https://orcid.org/0000-0002-9286-6711
Figures
Abstract
Objective
Equinus foot deformity (EFD) is the most common deviation after stroke. Several physiotherapy interventions have been suggested to treat it. However, studies evaluating the efficacy of these treatments vary widely in terms of assessment modalities, type of data analysis, and nomenclature. This scoping review aimed to map current available evidence on outcome measures and the modalities employed to assess the effectiveness of physiotherapy programs for the reduction of triceps surae (TS) spasticity and EFD in patients with stroke.
Methods
Scoping review methodological frameworks have been used. Three databases were investigated. Primary literature addressing TS spasticity in adult patients with stroke using physiotherapy interventions was included. Findings were systematically summarized in tables according to the intervention used, intervention dosage, control group, clinical, and instrumental outcome measures.
Results
Of the 642 retrieved studies, 53 papers were included. TS spasticity was assessed by manual maneuvers performed by clinicians (mainly using the Ashworth Scale), functional tests, mechanical evaluation through robotic devices, or instrumental analysis and imaging (such as the torque-angle ratio, the H-reflex, and ultrasound images). A thorough critical appraisal of the construct validity of the scales and of the statistics employed was provided, particularly focusing on the choice of parametric and non-parametric approaches when using ordinal scales. Finally, the complexity surrounding the concept of “spasticity” and the possibility of assessing the several underlying active and passive causes of EFD, with a consequent bespoke treatment for each of them, was discussed.
Conclusion
This scoping review provides a comprehensive description of all outcome measures and assessment modalities used in literature to assess the effectiveness of physiotherapy treatments, when used for the reduction of TS spasticity and EFD in patients with stroke. Clinicians and researchers can find an easy-to-consult summary that can support both their clinical and research activities.
Citation: Campanini I, Bò MC, Bassi MC, Damiano B, Scaltriti S, Lusuardi M, et al. (2023) Outcome measures for assessing the effectiveness of physiotherapy interventions on equinus foot deformity in post-stroke patients with triceps surae spasticity: A scoping review. PLoS ONE 18(10): e0287220. https://doi.org/10.1371/journal.pone.0287220
Editor: Donald L. Hoover, Western Michigan University, UNITED STATES
Received: November 17, 2022; Accepted: June 1, 2023; Published: October 12, 2023
Copyright: © 2023 Campanini 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 author and source are credited.
Data Availability: All relevant data are within the paper.
Funding: The submission of this study was funded by the Azienda USL-IRCCS of Reggio Emilia, where the authors work. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Authors MBò and AM were also employed by Merlo Bioengineering but this has not interfered with the paper writing. This does not alter our adherence to PLOS ONE policies on sharing data and materials.
Competing interests: Authors MBò and AM were also employed by Merlo Bioengineering but this has not interfered with the paper writing. This does not alter our adherence to PLOS ONE policies on sharing data and materials.
1 Introduction
In adult patients, the equinus foot deviation (EFD) is one of the most common acquired deformities of the lower limb following a stroke. The ankle is positioned in a plantarflexed stance, and it is also usually associated with supination of the foot leading to the equinovarus deviation (EVFD). Clawed toes can also be present [1]. EFD could be due to multiple factors, including paresis of the dorsiflexor muscles, plantarflexor muscles overactivity, stiffness, viscosity and contracture [1].
Cerebrovascular accidents can have several sequelae involving different functions. They often lead to cognitive impairments, sensory loss, difficulty in isolating movements, and increased muscle tone with the onset of pathological synergies [2]. EFD has considerable impacts on gait, balance, and safety. EFD is the most frequent acquired lower limb deformity in the population with stroke, and directly affects walking ability. It might alter both the stability of the foot-ankle complex during the stance phase of gait and the ability of foot clearance during the swing phase [3]. Given the resulting pain, instability, and increased risk of falls, patients often need supervision and different levels of assistance during their outings, depending on the degree of the impairment. This reduces the odds of a successful return to social and working activities and requires an outflow of resources to remain in the community [4], affecting patients’ and caregivers’ quality of life [5,6] and increasing the economic burden for health care systems [7].
In literature, several treatments have been suggested for the management of spasticity-related EFD in patients with stroke. Conservative interventions include botulinum toxin injections, focal inhibition, oral or intrathecal medications, serial casting or orthosis, and physiotherapy (PT) [8]. Surgery is performed by neuro-orthopedic surgeons when chronic deformities develop [3,9].
Recent studies have focused on many PT treatments of triceps surae (TS) spasticity following stroke [5,8,10–14]. These include stretching, shock waves, electrostimulation, dry-needling, transcutaneous electrical nerve stimulation, vibrations, ultrasound, cryotherapy, and physiotherapist-guided physical exercising. On the one hand, some of these treatments, such as shock waves, dry needling, and electrical stimulation, showed similar promising results. On the other hand, when analyzing these studies, at least two weak points can be identified [14]. Firstly, the countless modalities used for the assessment of spasticity in EVFD prevent direct comparisons of the results. Secondly, the type of statistical analysis chosen is often incorrect when dealing with clinical scales, since parametric statistics (e.g., mean value and t-test) cannot be used when analyzing ordinal scores.
Given the variety of outcome measures and data analysis procedures used in the studies on PT interventions, which aim to reduce triceps surae (TS) impairment in patients with stroke, a scoping review was the study design that best fitted our needs. Scoping reviews are employed to map available literature on a novel, wide-ranging topic, to examine how research is conducted, highlighting any present gaps, and steering the scientific community towards filling these gaps [15].
In this study, a scoping review was performed to analyze current available evidence pertaining to PT interventions used with adult patients with stroke and relieve at least one of the causes underlying EFD. The focus was kept on the evaluation methods used by the authors to separately assess the various components that could be the underlying cause of EFD and on the methodological procedures used for data analysis. In this scoping review, clinicians and researchers can find an easy-to-consult summary on the methods used to assess PT interventions on EFD. Suggestions to improve everyday practice when dealing with clinical data have been provided to support further studies.
2 Methods
The methodology used for this scoping review is described by Tricco et al. [16] and is an extension of PRISMA statement for systematic reviews [17]. It consists of five stages, as described below.
2.1 Stage 1: Identifying the research question
The leading question for this investigation was: Which are the evaluation methods employed in literature to assess the effectiveness of PT interventions in patients with stroke with TS spasticity and EFD?
2.2 Stage 2: Identifying relevant studies
Comprehensive and systematic searches were developed by two researchers and a scientific librarian. The research was conducted in May 2021 with the following databases: Medline, Cinahl, and Cochrane. No time limitations were set and only articles published in English or Italian were considered eligible.
Keywords searched included “equinus deformity”, “stroke”, “physiotherapy”, “rehabilitation”, “extracorporeal shock waves”, “dry needling”, “stretching”, “ultrasound”, “vibration”, “tens”, “electric stimulation”, “muscle spasticity”, “spastic paresis”. When available, Medical Subjects Headings (MeSH) were included to ensure consistency of search terms. The complete search strategies can be consulted in Table 1. Additional papers were included by hand searching, retrieving them from bibliography of other studies.
2.3 Stage 3: Selecting studies
The eligibility criteria were set according to the PICO framework [18], as reported in Table 2.
2.4 Stage 4: Charting the data
Relevant titles and abstracts were screened according to the inclusion and exclusion criteria and full text papers were independently evaluated by two reviewers (IC and MCBO, two licensed PTs). When a consensus was not reached, a third researcher (AM) resolved any discrepancy.
2.5 Stage 5: Summarizing and reporting the data
Relevant data were extracted from papers and collected in a pre-defined Excel form (including first author, year of publication, intervention type, outcome measure, etc.) [19,20]. The form was updated once during the data extraction process to maximize the accuracy of this study, in line with the methodology for scoping reviews [20]. Data were finally collected in tables and classified by author and year of publication, intervention types and clinical and instrumental outcome measures. Findings were presented in a narrative synthesis, grouped by type of intervention.
