Strength training protocols in hemiparetic individuals post stroke : a systematic review

Abstract Introduction: Hemiparesis is one of the main sequels of stroke. Evidence suggests that muscle strength exercises are important in rehabilitation programs for hemiparetic patients, but wide variation in previously studied protocols makes the most suitable choice difficult in clinical practice. Objective: The aim of this study was to investigate strength training protocols for people with hemiparesis after stroke. Methods: A systematic review of literature was performed in the PubMed, PEDro (Physiotherapy Evidence Database), SciELO (Scientific Electronic Library Online), and LILACS (Latin American and Caribbean Literature in Health Science) databases. Only controlled clinical studies that contained strength training protocols for hemiparesis after stroke were selected. Results: In total, 562 articles were found. Of them, 12 were accepted for the systematic review. Although strength training protocols are effective in hemiparetic patients, we did not found a standard method for strength training. Conclusion: This systematic revision highlights the lack of a standard protocol for strength training, considering the following training parameters: volume, intensity, frequency, series, and repetitions. Isotonic exercises are most commonly used.


Introduction
Stroke is one of the major causes of hospitalization and mortality worldwide.In 2013, there were nearly 25.7 million stroke survivors, 6.5 million deaths from stroke, and 10.3 million new cases of stroke, with a more pronounced increase in the incidence and prevalence of ischemic stroke after the age of 49 and 39 years, respectively, in developed countries [1].In Brazil, 160,621 hospital admissions for cerebrovascular diseases were registered in 2009.The mortality rate was 0.05%, and almost 35% of the 99,174 deaths occurred among patients who were over 80-years-old [2].
Stroke patients may exhibit sensorimotor deficits that limit the performance of functional activities such as gait, orthostatism, and sit-up [3] tasks.These affect the mobility of patients, limiting their daily activities, society intervention, and the probability of returning to professional activities, leading to reduced quality of life [4].Paresis is defined as the change in the ability to generate normal levels of muscle strength and manifests in different forms, including paresis of the contralateral body and brain injury (hemiparesis) [5 -7].Muscle weakness seems to be one of the factors responsible for functional limitation in individuals with stroke [8].
Physical rehabilitation is the most effective way to reduce motor deficits in stroke patients [4] and many therapies are proposed [9 -15].Strength/ resistance training (ST) in stroke rehabilitation was rejected for a long time because of it supposedly inducing spasticity [4,6].However, it appears to be an essential part of rehabilitation programs in patients with brain injury [4].In this context, a recent meta-analysis concluded that ST is the most efficient method for gaining strength in the lower limbs in hemiparetic populations [7].Another systematic review indicates that muscle strengthening exercises can be integrated as a poststroke rehabilitation strategy to improve upper limb motor deficits [4].Furthermore, ST produces increased strength, gait velocity, functional outcomes, and quality of life without exacerbating spasticity after stroke [6].
However, the authors of this study, as well as the others [6], observed a large variation in training parameters/protocols in studies that performed ST in hemiparetic patients, making it difficult to choose these parameters in clinical practice.Thus, the current study aimed at investigating and analyzing the ST parameters/protocols for post-stroke hemiparetic patients.

Study types
Controlled experimental randomized clinical trial studies were considered.Studies with case series/ case report design, bibliographic reviews, and uncontrolled experimental studies were excluded.Furthermore, conference abstracts as well as studies falling outside the methodology investigated in this review were disregarded.

Type of participants
Study samples should include stroke patients of both genders and with no age and time of diagnosis restrictions.The classification of tonus (hypotonia or hypertonia) exhibited by study patients was not considered.Studies including patients with other neurological pathologies associated with stroke were excluded.

Type of intervention
The type of training accepted in this review included protocols that used, for instance, equipment (leg press, extender, flexor, high pulley, adductors, and hip abductors) and free weights aimed at strengthening the upper and lower limbs.Training protocols included isokinetic, isotonic (eccentric and concentric), and isometric exercises.

Type of outcome measured
Primary outcome: intervention protocols that include the description of exercises with weights, volume, intensity, and frequency of training.

Data sources
The search for articles was performed between August 1 and September 30, 2016 in the following electronic databases: MEDLINE, PubMed, LILACS (Latin American and Caribbean Literature in Health Science), Cochrane, SciELO (Scientific Electronic Library Online), Manual Search, and PEDro (Physiotherapy Evidence Database).Studies published before September 2016, were considered.

Period and language
No date and language restrictions.

Search Keywords
Keywords are described in Table 1.

