Resistance Training and Stroke: A Critical Analysis of Different Training Programs

Gambassi, Bruno Bavaresco; Coelho-Junior, Hélio José; Schwingel, Paulo Adriano; Almeida, Fabiano de Jesus Furtado; Gaspar Novais, Tânia Maria; Lauande Oliveira, Paula de Lourdes; Sauaia, Bismarck Ascar; Melo, Cristiane Dominice; Uchida, Marco Carlos; Rodrigues, Bruno

doi:https://doi.org/10.1155/2017/4830265

Stroke Research and Treatment

On this page

Abstract Introduction Materials and Methods Results and Discussion Conclusions Abbreviations Disclosure Conflicts of Interest Authors’ Contributions Acknowledgments References Copyright Related Articles

Review Article | Open Access

Volume 2017 | Article ID 4830265 | https://doi.org/10.1155/2017/4830265

Resistance Training and Stroke: A Critical Analysis of Different Training Programs

Bruno Bavaresco Gambassi,¹Hélio José Coelho-Junior,¹Paulo Adriano Schwingel,²Fabiano de Jesus Furtado Almeida,³Tânia Maria Gaspar Novais,³Paula de Lourdes Lauande Oliveira,³Bismarck Ascar Sauaia,³Cristiane Dominice Melo,³Marco Carlos Uchida,¹and Bruno Rodrigues¹

Academic Editor: David Vaudry

Received19 Aug 2017

Accepted29 Nov 2017

Published20 Dec 2017

Abstract

The aim of this study was to carry out a literature review on the overall benefits of resistance training (RT) after stroke and undertake a critical analysis of the resistance exercise programs surveyed (rest interval between sets and exercises, number of sets, number of repetitions, intensity, duration of training, and weekly frequency). To obtain articles for the review, we searched PubMed, Google Scholar, and Physiotherapy Evidence Database (PEDro). Inclusion criteria were considered using the PICO (population, intervention, control/comparison, and outcome variables) model. The following characteristics were recorded for all articles: type of study, author, year of publication, participants (time after stroke, sample size, and age), benefits of RT, and structured resistance exercise programs. Positive effects of training were found on anxiety status, quality of life, muscle hypertrophy, cognitive function, strength, and muscle power. Only 5 studies described the main variables of RT in detail. Lack of control of some variables of RT may negatively affect the results of this practice. The findings of the present study may further inform health and physical conditioning professionals on the importance and necessity of using the main variables in the search for benefits for individuals with stroke.

1. Introduction

Stroke is generally defined as a neurological loss caused by an abnormal perfusion of brain tissue. The most common types of stroke are intracerebral hemorrhage, subarachnoid hemorrhage, and ischemic (cerebral infarction) [1]. A recent projection from the American Heart Association (AHA) [2] indicated that, by 2030, 3.4 million people aged ≥18 years will have had a clinical diagnosis of stroke. These data deserve concern, once this disease is characterized by a poor prognosis, from—at least—a marked impairment of functional capacity and cardiorespiratory fitness due to central and peripheral mechanisms until early death [3–5]. In fact, in 2013, stroke was the cause of 1 in every 20 deaths in the US, and every 40 seconds someone is affected by this disease [2].

Several risk factors have been suggested to be associated with the physiopathology of stroke, such as hypertension, diabetes mellitus, atrial fibrillation, high triglycerides, tobacco use, inadequate diet, family history and genetics, gender, atherosclerosis, chronic kidney disease, sleep apnea, and physical inactivity [2, 6–16]. Regarding the last one, indeed, not only is physical inactivity known to be associated with the development of some, if not all, of the aforementioned risk factor for stroke, but also data demonstrate that moderately active individuals and highly active individuals have a 20% and 27%, respectively, lower risk stroke incidence than low-active individuals [17].