3 Results
The search led to the identification of 778 articles and 642 papers remained after removing all duplicates. Of these, 61 papers were selected for full-text screening based on the title and abstract and 36 were included in the scoping review. In addition, 17 studies were identified by hand searching and were later included, for a total of 53 studies. The flow chart in Fig 1 follows the PRISMA guidelines [17].
The selected papers were published between 2001 and 2020, with samples ranging from 1 to 83 adult patients with EFD and TS spasticity following stroke. Thirty-two of the included studies were randomized controlled trials (RCTs), while the remaining had study designs without randomization or controls.
The rationale followed by authors in delivering one treatment over another was that each author could intervene on different factors causing EFD (e.g., either active, reflex or passive). Details of the components addressed by the included studies as stated by authors are presented in Table 3.
3.1 Stretching
Twelve studies used stretching maneuvers. Two of them were RCTs. Their characteristics can be seen in Table 4.
The effect of stretching on EVD was assessed both by clinical and instrumental measures. Six studies measured passive range of motion (ROM) [22,25,26,28,30,73]. The Modified Ashworth Scale (MAS) was employed in three of them [22,26,73], while Pradines and colleagues used the Tardieu Angle [21,23]. The remaining seven papers used instrumental measures as the primary outcome for the quantification of spasticity or stiffness, such as the H/M ratio (i.e., the ratio between the maximum amplitude of H-wave and M-wave) [24], the Achilles Tendon Reflex Excitability [22,25], kinematic data extracted by gait analysis [31] or the torque-angle ratio [27–30].
3.2 Shock waves
The effect of shock waves on TS spasticity was the main topic in nine studies. Study characteristics can be viewed in Table 5. Four were RCTs. Eight out of nine studies used MAS or its subsequent versions, [32–37,39,40]. Wu and colleagues assessed TS spasticity using the Tardieu Angle [36]. Other frequently used clinical measurements were active and passive ankle ROM and gait velocity retrieved from different functional tests. Only Sawan’s group employed an instrumental outcome measure—the H/M ratio—as the primary outcome for spasticity quantification [38]. Almost all studies used instrumental evaluations as secondary outcomes.
3.3 Electrical stimulation
Seven studies employed electrical stimulation to treat spasticity and lack of strength in patients with stroke with EFD. Six were RCTs. Study characteristics are presented in Table 6.
To assess spasticity all trials used MAS or its subsequent versions [41–47]. Other clinical outcome measures were ROM, muscle strength, gait performance scores (Timed Up and Go, modified Emory Functional Ambulation Profile, 10-Metre Ambulation Speed), and stability scores (Berg Balance Scale, Fugl-Meyer Assessment, Gait Dynamic Index).
Three studies also included instrumental measures. Yang and Colleagues used dynamic electromyography during gait analysis to measure TS activity during walking [42]. The remaining two studies measured the H-reflex and other neurophysiological parameters [46,47].
3.4 Dry needling
Six studies performed dry needling to treat either the passive or active components of EFD in patients with stroke. Four were RCTs. Their characteristics can be seen in Table 7.
MAS score was the main clinical outcome measure for assessing the effects of the intervention in five out of six papers [48–50,52,53], while Calvo and colleagues used an instrumental measure called Maximal Radial Muscle Displacement which is computed by tensiomyography [51]. Secondary clinical measures included functional performance scales (Timed Up and Go, 10-Meter Walking Test, Fugl-Meyer Assessment, Single Leg Stance). Other instrumental outcomes used by authors were associated to the structural characteristics of muscles (pennation angle, muscle thickness, fascicle length) and to the patients’ static and dynamic stability.
3.5 Transcutaneous electrical nerve stimulation (TENS)
Six studies used TENS to treat spasticity in patients with stroke with EFD. Five were RCTs. Their characteristics can be seen in Table 8.
Four papers performed a clinical evaluation. Two used MAS [55,56], while Yan and Ng, employed another clinical scale called the Composite Spasticity Scale (CSS) [58,59].
The remaining two papers used instrumental neurophysiological measures: H/M ratio, H-reflex latency and the amount of both reciprocal and presynaptic inhibition [54,57]. Moreover, Ng and Cho measured gait velocity and postural stability in dynamic conditions with the aid of instrumented devices [56,59].
3.6 Whole-body vibrations
In six studies, patients with EFD were given whole-body vibration therapy to treat spasticity. Four were RCTs. Their characteristics can be seen in Table 9.
Five out of six studies selected MAS clinical assessment [60,62–65]; other clinical measures employed were gait velocity, stability, and joint ROM.
One study by Huang and colleagues assessed patients using the H/M ratio while standing [61], as primary outcome. Three other authors added instrumental evaluations assessing either the neurophysiological parameters of the reflex arc function (the tendon reflex excitability, the F-waves, or the F/M ratio), or the biomechanical variables (weight distribution under the foot, or muscle power).
3.7 Ultrasound
Five studies employed ultrasound to treat spasticity in patients with EFD. All were RCTs. Their characteristics can be seen in Table 10.
All authors used MAS as the main outcome [33,55,66–68]. Passive ROM was also assessed by all authors, along with several other functional tests. The most frequent instrumental measurement used were H/M ratio or H-reflex latency.
3.8 Cryotherapy
Three studies used cryotherapy. All were RCTs. Their characteristics can be seen in Table 11.
Authors Alcantara and Garcia, chose MAS score as the primary clinical outcome in their studies [69,70]. In their first paper they also investigated the joint position sense of patients (i.e., how patients perceived their joint positions) [70].
When considering instrumental outcomes, Martins and Colleagues set the H/M ratio as their primary measurement, together with H-reflex latency and electromyographic activity of the tibialis anterior during maximum contraction [57]. Alcantara measured muscle strength with an isokinetic dynamometer and performed a gait analysis collecting many parameters, including ankle joint angles [69].
3.9 Physiotherapist-guided physical exercise
Two studies provided physical exercise programs led by physiotherapists. Both were RCTs. Their characteristics can be seen in Table 12.
Both studies assessed TS spasticity with MAS [71,72]. Zhang also performed two functional tests [71]. Again, both works measured muscle activity parameters with instrumental tools: one computed the Maximum Voluntary Isometric Contraction through surface electromyography [71], while the other measured strength with a dynamometer [72].
4 Discussion
4.1 An overview on the main findings
The main purpose of this scoping review was to collect and analyze all evaluation methods used in literature to assess the efficacy of PT interventions for the treatment of EFD due to TS spasticity in patients with stroke. In the manuscripts, all treatments performed by physiotherapists were analyzed. It is worth noting that laws that govern physical therapists’ ability to perform specific treatments (e.g., dry needling) may vary among countries.
Most of the included studies were RCTs, comparing PT interventions to placebo treatments or usual care (see Tables 4–12). Six studies [24,25,27,31,40,62] compared an intervention group with patients with stroke to a control group of healthy subjects. This is a limitation since it does not allow for an appropriate comparison between groups and the only viable analysis to be made is within-group difference only prior to, and after the intervention. The same applies for the eleven studies with a single-arm trial design [23,28,30,34,37,39,49,51,54,60,73]. Four further studies [26,29,38,45] did not randomize participant allocation. This choice could have been made because of clinical feasibility issues. However, this limits the considerations that can be drawn from the findings and, when possible, should be avoided.