Study selection
After exclusion of duplicates, two reviewers (D.B and M.T.R) evaluated the titles and abstracts of the identified references based on the inclusion and exclusion criteria; in a case of a conflict, a third reviewer was consulted (V.S.H).Clearly irrelevant references were excluded.In the second phase, the reviewers assessed the full text and selected the references based on the same inclusion and exclusion criteria.

Data collection process
The same reviewers read the articles and collected the data according to a previously prepared table (see collected items).

Collected items
The items extracted from each study were: author/year, population and experimental groups, exercise types, frequency, volume, intensity of the training, outcomes evaluated by the authors of the studies, and the results.

Quality assessment of the included studies
The evaluation of the methodological quality of included studies was performed according to the PEDro scale [16 -19].

Characterization of the studies
The characteristics of the included studies are presented in Table 2.The studies found that ST is a valid therapy for strength gain in hemiparetic patients.The considered studies involved a total of 371 patients, who were allocated to different intervention groups and controls: control (e.g., range of motion exercises, flexibility exercises, maintenance of daily routines), sham control, aerobic exercises, and task oriented training.
All studies (12/12; 100%) included ST of the lower limbs, while a single study included ST of the upper limbs.With respect to the muscle groups exercised, those with greater incidence were the knee extensors, plantiflexors, and dorsiflexors.Regarding the exercises used, knee extension and/ or flexion (8/12; ~ 66%), leg press (6/12; 50%), and ankle flexion and/or extension (6/12; 50%) were the most studied.Regarding the number of sessions per week, only two out of 12 (17%) studies involved five weekly sessions; the other studies involved two or three sessions per week.Concerning duration, six (50%) studies covered a period between 10 to 12 weeks, four (~ 33%) studies involved six weeks, and two (~ 17%) studies were less than six weeks long.
Regarding the intensity of ST, the mean intensity used was between 70% and 80% of a maximal repetition (1MR).This review also included two studies that analyzed the differences between the benefits associated with eccentric and concentric ST, using maximum repetitions as intensity grading; the remaining studies involved isotonic exercises.
The studies considered in this review exhibit a great variety of outcomes and evaluation tools.Examples include: dynamometry, timed up and go, six-minute walk test, stair climbing test, sit and stand up test, isokinetic strength, walking speed, FC Peak and peak VO2, 1MR, quality of life, balance, scales used to monitor perception of effort, electromyography (EMG), and force platform.All studies reported beneficial results associated with ST regarding different outcomes.(To be continued) Methodological Quality of the Studies Table 3 (supporting information) represents the evaluation of the methodological quality of the studies, which was performed according to the PEDro scale.The results showed an average score of 5.42 points.There was greater score loss in the studies in item three (allocation omission), item five (participants blinding), item six (therapist blinding), and item nine (intention-to-treat analysis).No study reached the maximum score.Note: Criteria: 1) eligibility; 2) random allocation; 3) allocation omission; 4) baseline comparison; 5) blinding to participants; 6) blinding to therapists; 7) blinding to evaluators; 8) adequate follow-up; 9) intention-to-treat analysis; 10) comparison between groups; 11) estimation of effect and variability.