On the other hand, evidences have demonstrated that exercise training has a strong capacity to collaborate with changes on cardiorespiratory capacity, mobility, cognition, upper and lower limb motor capacity, and balance of stroke survivors [18, 19]. Within the myriad of possibilities with physical training, some researchers have proposed that resistance training (RT)—the kind of exercise that leads muscles to work or hold against an applied weight—may have a key role in the rehabilitation process after stroke as an effective strategy in the treatment of these individuals [20–22]. Much of the expectation around RT is due its capacity to modulate neuromuscular parameters (e.g., muscle mass, strength, and power) in samples composed of individuals who present a similar phenotype to the patient with a stroke, such as older adults who commonly show a nonconducive physiological environment due to neuromuscular denervation, low-grade inflammation, and functional incapacity [23, 24].

In this sense, an increasing number of evidence have been published in the last years demonstrating the benefits of RT in stroke patients. This phenomenon encourages authors to publish a review discussing the potential clinical variables that have not been evaluated in the context of exercise training and are extremely important to be measured in stroke survivors, as, for example, cognition, aphasia, and fatigue to quote a few [18]. Moreover, a recent systematic review with metanalytic regression suggests that most RT studies present a considerable number of biases, strongly limiting possible inferences about the data [19].

In addition to these concerns regarding the internal and external validity of these data, very little has been discussed about the design of the RT programs proposed in these studies. This kind of consideration seems to be important because the manipulation of the RT variables (rest interval between sets and exercises, number of sets, number of repetitions, intensity, duration of training, and weekly frequency) leads to different cardiovascular, metabolic, and neuromuscular responses [25–28]. Furthermore, many healthcare consumers—with or without previous scientific training in exercises sciences—base their clinical practices on exercise training studies. Lastly, it is noteworthy that the effectiveness or not of the RT program is dependent on the organization of its variables. Therefore, we indicate the limitations associated with RT prescription will collaborate with future investigations that aimed to understand the potential of RT to collaborate with rehabilitation in stroke survivors.

Thus, the current study aimed to discuss critically the main aspects regarding the RT prescription in programs with stroke patients, indicating the benefits of this type of training when all variables of importance are fully incorporated, as well as suggesting how studies may be better designed in an attempt to improve their internal and external validity.

2. Materials and Methods

2.1. Data Sources and Searches

Relevant studies were identified through computerized and manual searches. For data collection, PubMed, Google Scholar, and PEDro databases were systematically searched from 2003 until August 2017 (last 15 years). The following keywords were used for our search: stroke, cerebrovascular accident, cerebral vascular accident, resistance exercise, and resistance training. This review is written in accordance with Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.

2.2. Study Selection

The PICO (population, intervention, control/comparison, and outcome variables) model was used for inclusion criteria. Studies were chosen for inclusion if they met the following 4 inclusion criteria: (A) humans of both genders, aged over 18 years with chronic stroke; (B) structured resistance exercise program; (C) randomized controlled trials; (D) health benefits.

The screening was performed by 2 independent reviewers. For each article, any discrepancy between the 2 reviewers was resolved by discussion. In the first screening stage (titles plus abstracts), studies were included when both reviewers agreed they were eligible for inclusion or if there was doubt about whether to exclude them. In the second screening stage (full text), studies were included when both reviewers felt they met all the inclusion criteria.

These reviewers documented the methodological quality of studies and extracted relevant data. The following quality criteria were documented: baseline comparison of groups, randomization, all assessed outcomes, and details of participants (i.e., age, gender, time after stroke, and comorbid conditions).

2.3. Data Extraction

The following characteristics were recorded for all articles: type of study, author, year of publication, participants (time after stroke, sample size, and age), benefits of RT, and structured resistance exercise programs. This procedure was performed by 2 reviewers: one collected the data and the second double-checked it.

3. Results and Discussion

A total of 478 articles were identified initially. In total, 12 peer-reviewed articles were included based on our inclusion criteria. The 12 studies enrolled 424 participants (middle-aged or elderly) with chronic stroke. The extracted study and population characteristics, protocols, and outcomes are shown in Tables 1 and 2.