4.1.1 Clinical measures of spasticity.
From this scoping review, it emerges that almost all authors stated that their main goal was to reduce TS spasticity (see Table 3). Most of them employed MAS to estimate it. MAS was in fact used in 37 studies out of 53 (69%) of the included studies. Regardless of the therapy administered, almost all authors chose MAS as the main outcome measurement, with the exception of stretching and TENS. MAS was both used as a primary outcome and as an inclusion criterion. In fact, almost all samples of the included studies had to score at least one point at MAS to be considered eligible. Since MAS measures an overall increase in tone, this could have led to the inclusion of patients with EFD only due to TS retraction, instead of TS spasticity [74–77]. Because EFD can have several underlying potential causes, these patients might not have been sensitive to the treatments provided, especially those focusing solely on the reflex components [78].
Twelve included studies used MAS, citing the works by Bohannon and Smith, who conducted a study in 1986, on a largely heterogeneous sample of neurological patients [79]. Their aim was to increase the inter-assessor reliability of the scale through the introduction of the 1+ score between 1 and 2 levels of the original Ashworth Scale [79]. Nine other papers cited Ghotbi and Ansari’s works, who later derived the Modified-MAS by removing once more the 1+ score [80,81]. Both references are quite outdated. We believe that most authors used those references out of habit, as confirmed by further five studies that assessed spasticity with MAS without even justifying its use. However, a careful analysis could highlight the methodological shortcomings of the studies that developed these assessment scales. In fact, since the 1990s, the scientific community began questioning the use of MAS as an appropriate scale for measuring spasticity, suggesting the presence of a cultural bias that sometimes seems to persist even today [74]. Despite providing satisfactory repeatability among assessors, thanks to the development of the modified versions [82], MAS still fails in terms of construct validity on larger muscles (e.g., TS muscle) [74,83], because of its complex outcome measurements that do not solely quantify spasticity, but an overall resistance to passive movement–otherwise known as muscle tone [84].
Given the limits of MAS, there is a need for alternative clinical scales. The Tardieu Scale and the Tardieu Angle have good construct validity [85,86]. These outcome measures try to isolate spasticity, according to its definition of a velocity-dependent response to phasic stretch [78,87]. The Tardieu Angle is used to identify a brake caused by passive resistance or by spasticity by performing two stretch maneuvers as slowly and as quickly as possible. The difference between the two angles is called Tardieu Angle and it measures how much spasticity contributes to ROM limitation [88]. Despite its good construct validity, only three studies, included in our review, used this method. It would be appropriate to increase its employment in future investigations. Li and colleagues analyzed the psychometric properties of MAS and Tardieu Scale in a cohort of patients with stroke and suggested using the latter during the clinical assessment of ankle plantarflexors due to better inter and intra-assessor reliability [89]. Another clinical scale used in two studies was CSS, which ordinally evaluates tendon jerks, resistance to passive stretch, and clonus [90].
The measurement of passive ROM was employed in 24 studies, crosswise for almost all treatments. The methods used for ROM assessment were various: most authors measured it manually, some with the aid of robotic devices or by means of electrical goniometers. ROM assessment at the bedside was not always accurately described among studies, e.g., it was not specified which landmarks were utilized and where the hand goniometer was placed (e.g., medial v. lateral). This might have led to different results. Moreover, some authors did not specify if the evaluation was performed with the knee in a flexed or an extended position, since ROM can greatly differ according to the retraction of the soleus, the gastrocnemius or both muscles of the TS. Finally, some authors measured the whole ROM from maximum plantarflexion to maximum dorsiflexion, according to its definition. Other authors only presented the maximum passive dorsiflexion measured from the neutral position. This discrepancy led to very different raw values among studies. However, improvements in ankle ROM in patients with stroke usually pertain to dorsiflexion measurements alone, so the effect of choosing a different starting point had little value when comparing ROM variations (ΔROM) among studies. It is crucial that future studies write a detailed description of the method used for ROM assessment, to facilitate replicating it and allowing for appropriate meta-analysis.
As outlined by these results, studies have long been emphasizing the need to update spasticity assessment practices for patients who suffered from stroke. The scientific community should foster a debate between experts in the field through topic-specific meetings, such as the Consensus Conferences and the Delphi Panel [91,92]. authors should stop using MAS as the primary outcome of their studies, and journals should similarly refuse studies focused on this outcome. It is now time to transition from outcome measures used out of habit to measures supported by actual evidence.
4.1.2 Methodological considerations on clinical measures.
A critical appraisal on the methodologies used in data analysis was conducted.
A total of 39 studies used MAS (or MMAS or CSS) to assess TS spasticity. Nearly half of these studies correctly reported the median score, provided the range, or reported the number of patients of patients for each level of the scale. Afterwards, non-parametric statistics was used to analyze the data (see Tables 4–12). Conversely, in 48% of the studies, authors incorrectly computed mean values and used the t-test (parametric statistics) to compare groups before and after treatment, as if the scales were numerical. MAS is an ordinal scale, i.e., it scores (0, 1, 1+, 2, 3, and 4). Consequently, numbers could just as easily be replaced by letters (e.g., A, B, C, D, E). For this reason, the score cannot be treated as numbers. In MAS scale, scoring a 2 rather than a 1 does not mean that spasticity has increased twofold. Moreover, a 2-point decrease has a different outcome in terms of spasticity reduction, e.g., from 4 to 2, is not the same as from 2 to 0. Treating MAS scores as numbers is misleading and may lead to unreliable conclusions.
When dealing with ordinal scales, computing differences (e.g., ΔMAS), mean values, and comparing groups by parametric statistics, as the t-test, leads to unreliable results and ought to be avoided. On the one hand, the actual effectiveness of a treatment may be not detected. On the other hand, a statistically significant difference between groups could be a result of treatments that are just as effective. For this reasons, non-parametric statistics must be the only one used for ordinal scales like MAS. The same applies for other functional clinicals scales employed in the included studies (e.g., Berg Balance Scale, Fugl-Meyer Assessment, Lower Extremity Functional Scale, Barthel Index, etc.). This methodological error might appear of little consequence to clinicians. However, it is quite the opposite; it is crucial in scientific research since it invalidates the conclusions of many studies published on this topic. This error was present in 22 out of 53 included studies [22,32,35–37,39,40,42–46,48,53,56,59,65–67,70,72,73]. A common incorrect procedure follows: authors compute ΔMAS and the percentage change after treatment (error #1), compare them with the t-test (error #2) and the statistically significant difference of this test is used to state the superiority of the treatment over the placebo (error #3). The rate of reduction can be greater in the experimental group with respect to that of the control group, but the post-intervention confidence intervals of MAS in the two groups can be overlapping, i.e., invalidating the results since there is no real benefit. To guarantee accuracy, journals ought better to consider the inclusion of an expert in methodology among reviewers when reviewing clinical studies.
4.1.3 The instrumental measures of spasticity.
Thirty-seven studies (69%) included in this current review combined clinical assessment with instrumental evaluation. Most authors chose a neurophysiological evaluation of the reflex arc, such as H-reflex latency or H/M ratio, especially when delivering shock waves and ultrasound. Direct measurement of the stretch reflex by surface EMG has been used in literature both for children with central palsy [93] and survivors from stroke [94] alike. Fewer studies employed gait analysis and dynamic electromyography to assess the effectiveness of their interventions [31,36,42,69,95].
The ultimate goal of rehabilitation is to recover function, including the ability to walk. Future studies should always consider assessing by how much spasticity limits movement not only at the bedside, but also when walking. It is known that a display of overactivity at the bedside does not always imply the presence of overactivity during gait, because fast joint rotation may be absent [1,96,97]. Many authors are supporting this argument, debating the need to integrate different practices to obtain more accurate information about patient condition [98] and to properly assess overactivity both at rest and while moving [1,96,97,99]. Dynamic instrumental assessment should be considered for patients with stroke [1]. On the one hand, it must be recognized that instrumental evaluation requires resources and specific knowledge to be performed correctly [100–104]. On the other hand, the increasing availability of low-cost wearable devices makes it easier to equip rehabilitation wards with these assessment tools. In addition, universities and the scientific community should make an effort to properly train their students since it is necessary to enable rehabilitation professionals to use these techniques and to correctly interpret data [1,84,95,105].