Discussion
This systematic review aimed at identifying ST protocols in hemiparetic individuals.Twelve controlled clinical trials that tested ST in hemiparetic patients were included.All studies considered in this review showed that ST increased muscle strength in hemiparetic individuals relative to their controls, although no standard protocol was found for this intervention.
The ST program exhibits some variables that form the basis of any method: intensity percentage, volume of exercise (number of sets, repetitions, and exercises), frequency, type of exercises, and training structure [31].The average load percentage found in this study was 75%.In this context, Kraemer and Ratamess [32] reported that exercises performed with 70-80% of the maximum load induce a change in strength.Nonetheless, different authors report positive results with workloads between 50% and 80% of 1MR and with 40% loads already showing positive results with regards to muscle strength enhancement [33].This technique of load percentage definition is widely recognized as a reference standard for the evaluation of muscle strength [34].Although the data resulting from this review showed that there was no defined ST protocol for hemiparetic patients, all the studies used a load percentage within the recommended ideal values for strength gain.
Although it was not one of the factors of analysis of this study, it should be emphasized that all studies selected included hemiparetic patients six and nine months after the cerebrovascular event.This time period is consistent with that of the study by Teixeira et al. [35], which reported an improvement in physical activities after a training period involving bodybuilding strengthening exercises.
In addition, it was observed that the selected articles aimed at studying the lower limbs.Only the study reported by Aidar et al. [25] involved both the upper and lower limbs.Among the most studied exercises are knee extensors and flexors, hip flexors, plantar flexors, and dorsiflexors, while bench press exercises are the most common for the upper limbs.These exercises may contribute to walking in these individuals, since gait training is one of the main goals in functional rehabilitation after stroke [36].
Among the studies analyzed in this review, the type of exercise used by ~ 92% of the studies was isotonic.Only two studies [22,23] aimed at measuring differences between eccentric and concentric contractions.The skeletal muscle system produces less strength in concentric contraction when compared to eccentric contraction in poststroke patients submitted to ST, and in this context, the eccentric exercise has been shown to be more effective in neural adaptations [23].
The studies included in this review exhibit a great variability of outcomes and evaluation tools.Muscle strength was assessed using dynamometry [20,23] and functional tests (functional capacity) such as the timed up and go test, which measures the time (seconds) it takes for an individual to stand up from a standard armchair (about 46 cm in height), walk a distance of 3 m, turn around, walk back to the chair, and sit again [37].Another common functional test was the six-minute walk test, which has been recommended and used in evaluating the results of a cardiorespiratory rehabilitation program.It is a simple and easily performed test for the measurement of functional capacity [38].Other outcomes, such as climbing stairs, sit-up and stand-up tests, isokinetic strength, walking speed, peak heart rate, oxygen consumption, 1MR, quality of life, dynamic balance, scales used to monitor perception of effort, EMG, and force platform, were also used.
The methodological quality assessment tool, PEDro, was used.A mean of 5.42 points was observed in the studies included in this review.Similar results (5.78 points) were observed in another study, which evaluated 272 stroke studies using the PEDro scale, concluding that the PEDro scale provides a more comprehensive measure of the methodological quality of literature on stroke [19].The same authors reported that in studies on stroke rehabilitation, double-blinding is usually not possible.Other authors reported that two criteria of the PEDro scale (therapist and patient blinding) are not always possible to be fulfilled during the studies, namely, in studies where the intervention is the exercise [39].Thus, the maximum score of the study would be eight points.
This study, as well as others [6,7], found that there is no standard protocol for ST in stroke patients.Pak and Patten [6] recommend parameters for ST.However, unlike this review, that study aimed at determining whether high-intensity ST counteracts muscle weakness without increasing spasticity in post-stroke patients and whether ST is effective in improving functional outcomes compared to traditional rehabilitation programs.Table 4 summarizes the ST protocols of the studies included in this review.Although the use of resistance exercises is commonly accepted as an excellent ST method in healthy muscles, the benefits and risks of resistance exercises in post-stroke patients remains a matter of debate [40].Despite the restriction of many physiotherapists regarding the use of muscle strengthening techniques, ST has been shown to increase muscle strength, gait velocity, and functional outcomes and to improve quality of life without exacerbation of spasticity in post-stroke patients [6].Recently, it has been shown that ST appears as the most efficient method for gaining strength in the lower limbs in hemiparetic populations [7].

Conclusion
Despite the observed benefits of ST in hemiparetic patients, this systematic review highlights the lack of standard protocols regarding volume, intensity, frequency, series, and training repetitions.Isotonic exercises are the most commonly used.Thus, it is suggested that more controlled studies should be designed to define the optimal parameters of ST for hemiparetic individuals, which can be used as a reference for treatment personalization.

Figure 1 FIGURE 1 -
Figure1represents a flowchart of search methods for identification and selection of studies.A total of 562 articles were found in the databases, of which 515 were excluded based on the title and abstract.Full text reading of the remaining studies led to the exclusion of another 35 articles, which did not meet the inclusion criteria, because they were not controlled studies, omitted the training protocols, or included another type of protocol combined with ST.A total of 12 articles were included in this review.

Table 1 -
Search strategies for retrieving articles

Table 2 -
Characterization of the studies according to the analyzed outcomes

Table 4 -
Summary of the protocols of the included studies on strength training in hemiparetic patients MMII: knee extensors and flexors, hip flexors, plantar flexors, and dorsiflexors; MMSS: bench press.
Outcomes/measuresDynamometry; timed up and go; six-minute walk test; stair climbing test; sit and stand up test; isokinetic strength; walking speed; peak FC; peak VO2; 1MR; quality of life; balance; scales used to monitor perception of effort; EMG; strength platform.Note: * the MR maximum load and the maximum number of repetitions were considered.MR (maximum repetition); HR (heart rate); VO2 (oxygen consumption); EMG (electromyography).