3.1. Beneficial Effects of Different Designs of RT in Stroke Survivors

The variables investigated could be didactically divided into five large constructs as follows: physical capabilities (i.e., muscle endurance [VO2 max, 6 minutes’ walk distance, and peak aerobic capacity], muscle strength and power, and balance), body composition (i.e., body mass index, muscle mass), cognition (general and executive functions [working memory, verbal fluency tasks, attention, and speed of information processing]), quality of life elements (e.g., anxiety, pain), and blood cardiovascular risk factors (i.e., fasting insulin, HOMA-IR, 2 h plasma glucose, total cholesterol, LDL cholesterol, and HDL cholesterol). All these variables were improved after resistance exercise programs in individuals with stroke.

Tables 1 and 2 depict data about participants, such as time after stroke, sample size and age, type of study, author’s name, year of publication, evaluations of the investigated variables, benefits of RT, and structured resistance training programs (rest interval between sets and exercises, number of sets, number of repetitions, intensity, duration of training, and weekly frequency). Regarding RT methodology and protocols we found the following characteristics: number of exercises, 1 to 7; number of series, 2 to 4; intensity, low, moderate, and high; weekly frequency, 2 to 4 days; duration of the protocol, 5 to 12 weeks; number of repetitions, 6, 8, 10, 15, and 20; and rest interval between sets and exercises when shown, 2 and 3 minutes.

To our knowledge, this is the first review that critically evaluated RT programs used in stroke patients. This research is important to help to inform the healthcare consumers, mainly strength and conditioning professionals, about the need to control the variables of RT in stroke patients. In addition, the present study provides trainers and coaches with examples of well-controlled RT protocols and their benefits on the prognosis of stroke patients [29–33].

The main finding of this literature review lies in the fact that only 5 studies clearly laid out the main variables of RT used. The other 7 randomized controlled trials linking RT to stroke lack any description of rest interval between sets and exercises. According to some researchers, this important variable is widely used in studies involving resistance exercises [34–46]. In this context, we attempted to scrutinize how researchers dealt with the variables involved in RT and the associated benefits for poststroke patients.

Physical capabilities are extremely benefited after RT programs. Interestingly, the different RT designs might elicit different adaptations. Due to the principle of specificity—where it is postulated that a physical capacity is increased when the stimulus is similar to its performance (e.g., muscle strength is improved in response to resistance training)—most studies have focused on the capacity of RT to elicit significant improvements on the neuromuscular tract. This hypothesis has been confirmed, once numerous findings demonstrated that different designs of RT might cause improvements on dynamic, isokinetic, and isometric muscle strength, muscle power, and muscle tone of the nonparetic (muscle strength: +38.2%; muscle power: +28.5–61%) and paretic limbs (muscle strength: +31.4%; muscle power: +33.0–61%) of stroke survivors [31, 32, 47–51]. In fact, the studies differ in the number of repetitions (6–20), sets (2–4), sessions per week (2-3), intensities (low [50% 1RM], moderate [~70% 1RM], and moderate to high/high [80% 1RM]); pattern of muscle contraction (eccentric, concentric, or both), trained limb (paretic, nonparetic, or both).

In an elegant study performed by Lee et al. [52], for example, poststroke patients were submitted to a progressive resistance training program that consisted of two sets of eight repetitions at 50% of 1RM (in the first two weeks) and at 80% of 1RM in the following weeks. To ensure that the participants performed exercises in the target intensity, researchers monitored the perceived exertion through a Borg Perceived Exertion Scale. Results indicated that the progressive RT was able to significantly improve muscle strength, muscle power, and muscle endurance. Furthermore, authors observed that these results were not reached by volunteers that had performed a high-intensity cycling exercise (85% of VO2 peak). Nevertheless, as aforementioned, if a lower intensity was approached, as performed by Ouellette et al. [49], similar improvements in muscle capacity were observed.

It is important to mention that these improvements in muscle strength and power can be associated with elevated walking velocity and performance, balance, and transfer capacity (i.e., timed up and go [TUG]), as demonstrated by Fernandez-Gonzalo et al. [31], Flansbjer et al. [32], Severinsen et al. [48], and Ouellette et al. [49], as well as self-reported function [49]. These data have high external validity because stroke patients commonly show a high prevalence of motor impairment (67.0%), which is associated with poor outcomes, such as low quality of life and falls risk [53, 54], and predominantly characterized by low walking ability (88%), poor balance (51.4%), and dysfunction on mobility (54.1%). Moreover, improvements in self-reported function indicate that stroke patients are feeling better to perform the basic, instrumental, and advanced activities of daily living, probably suffering less with muscle fatigue and weakness.