4.1.4 Future challenges.
Few studies included the assessment of stiffness and viscosity, even though these alterations can be present in patients with stroke, along with overactivity [106]. Performing sEMG during gait can help explaining the underlying causes of an alteration in the pattern by differentiating between overactivity and soft tissues modifications. In particular, it would help identifying the main cause in velocity-dependent alterations, between spasticity and increased viscosity, and the main cause in tension-dependent alterations, between spastic dystonia and increased stiffness.
Overlapping patterns from an observational point of view can have completely different causes as described by Campanini et al. [1,105]. The build-up of connective tissue in muscles, as a result of immobilization after a central injury, leads to an increase in muscle stiffness and viscosity [87]. Stiffness and viscosity result in an overall increase in muscle tone. Therefore, with a clinical evaluation, in which the joint is manually mobilized quickly and/or slowly, it is not possible to distinguish when, and how much the response is due to passive and/or reflex components.
In the future, it would be appropriate to routinely introduce sEMG in the clinical assessment to differentiate between the various components of increased muscle tone and consequently choose the appropriate rehabilitation treatment. For example, injection with botulinum toxin can alter the reflex response but not the passive components that are otherwise sensitive to shock waves, dry-needling, stretching, and muscle strengthening [1]. By introducing an integrated evaluation that reveals the underlying causes, it is possible to select a targeted treatment and understand why and when the different treatments reported in literature are effective [3,94,97,107–112].
4.1.5 The issue of taxonomy.
The presence in literature of several assessment modalities is a clear indicator of the complexity of the phenomenon being analyzed. Several authors have recently been debating that the word “spasticity” has been misused as an umbrella term to refer as a combination of different central and peripheral phenomena that must instead be considered separately [84]. We agree with the need to differentiate the individual causes underlying the overall phenomenon of EFD between its active, connective-related, and reflex components (see Table 3) [113]. A revision of taxonomy shared among all professionals, such as what happens in the Delphi Panels or at the Consensus Conferences [91,92], is highly advisable. In this way, unclear terms in literature could be avoided, preventing the use of vague and unspecific assessment measures such as MAS. The adoption of a shared language would enable clinicians to choose the most appropriate scales and/or tools according to their needs, to correctly diagnose a patient, and, finally, to select the most appropriate treatment tailored to the patient’s characteristics [97].
4.2 Limitations
To our knowledge, this is the first scoping review focusing on the assessment methods for PT treatments of the EVFD with TS spasticity in patients with stroke.
The main limitation of the study is that it only included papers that claimed PT to be able to influence TS spasticity. Since the results highlighted the lack of a common and shared taxonomy in the field of neurorehabilitation, some papers might have been missed due to a different terminology adopted by the authors. Moreover, the search focused on patients with stroke since they represent the main population with acquired neurological disorders often presenting alterations to the lower limbs. The eligibility criteria excluded neurological patients with congenital, degenerative or childhood pathologies because the development of structural soft tissue deformities may follow different patterns. For this reason, the considerations drawn in this review may not be relatable to all studies involving neurological patients, although they could provide an equally interesting insight from a methodological point of view.
5 Conclusions
This scoping review summarized all outcome measures and assessment modalities used in literature to assess the effectiveness of PT treatments, when used for the reduction of TS spasticity and EFD in patients with stroke. Clinicians and researchers can find an easy-to-consult synthesis that could be of help to both their clinical and research activities.
The results of this scoping review also highlighted the need to standardize assessment methods employed to evaluate the efficacy of PT interventions on EFD and a gap of knowledge in the appropriate methodology for managing the outcome measures when assessed by ordinal scales. Finally, when PT is the treatment of choice, the use of a shared taxonomy that differentiates the underlying components could lead to identifying the best intervention among those suggested in literature.
Supporting information
S1 Checklist. Preferred Reporting Items for Systematic reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR) checklist.
https://doi.org/10.1371/journal.pone.0287220.s001
(DOCX)
References
- 1. Campanini I, Cosma M, Manca M, Merlo A. Added Value of Dynamic EMG in the Assessment of the Equinus and the Equinovarus Foot Deviation in Stroke Patients and Barriers Limiting Its Usage. Front Neurol. 2020;11(November):1–8. pmid:33329327
- 2. American Stroke Association. Effects of Stroke [Internet]. [cited 2023 Feb 21]. Available from: https://www.stroke.org/en/about-stroke/effects-of-stroke.
- 3. Giannotti E, Merlo A, Zerbinati P, Longhi M, Prati P, Masiero S, et al. Early rehabilitation treatment combined with equinovarus foot deformity surgical correction in stroke patients: safety and changes in gait parameters. Eur J Phys Rehabil Med [Internet]. 2016 Jun;52(3):296–303. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26629841. pmid:26629841
- 4. Ghoshchi SG, de Angelis S, Morone G, Panigazzi M, Persechino B, Tramontano M, et al. Return to work and quality of life after stroke in Italy: A study on the efficacy of technologically assisted neurorehabilitation. Int J Environ Res Public Health. 2020 Jul 2;17(14):1–12.
- 5. Khan F, Amatya B, Bensmail D, Yelnik A. Non-pharmacological interventions for spasticity in adults: An overview of systematic reviews. Ann Phys Rehabil Med. 2019 Jul;62(4):265–73. pmid:29042299
- 6. Naro A, Leo A, Russo M, Casella C, Buda A, Crespantini A, et al. Breakthroughs in the spasticity management: Are non-pharmacological treatments the future? Journal of Clinical Neuroscience. 2017;39:16–27.
- 7. Strilciuc S, Grad DA, Radu C, Chira D, Stan A, Ungureanu M, et al. The economic burden of stroke: a systematic review of cost of illness studies. Vol. 14, Journal of medicine and life. NLM (Medline); 2021. p. 606–19. pmid:35027963
- 8. Bethoux F. Spasticity Management After Stroke. Phys Med Rehabil Clin N Am. 2015;26(4):625–39. pmid:26522902
- 9. Keenan MA, Fuller DA, Whyte J, Mayer N, Esquenazi A, Fidler-Sheppard R. The influence of dynamic polyelectromyography in formulating a surgical plan in treatment of spastic elbow flexion deformity. Arch Phys Med Rehabil. 2003;84(2):291–6. pmid:12601663
- 10. Dymarek R, Ptaszkowski K, Słupska L, Halski T, Taradaj J, Rosińczuk J. Effects of extracorporeal shock wave on upper and lower limb spasticity in post-stroke patients: A narrative review. Top Stroke Rehabil. 2016 Jun 6;23(4):293–303. pmid:27077981
- 11. Xiang J, Wang W, Jiang W, Qian Q. Effects of extracorporeal shock wave therapy on spasticity in post-stroke patients: A systematic review and meta-analysis of randomized controlled trials. J Rehabil Med. 2018 Nov 7;50(10):852–9. pmid:30264850
- 12. Lecharte T, Gross R, Nordez A, Le Sant G. Effect of chronic stretching interventions on the mechanical properties of muscles in patients with stroke: A systematic review. Ann Phys Rehabil Med. 2020 May;63(3):222–9. pmid:31981838
- 13. Mills PB, Dossa F. Transcutaneous Electrical Nerve Stimulation for Management of Limb Spasticity: A Systematic Review. Am J Phys Med Rehabil. 2016;95(4):309–18. pmid:26829077
- 14. Campanini I, Bò MC, Salsi F, Bassi MC, Damiano B, Scaltriti S, et al. Physical therapy interventions for the correction of equinus foot deformity in post-stroke patients with triceps spasticity: A scoping review. Front Neurol [Internet]. 2022 Oct 28;13. Available from: https://www.frontiersin.org/articles/10.3389/fneur.2022.1026850/full. pmid:36388227
- 15. Munn Z, Peters MDJ, Stern C, Tufanaru C, McArthur A, Aromataris E. Systematic review or scoping review? Guidance for authors when choosing between a systematic or scoping review approach. BMC Med Res Methodol [Internet]. 2018 Dec 19;18(1):143. Available from: https://bmcmedresmethodol.biomedcentral.com/articles/10.1186/s12874-018-0611-x. pmid:30453902
- 16. Tricco AC, Lillie E, Zarin W, O’Brien KK, Colquhoun H, Levac D, et al. PRISMA extension for scoping reviews (PRISMA-ScR): Checklist and explanation. Ann Intern Med. 2018;169(7):467–73. pmid:30178033
- 17. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. The BMJ. 2021;372.
