article in children with cerebral palsy has been uncovered, while the clinical care of these children is mostly based on muscle stretching.

Reply: We agree. However, no article in children with cerebral palsy fitted our inclusion criteria during the systematic search of the literature. We add a whole paragraph in a specific section “limitations of the study”:

Please see L397-406: Some patient categories were not included in the present review, although muscle stretching is commonly indicated in their clinical care to reduce spasticity⁸². This is for example the case for children with cerebral palsy⁸³. In fact, we were able to identify studies in the literature focusing on the effects of stretching on gait in this population during the first phase of the present review, but the protocol of these studies combined stretching with another form of training (e.g.^84,85) or there was no control group (e.g.⁸⁶). These studies therefore did not fit with the inclusion criteria of the present systematic review and were consequently excluded. Now, it should be stressed that the effectiveness of static stretching to improve motor function in children with cerebral palsy is still controversial⁸⁷, although some authors showed that functional stretching exercises may be effective to improve gait⁸⁶. Further randomized controlled trials are needed to explore the impact of stretching on gait in this population.

Best regards
Arnaud Delafontaine
on behalf of all the authors

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Competing Interests

None

Alongside their report, reviewers assign a status to the article:

Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested

Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.

Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions

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Effects of stretching exercises on human gait: a systematic review and meta-analysis

Abstract

Keywords

Revised Amendments from Version 1

Introduction

Methods

Design and literature screening

Inclusion and exclusion criteria

Data extraction and main measurements examined

Quality and risk of bias assessment

Statistical analysis

Level of evidence

Results

Included studies

Figure 1. PRISMA flow chart of study selection process.

Table 1. Summary of the included studies.

Table 2. Quality assessment of the included studies.

Results in different patient categories

Figure 2.

Discussion

Healthy older adults

Stroke patients

Young adults

Limitations of the study

Conclusion

Data availability

Underlying data

Reporting guidelines

References

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