On the other hand—different from muscle strength, which does not seem to be much influenced by different structures of RT—changes on aerobic capacity may be dependent on the organization of the RT variables. Indeed, Severinsen et al. [48] submitted stroke patients to a classical lower limbs RT program for 12 weeks. The prescription of exercise was based on three sets of 8 repetitions at ~50–80% of 1RM. The findings did not demonstrate significant alterations on aerobic capacity.

When poststroke survivors underwent a moderate to high/high-intensity RT based on three sets of 8 repetitions at 80% of 1RM [52], the authors observed not only an ameliorated muscle strength and power, but also an increased muscle endurance in both limbs—paretic and nonparetic—which was considered as the maximal number of repetitions that the volunteers could achieve in the 30s. Similarly, volunteers of Ivey et al. [47] showed significant improvements in peak oxygen consumption (+6%) and muscle endurance (paretic: +178%; nonparetic: +161%) after a RT program. However, the protocol was based on two sets of 20 repetitions until failure in three exercises for each lower limb member.

These data strongly highlight the importance of the right modulation of RT variables on organic adaptations, mainly the use of specificity in the context of muscle endurance. As stated by Lee et al. [52] daily activities frequently require the capacity to sustain muscle contraction for long periods. Interestingly, muscle endurance was improved after RT program with an elevated intensity (80%) [52], not in concordance with literature, because authors believe that programs with a high number of repetitions and a low intensity, such as that performed by Ivey et al. [47], are more probable to cause this type of adaptation due to biochemical responses. However, it is possible that the threshold to improve muscle endurance in patients with chronic diseases (e.g., stroke) is lower than in healthy patients. The plausibility of this theory is based on the findings that demonstrated increased aerobic capacity in patients with heart failure after RT [55].

The monitoring of morphological parameters is another important clinical aspect in stroke patients, once several evidences have been discussing that a sarcopenic phenotype—characterized by a decreased lean muscle mass followed by impaired muscle strength and/or functionality—is showed by these patients [5, 56]. In nonstroke patients, exercise intensity has a key role in the hypertrophic response to RT, so that most studies have demonstrated that RT programs at moderate to high and high intensities demonstrate a superior capacity to elicit improvements on muscle mass compared with RT programs with lower intensities [57].

In the context of stroke, just a few randomized clinical trials have investigated the impact of different RT programs on morphological parameters. In one of the few studies, Fernandez-Gonzalo et al. [31] decided to investigate the impact of a RT program with an overload on eccentric contractions in the cross-sectional area (CSA) of quadriceps muscle of stroke survivors. This approach is interesting because most interventions focus on muscle contractions composed of concentric and eccentric actions. On the other hand, eccentric muscle contractions have been used as a tool to induce muscle damage, for example, since during this kind of muscle contraction a lower number of fibers are working, leaving the muscle more susceptible to damage, collaborating to the study of delayed onset muscle soreness, inflammation, and hypertrophic response [58–61].

Nevertheless, some groups have proposed that RT programs composed of isolated eccentric contractions might propitiate superior gains in muscle mass and strength compared to concentric training programs [62]. In this sense, stroke survivors were submitted to a RT program based on eccentric overload in a flywheel characterized by 4 sets of 7 maximal knee extensions of the more-affected lower limb.

The findings demonstrated an increased CSA after 12 weeks of RT. This increase in lean muscle mass could help to explain the higher muscle strength and power, as well as walking speed observed in stroke patients undergoing an eccentric RT program in comparison with volunteers who performed a concentric RT program [50], so that taken together data demonstrate a potential superior effectiveness of eccentric RT programs in comparison with concentric RT programs.