- 18. Huang X, Lin J, Demner-Fushman D. Evaluation of PICO as a knowledge representation for clinical questions. AMIA Annu Symp Proc [Internet]. 2006;2006:359–63. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17238363. pmid:17238363
- 19. Büchter RB, Weise A, Pieper D. Development, testing and use of data extraction forms in systematic reviews: a review of methodological guidance. BMC Med Res Methodol. 2020 Dec 1;20(1). pmid:33076832
- 20.
Peters MDJ, Godfrey CM, McInerney P, Munn Z, Tricco AC, Khalil H. Chapter 11: Scoping reviews. In: Aromataris E, Munn Z, editors. JBI Reviewer´s Manual [Internet]. Joanna Briggs Institute Reviewer’s Manual, JBI, 2020; 2020. p. 407–52. Available from: https://reviewersmanual.joannabriggs.org/.
- 21. Pradines M, Ghedira M, Portero R, Masson I, Marciniak C, Hicklin D, et al. Ultrasound Structural Changes in Triceps Surae After a 1-Year Daily Self-stretch Program: A Prospective Randomized Controlled Trial in Chronic Hemiparesis. Neurorehabil Neural Repair [Internet]. 2019 Apr 22;33(4):245–59. Available from: http://journals.sagepub.com/doi/ pmid:30900512
- 22. Ghasemi E, Khademi-Kalantari K, Khalkhali-Zavieh M, Rezasoltani A, Ghasemi M, Akbarzadeh Baghban A, et al. The Effect of Functional Stretching Exercises on Neural and Mechanical Properties of the Spastic Medial Gastrocnemius Muscle in Patients with Chronic Stroke: A Randomized Controlled Trial. Journal of Stroke and Cerebrovascular Diseases. 2018 Jul;27(7):1733–42. pmid:29706442
- 23. Pradines M, Baude M, Marciniak C, Francisco G, michel Gracies J, Hutin E, et al. Effect on Passive Range of Motion and Functional Correlates After a Long-Term Lower Limb Self-Stretch Program in Patients With Chronic Spastic Paresis. PM&R. 2018 Oct;10(10):1020–31.
- 24. Bakheit AMO, Maynard V, Shaw S. The effects of isotonic and isokinetic muscle stretch on the excitability of the spinal alpha motor neurones in patients with muscle spasticity. Eur J Neurol. 2005 Sep;12(9):719–24. pmid:16128875
- 25.
Chung SG, Bai Z, Rymer WZ, Zhang LQ. Changes of Reflex, Non-reflex and Torque Generation Properties of Spastic Ankle Plantar Flexors Induced by Intelligent Stretching. In: 2005 IEEE Engineering in Medicine and Biology 27th Annual Conference [Internet]. IEEE; 2005. p. 3672–5. Available from: http://ieeexplore.ieee.org/document/1617279/.
- 26. Yeh CY, Tsai KH, Chen JJ. Effects of prolonged muscle stretching with constant torque or constant angle on hypertonic calf muscles. Arch Phys Med Rehabil [Internet]. 2005 Feb;86(2):235–41. Available from: https://linkinghub.elsevier.com/retrieve/pii/S000399930400471X. pmid:15706549
- 27. Gao F, Ren Y, Roth EJ, Harvey R, qun Zhang L. Effects of repeated ankle stretching on calf muscle–tendon and ankle biomechanical properties in stroke survivors. Clinical Biomechanics. 2011 Jun;26(5):516–22. pmid:21211873
- 28. Selles RW, Li X, Lin F, Chung SG, Roth EJ, Zhang LQ. Feedback-Controlled and Programmed Stretching of the Ankle Plantarflexors and Dorsiflexors in Stroke: Effects of a 4-Week Intervention Program. Arch Phys Med Rehabil [Internet]. 2005 Dec;86(12):2330–6. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0003999305009354. pmid:16344031
- 29. Bressel E, McNair PJ. The effect of prolonged static and cyclic stretching on ankle joint stiffness, torque relaxation, and gait in people with stroke. Phys Ther. 2002;82(9):880–7. pmid:12201802
- 30. Zhang LQ, Chung SG, Bai Z, Xu D, van Rey EMT, Rogers MW, et al. Intelligent stretching of ankle joints with contracture/spasticity. IEEE Transactions on Neural Systems and Rehabilitation Engineering [Internet]. 2002 Sep;10(3):149–57. Available from: https://ieeexplore.ieee.org/document/1114834/. pmid:12503779
- 31. Maynard V, Bakheit AMO, Shaw S. Comparison of the impact of a single session of isokinetic or isotonic muscle stretch on gait in patients with spastic hemiparesis. Clin Rehabil. 2005 Mar;19(2):146–54. pmid:15759529
- 32. Lee CH, Lee SH, Yoo J il, Lee S. Ultrasonographic Evaluation for the Effect of Extracorporeal Shock Wave Therapy on Gastrocnemius Muscle Spasticity in Patients With Chronic Stroke. PM&R [Internet]. 2019 Apr;11(4):363–71. Available from: pmid:30145342
- 33. Radinmehr H, Ansari NN, Naghdi S, Tabatabaei A, Moghimi E. Comparison of Therapeutic Ultrasound and Radial Shock Wave Therapy in the Treatment of Plantar Flexor Spasticity After Stroke: A Prospective, Single-blind, Randomized Clinical Trial. Journal of Stroke and Cerebrovascular Diseases. 2019 Jun;28(6):1546–54. pmid:30935809
- 34. Radinmehr H, Nakhostin Ansari N, Naghdi S, Olyaei G, Tabatabaei A. Effects of one session radial extracorporeal shockwave therapy on post-stroke plantarflexor spasticity: a single-blind clinical trial. Disabil Rehabil [Internet]. 2017 Feb 27;39(5):483–90. Available from: https://www.tandfonline.com/doi/full/10.3109/09638288.2016.1148785. pmid:26971745
- 35. Taheri P, Vahdatpour B, Mellat M, Ashtari F, Akbari M. Effect of Extracorporeal Shock Wave Therapy on Lower Limb Spasticity in Stroke Patients. Arch Iran Med. 2017 Jun;20(6):338–43. pmid:28646841
- 36. ting Wu Y, ning Chang C, min Chen Y, chi Hu G. Comparison of the effect of focused and radial extracorporeal shock waves on spastic equinus in patients with stroke: a randomized controlled trial. Eur J Phys Rehabil Med [Internet]. 2018 Jun;54(4):518–25. Available from: https://www.minervamedica.it/index2.php?show=R33Y2018N04A0518. pmid:29072044
- 37. Moon SW, Kim JH, Jung MJ, Son S, Lee JH, Shin H, et al. The Effect of Extracorporeal Shock Wave Therapy on Lower Limb Spasticity in Subacute Stroke Patients. Ann Rehabil Med [Internet]. 2013;37(4):461. Available from: http://e-arm.org/journal/view.php?doi=10.5535/arm.2013.37.4.461. pmid:24020026
- 38. Sawan S, Abd-Allah F, Hegazy MM, Farrag MA, El-Den NHS. Effect of shock wave therapy on ankle plantar flexors spasticity in stroke patients. NeuroRehabilitation [Internet]. 2017 Mar 6;40(1):115–8. Available from: https://www.medra.org/servlet/aliasResolver?alias=iospress&doi=10.3233/NRE-161396. pmid:27814307
- 39. Santamato A, Micello MF, Panza F, Fortunato F, Logroscino G, Picelli A, et al. Extracorporeal shock wave therapy for the treatment of poststroke plantar-flexor muscles spasticity: a prospective open-label study. Top Stroke Rehabil [Internet]. 2014;21 Suppl 1(Suppl 1):S17–24. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24722040. pmid:24722040
- 40. Sohn MK, Cho KH, jae Kim Y, Hwang SL. Spasticity and Electrophysiologic Changes after Extracorporeal Shock Wave Therapy on Gastrocnemius. Ann Rehabil Med [Internet]. 2011;35(5):599. Available from: http://e-arm.org/journal/view.php?doi= pmid:22506181
- 41. Ganesh GS, Kumari R, Pattnaik M, Mohanty P, Mishra C, Kaur P, et al. Effectiveness of Faradic and Russian currents on plantar flexor muscle spasticity, ankle motor recovery, and functional gait in stroke patients. Physiotherapy Research International [Internet]. 2018 Apr;23(2):e1705. Available from: https://onlinelibrary.wiley.com/doi/ pmid:29417699
- 42. Yang YR, Mi PL, Huang SF, Chiu SL, Liu YC, Wang RY. Effects of neuromuscular electrical stimulation on gait performance in chronic stroke with inadequate ankle control—A randomized controlled trial. Baur H, editor. PLoS One [Internet]. 2018 Dec 10;13(12):e0208609. Available from: pmid:30532195
- 43. Sharif F, Ghulam S, Malik AN, Saeed Q. Effectiveness of Functional Electrical Stimulation (FES) versus Conventional Electrical Stimulation in Gait Rehabilitation of Patients with Stroke. J Coll Physicians Surg Pak. 2017 Nov;27(11):703–6. pmid:29132482
- 44. Suh HR, Han HC, young Cho H. Immediate therapeutic effect of interferential current therapy on spasticity, balance, and gait function in chronic stroke patients: a randomized control trial. Clin Rehabil. 2014 Sep 7;28(9):885–91.
- 45. Sabut SK, Sikdar C, Kumar R, Mahadevappa M. Functional electrical stimulation of dorsiflexor muscle: Effects on dorsiflexor strength, plantarflexor spasticity, and motor recovery in stroke patients. NeuroRehabilitation [Internet]. 2011 Dec 22;29(4):393–400. Available from: https://www.medra.org/servlet/aliasResolver?alias=iospress&doi= pmid:22207067
- 46. Bakhtiary AH, Fatemy E. Does electrical stimulation reduce spasticity after stroke? A randomized controlled study. Clin Rehabil [Internet]. 2008 May 1;22(5):418–25. Available from: http://journals.sagepub.com/doi/10.1177/0269215507084008. pmid:18441038
- 47. Chen SC, Chen YL, Chen CJ, Lai C h, Chiang W h, Chen W l. Effects of surface electrical stimulation on the muscle–tendon junction of spastic gastrocnemius in stroke patients. Disabil Rehabil. 2005 Feb 4;27(3):105–10. pmid:15823991
- 48. Ghannadi S, Shariat A, Ansari NN, Tavakol Z, Honarpishe R, Dommerholt J, et al. The Effect of Dry Needling on Lower Limb Dysfunction in Poststroke Survivors. Journal of Stroke and Cerebrovascular Diseases [Internet]. 2020 Jun;29(6):104814. Available from: https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.104814. pmid:32327366
- 49. Hadi S, Khadijeh O, Hadian M, Niloofar AY, Olyaei G, Hossein B, et al. The effect of dry needling on spasticity, gait and muscle architecture in patients with chronic stroke: A case series study. Top Stroke Rehabil [Internet]. 2018 Apr 23;9357:1–7. Available from: https://www.tandfonline.com/doi/full/10.1080/10749357.2018.1460946. pmid:29683410
- 50. Sánchez-Mila Z, Salom-Moreno J, Fernández-de-las-Peñas C. Effects of Dry Needling on Post-Stroke Spasticity, Motor Function and Stability Limits: A Randomised Clinical Trial. Acupuncture in Medicine [Internet]. 2018 Dec 1;36(6):358–66. Available from: http://journals.sagepub.com/doi/10.1136/acupmed-2017-011568. pmid:29986902
- 51. Calvo S, Quintero I, Herrero P. Effects of dry needling (DNHS technique) on the contractile properties of spastic muscles in a patient with stroke: a case report. International Journal of Rehabilitation Research. 2016 Dec;39(4):372–6. pmid:27362968
- 52. Salom-Moreno J, Sánchez-Mila Z, Ortega-Santiago R, Palacios-Ceña M, Truyol-Domínguez S, Fernández-de-las-Peñas C. Changes in Spasticity, Widespread Pressure Pain Sensitivity, and Baropodometry After the Application of Dry Needling in Patients Who Have Had a Stroke: A Randomized Controlled Trial. J Manipulative Physiol Ther. 2014 Oct;37(8):569–79. pmid:25199825
- 53. Fink M, Rollnik JD, Bijak M, Borsta C, Da J, Guergueltcheva V, et al. Needle acupuncture in chronic poststroke leg spasticity. Arch Phys Med Rehabil [Internet]. 2004 Apr;85(4):667–72. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0003999303009419. pmid:15083445
- 54. Koyama S, Tanabe S, Takeda K, Sakurai H, Kanada Y. Modulation of spinal inhibitory reflexes depends on the frequency of transcutaneous electrical nerve stimulation in spastic stroke survivors. Somatosens Mot Res [Internet]. 2016 Jan 2;33(1):8–15. Available from: https://www.tandfonline.com/doi/full/10.3109/08990220.2016.1142436. pmid:26949041
- 55. Picelli A, Dambruoso F, Bronzato M, Barausse M, Gandolfi M, Smania N. Efficacy of Therapeutic Ultrasound and Transcutaneous Electrical Nerve Stimulation Compared With Botulinum Toxin Type A in the Treatment of Spastic Equinus in Adults With Chronic Stroke: A Pilot Randomized Controlled Trial. Top Stroke Rehabil. 2014 Mar 5;21(sup1):S8–16. pmid:24722047
- 56. Cho HY, Sung In T, Hun Cho K, Ho Song C. A Single Trial of Transcutaneous Electrical Nerve Stimulation (TENS) Improves Spasticity and Balance in Patients with Chronic Stroke. Tohoku J Exp Med. 2013;229(3):187–93. pmid:23419328
- 57. Martins FL, Carvalho LC, Silva CC, Brasileiro JS, Souza TO, Lindquist ARR. Immediate effects of TENS and cryotherapy in the reflex excitability and voluntary activity in hemiparetic subjects: a randomized crossover trial. Braz J Phys Ther [Internet]. 2012 Aug;16(4):337–44. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1413-35552012000400002&lng=en&nrm=iso&tlng=en. pmid:22801453
- 58. Yan T, Hui-Chan C. Transcutaneous electrical stimulation on acupuncture points improves muscle function in subjects after acute stroke: A randomized controlled trial. J Rehabil Med. 2009;41(5):312–6. pmid:19363561
- 59. Ng SSM, Hui-Chan CWY. Transcutaneous Electrical Nerve Stimulation Combined With Task-Related Training Improves Lower Limb Functions in Subjects With Chronic Stroke. Stroke [Internet]. 2007 Nov;38(11):2953–9. Available from: https://www.ahajournals.org/doi/ pmid:17901383
- 60. Miyara K, Matsumoto S, Uema T, Noma T, Ikeda K, Ohwatashi A, et al. Effect of whole body vibration on spasticity in hemiplegic legs of patients with stroke. Top Stroke Rehabil [Internet]. 2018 Feb 17;25(2):90–5. Available from: https://www.tandfonline.com/doi/full/ pmid:29032720
- 61. Huang M, Miller T, Ying M, Pang MYC. Whole-body vibration modulates leg muscle reflex and blood perfusion among people with chronic stroke: a randomized controlled crossover trial. Sci Rep. 2020 Dec 30;10(1):1473. pmid:32001783
- 62. Miyara K, Kawamura K, Matsumoto S, Ohwatashi A, Itashiki Y, Uema T, et al. Acute changes in cortical activation during active ankle movement after whole-body vibration for spasticity in hemiplegic legs of stroke patients: a functional near-infrared spectroscopy study. Top Stroke Rehabil [Internet]. 2020 Jan 2;27(1):67–74. Available from: pmid:31483746
- 63. Alp A, Efe B, Adalı M, Bilgiç A, Demir Türe S, Coşkun Ş, et al. The Impact of Whole Body Vibration Therapy on Spasticity and Disability of the Patients with Poststroke Hemiplegia. Rehabil Res Pract. 2018 May 2;2018:1–6.
- 64. Pang MYC, Lau RWK, Yip SP. The effects of whole-body vibration therapy on bone turnover, muscle strength, motor function, and spasticity in chronic stroke: a randomized controlled trial. Eur J Phys Rehabil Med. 2013 Aug 2;49(4):439–50. pmid:23486302
- 65. shan Chan K, wei Liu C, wen Chen T, cheng Weng M, hsiung Huang M, Chen CH. Effects of a single session of whole body vibration on ankle plantarflexion spasticity and gait performance in patients with chronic stroke: a randomized controlled trial. Clin Rehabil. 2012 Dec 3;26(12):1087–95. pmid:23035004
- 66. Sahin N, Ugurlu H, Karahan AY. Efficacy of therapeutic ultrasound in the treatment of spasticity: A randomized controlled study. NeuroRehabilitation. 2011 Aug 23;29(1):61–6. pmid:21876297
- 67. Ansari NN, Naghdi S, Bagheri H, Ghassabi H. Therapeutic ultrasound in the treatment of ankle plantarflexor spasticity in a unilateral stroke population: a randomized, single-blind, placebo-controlled trial. Electromyogr Clin Neurophysiol. 2007;47(3):137–43. pmid:17557646
- 68. Ansari NN, Naghdi S, Hasson S, Rastgoo M. Efficacy of therapeutic ultrasound and infrared in the management of muscle spasticity. Brain Inj. 2009 Jan 21;23(7–8):632–8.
- 69. Alcantara CC, Blanco J, De Oliveira LM, Ribeiro PFS, Herrera E, Nakagawa TH, et al. Cryotherapy reduces muscle hypertonia, but does not affect lower limb strength or gait kinematics post-stroke: a randomized controlled crossover study. Top Stroke Rehabil. 2019 May 19;26(4):267–80. pmid:31012824
- 70. Garcia LC, Alcântara CC, Santos GL, Monção JVA, Russo TL. Cryotherapy Reduces Muscle Spasticity But Does Not Affect Proprioception in Ischemic Stroke. Am J Phys Med Rehabil. 2019 Jan;98(1):51–7.
- 71. Zhang Y, Wang YZ, Huang LP, Bai B, Zhou S, Yin MM, et al. Aquatic Therapy Improves Outcomes for Subacute Stroke Patients by Enhancing Muscular Strength of Paretic Lower Limbs Without Increasing Spasticity. Am J Phys Med Rehabil. 2016 Nov;95(11):840–9.
- 72. Akbari A, Karimi H. The Effect of Strengthening Exercises on Exaggerated Muscle Tonicity in Chronic Hemiparesis Following Stroke. Journal of Medical Sciences. 2006 Apr 15;6(3):382–8.
- 73. Tsai KH, Yeh CY, Chang HY, Chen JJ. Effects of a single session of prolonged muscle stretch on spastic muscle of stroke patients. Proc Natl Sci Counc Repub China B. 2001;25(2):76–81. pmid:11370763
- 74. Fleuren JFM, Voerman GE, Erren-Wolters C v, Snoek GJ, Rietman JS, Hermens , et al. Stop using the Ashworth Scale for the assessment of spasticity. J Neurol Neurosurg Psychiatry [Internet]. 2010 Jan 1;81(1):46–52. Available from: https://jnnp.bmj.com/lookup/doi/10.1136/jnnp.2009.177071. pmid:19770162
- 75. Alibiglou L, Rymer WZ, Harvey RL, Mirbagheri MM. The relation between Ashworth scores and neuromechanical measurements of spasticity following stroke. J Neuroeng Rehabil. 2008;5:1–14.
- 76. Pandyan AD, Price CIM, Rodgers H, Barnes MP, Johnson GR. Biomechanical examination of a commonly used measure of spasticity. Clinical Biomechanics. 2001;16(10):859–65. pmid:11733123
- 77. Malhotra S, Cousins E, Ward A, Day C, Jones P, Roffe C, et al. An investigation into the agreement between clinical, biomechanical and neurophysiological measures of spasticity. Clin Rehabil. 2008;22(12):1105–15. pmid:19052249
- 78. Lance JW. The control of muscle tone, reflexes, and movernent: Robert Wartenbeg lecture. Neurology. 1980;30(12):1303–13.
- 79. Bohannon RW, Smith MB. Interrater Reliability of a Modified Ashworth Scale of Muscle Spasticity. Phys Ther [Internet]. 1897;67(2):206–7. Available from: http://link.springer.com/10.1007/978-1-4471-5451-8_105.
- 80. Ghotbi N, Ansari NN, Naghdi S, Hasson S. Measurement of lower-limb muscle spasticity: Intrarater reliability of Modified Modified Ashworth Scale. J Rehabil Res Dev. 2011;48(1):83–8. pmid:21328165
- 81. Nakhostin Ansari N, Naghdi S, Forogh B, Hasson S, Atashband M, Lashgari E. Development of the persian version of the modified modified ashworth scale: Translation, adaptation, and examination of interrater and intrarater reliability in patients with poststroke elbow flexor spasticity. Disabil Rehabil. 2012;34(21):1843–7. pmid:22432437
- 82. Meseguer-Henarejos AB, Sánchez-Meca J, López-Pina JA, Carles-Hernández R. Inter- and intra-rater reliability of the Modified Ashworth Scale: a systematic review and meta-analysis. Eur J Phys Rehabil Med. 2018 Jun;54(4):576–90. pmid:28901119
- 83. Pandyan AD, Johnson GR, Price CIM, Curless RH, Barnes MP, Rodgers H. A review of the properties and limitations of the Ashworth and modified Ashworth Scales as measures of spasticity. Clin Rehabil. 1999 Oct 1;13(5):373–83. pmid:10498344
- 84. Baude M, Bo Nielsen J, Gracies JM. The neurophysiology of deforming spastic paresis: A revised taxonomy. Ann Phys Rehabil Med [Internet]. 2018;62(6):426–30. Available from: pmid:30500361
- 85. Mehrholz J, Wagner K, Meißner D, Grundmann K, Zange C, Koch R, et al. Reliability of the Modified Tardieu Scale and the Modified Ashworth Scale in adult patients with severe brain in jury: a comparison study. Clin Rehabil. 2005;19:751–9. pmid:16250194
- 86. Gracies JM, Burke K, Clegg NJ, Browne R, Rushing C, Fehlings D, et al. Reliability of the Tardieu Scale for Assessing Spasticity in Children With Cerebral Palsy. Arch Phys Med Rehabil. 2010;91(3):421–8. pmid:20298834
- 87. Gracies JM. Pathophysiology of spastic paresis. I: Paresis and soft tissue changes. Muscle Nerve. 2005;31(5):535–51. pmid:15714510
- 88. Ben-Shabat E, Palit M, Fini NA, Brooks CT, Winter A, Holland AE. Intra- and Interrater Reliability of the Modified Tardieu Scale for the Assessment of Lower Limb Spasticity in Adults With Neurologic Injuries. Arch Phys Med Rehabil [Internet]. 2013;94(12):2494–501. Available from: pmid:23851419
- 89. Li F, Wu Y, Li X. Test-retest reliability and inter-rater reliability of the Modified Tardieu Scale and the Modified Ashworth Scale in hemiplegic patients with stroke. Eur J Phys Rehabil Med. 2014;50(1):9–15. pmid:24309501
- 90. Chan CWY. Motor and sensory deficits following a stroke: Relevance to a comprehensive evaluation. Physiotherapy Canada. 1986;38(1).
- 91. Rodà F, Bevilacqua L, Merlo A, Prestini L, Brianti R, Lombardi F, et al. Evidence-Based Medicine and Clinical Practice: the first Italian attempt to define the appropriateness of rehabilitation admission criteria through the application of the Delphi method. Ann Ig. 2019;31(2):117–29. pmid:30714609
- 92. Merlo A, Rodà F, Carnevali D, Principi N, Grimoldi L, Auxilia F, et al. Appropriateness of admission to rehabilitation: definition of a set of criteria and rules through the application of the Delphi method. Eur J Phys Rehabil Med. 2020 Nov;56(5):537–46. pmid:32667147
- 93. Bar-On L, Aertbeliën E, Wambacq H, Severijns D, Lambrecht K, Dan B, et al. A clinical measurement to quantify spasticity in children with cerebral palsy by integration of multidimensional signals. Gait Posture. 2013;38(1):141–7. pmid:23218728
- 94. Trompetto C, Currà A, Puce L, Mori L, Serrati C, Fattapposta F, et al. Spastic dystonia in stroke subjects: prevalence and features of the neglected phenomenon of the upper motor neuron syndrome. Clinical Neurophysiology [Internet]. 2019;130(4):521–7. Available from: pmid:30776732
- 95.
Merletti R, Campanini I, Rymer WZ, Disselhorst-Klug C. Editorial: Surface Electromyography: Barriers Limiting Widespread Use of sEMG in Clinical Assessment and Neurorehabilitation. Merletti R, Disselhorst-Klug C, Rymer WZ, Campanini I, editors. Vol. 12, Frontiers in Neurology. Lausanne: Frontiers Media SA; 2021.
- 96. Campanini I, Merlo A, Damiano B. A method to differentiate the causes of stiff-knee gait in stroke patients. Gait Posture [Internet]. 2013;38(2):165–9. Available from: pmid:23755883
- 97. Merlo A, Campanini I. Impact of instrumental analysis of stiff knee gait on treatment appropriateness and associated costs in stroke patients. Gait Posture [Internet]. 2019;72(June):195–201. Available from: pmid:31228856
- 98. Sheean G, McGuire JR. Spastic Hypertonia and Movement Disorders: Pathophysiology, Clinical Presentation, and Quantification. PM&R. 2009 Sep;1(9):827–33. pmid:19769916
- 99. Wissel J, Ward AB, Erztgaard P, Bensmail D, Hecht MJ, Lejeune TM, et al. European consensus table on the use of botulinum toxin type a in adult spasticity. J Rehabil Med. 2009;41(1):13–25. pmid:19197564
- 100.
Merlo A, Campanini I. Applications In Movement And Gait Analysis. In: Surface Electromyography Physiology, Engineering, and Applications. 1st ed. Hoboken, New Jersey: John Wiley & Sons; 2016. p. 440–59.
- 101. Manca A, Cereatti A, Bar-On L, Botter A, della Croce U, Knaflitz M, et al. A Survey on the Use and Barriers of Surface Electromyography in Neurorehabilitation. Front Neurol. 2020;11(October):1–13. pmid:33123079
- 102. Merletti R, Farina D, Gazzoni M, Merlo A, Ossola P, Rainoldi A. Surface electromyography: A window on the muscle, a glimpse on the central nervous system. Eura Medicophys. 2001;37(1):57–68.
- 103. Campanini I, Merlo A, Degola P, Merletti R, Vezzosi G, Farina D. Effect of electrode location on EMG signal envelope in leg muscles during gait. Journal of Electromyography and Kinesiology. 2007;17(4):515–26. pmid:16889982
- 104. Campanini I, Merlo A, Disselhorst-Klug C, Mesin L, Muceli S, Merletti R. Fundamental Concepts of Bipolar and High-Density Surface EMG Understanding and Teaching for Clinical, Occupational, and Sport Applications: Origin, Detection, and Main Errors. Vol. 22, Sensors. MDPI; 2022. pmid:35684769
- 105. Campanini I, Disselhorst-Klug C, Rymer WZ, Merletti R. Surface EMG in Clinical Assessment and Neurorehabilitation: Barriers Limiting Its Use. Front Neurol. 2020;11(September):1–22. pmid:32982942
- 106. Platz T, Eickhof C, Nuyens G, Vuadens P. Clinical scales for the assessment of spasticity, associated phenomena, and function: A systematic review of the literature. Disabil Rehabil. 2005;27(1–2):7–18. pmid:15799141
- 107. Campanini I, Merlo A, Damiano B. A method to differentiate the causes of stiff-knee gait in stroke patients. Gait Posture. 2013 Jun;38(2):165–9. pmid:23755883
- 108. Mazzoli D, Giannotti E, Manca M, Longhi M, Prati P, Cosma M, et al. Electromyographic activity of the vastus intermedius muscle in patients with stiff-knee gait after stroke. A retrospective observational study. Gait Posture [Internet]. 2018 Feb;60:273–8. Available from: pmid:28735780
- 109. Vinti M, Bayle N, Merlo A, Authier G, Pesenti S, Jouve JL, et al. Muscle Shortening and Spastic Cocontraction in Gastrocnemius Medialis and Peroneus Longus in Very Young Hemiparetic Children. Biomed Res Int. 2018;2018. pmid:29951529
- 110. Merlo A, Galletti M, Zerbinati P, Prati P, Mascioli F, Basini G, et al. Surgical quadriceps lengthening can reduce quadriceps spasticity in chronic stroke patients. A case-control study. Front Neurol [Internet]. 2022 Oct 13;13. Available from: https://www.frontiersin.org/articles/10.3389/fneur.2022.980692/full. pmid:36313503
- 111. Merlo A, Montecchi MG, Lombardi F, Vata X, Musi A, Lusuardi M, et al. Monitoring involuntary muscle activity in acute patients with upper motor neuron lesion by wearable sensors: A feasibility study. Sensors. 2021;21(9). pmid:33946234
- 112. Campanini I, Merlo A, Farina D. Motor unit discharge pattern and conduction velocity in patients with upper motor neuron syndrome. Journal of Electromyography and Kinesiology [Internet]. 2009;19(1):22–9. Available from: pmid:17709261
- 113. Gracies J. Coefficients of impairment in deforming spastic paresis. Ann Phys Rehabil Med. 2015;58(3):173–8. pmid:26027752