However, unfortunately, these are isolated evidences and more studies are still necessary to understand the importance of this kind of muscle contraction in the morphological and neuromuscular parameters of stroke survivors. Furthermore, future studies should utilize protocols of eccentric overload RT training with higher external validity than the proposed one by Fernandez-Gonzalo et al. [31] and Clark and Patten [50] since flywheels and isokinetic equipment are expensive and limited to be used in the context of health promotion.

Regarding cognition, data have demonstrated that stroke patients show cognitive impairment rates range from 20% to 70%, depending on the type of diagnosis [63]. These data deserve concern because this phenomenon indicates that stroke survivors present a high risk to develop dementia [63]. Between the several domains that compose cognition, executive function, which is an essential cognitive domain to maintenance of autonomy and independence during aging [64], seems to be one of the most affected domains after the cerebrovascular event, since evidence suggests that stroke survivors demonstrate a faster decline in this cognitive domain (0.63 points/year) [65].

Intriguingly, even in the face of such data, a recent review indicated that studies are not investigating the impact of RT programs on cognitive parameters of poststroke survivors [18]. In fact, to the best of our knowledge, just one study aimed to investigate this phenomenon. In the trial of Fernandez-Gonzalo et al. [31], an improved executive function (working memory, verbal fluency tasks, attention, and speed of information processing) were observed after the RT program. However, as aforementioned, this study was performed on a specific machine and most studies are still necessary.

After the cerebrovascular event, stroke patients present an increased prevalence of cardiometabolic disorders, leading to an elevated risk of recurrent stroke or other cardiovascular events (e.g., myocardial infarction). In this sense, Zou et al. [66] proposed a RT program based on three sets of 15 repetitions until muscle failure of the leg press, leg extension, and leg curl. This kind of RT training might be beneficial because of two factors: (a) a larger number of repetitions may elicit a larger translocation of glucose transporter 4 (GLUT4) to sarcolemma and, consequently, larger glucose uptake; (b) muscle contractions until failure might elicit a hypertrophic muscular signalization, inducing increase in muscle mass [57], the largest site of glucose uptake in the human organic system. Data demonstrated that several blood cardiovascular risk factors (i.e., fasting insulin, HOMA-IR, 2 h plasma glucose, total, LDL, and HDL cholesterol) were improved after the RT program, regardless of the alterations on body mass.

3.2. What Were the Main Limitations Observed in RT Prescriptions?

The acute and chronic organic responses to RT are dependent on the organization of its variables (rest interval between sets and exercises, number of sets, number of repetitions, intensity, duration of training, and weekly frequency). Regarding the acute effects, patients with and without hypertension, for example, experienced postexercise hypotension (PEH) in RT protocols performed at moderate intensity [67–69]. However, an increasing number of evidences have indicated that exercise cadence might have a key role in this phenomenon [70]. In turn, chronic changes on cognitive parameters do not seem to be intensity-dependent, but time-dependent [71–75]. On the other hand, muscle strength is increased after RT protocols composed of elevated tension [25].

Regardless of its beneficial effects, for a long time, RT was not recommended for patients clinically diagnosed with any cardiovascular diseases [76]. This conduct was assumed because some experiments demonstrated an important increase in blood pressure values during the performance of RT [77]. However, recently, numerous evidences have to indicate that RT may be carried out safely if the variables are controlled [78].

This brief explanation demonstrates the importance of organizing the RT variables for effectiveness and safeness of the exercise program. Stroke survivors are, undoubtedly, patients who deserve special attention during the performance of the exercise training, once they present increased risk of falls, muscle weakness, exacerbated fatigue, autonomic dysfunction, and hemodynamic instability, to quote a few clinical symptoms. Therefore, researchers should perform a detailed explanation about the RT protocols in an attempt to provide the information necessary for healthcare consumers to replicate—within their means—the protocols in their clinical practice. Unfortunately, despite the abovementioned beneficial effects, most studies have failed to detailedly describe the organization of the RT variables. The main limitations include an insufficient or even absent description of the rest intervals between sets and exercises, the name of exercises, the cadence of muscle contraction, and the tools used for RT prescription.

Regarding the description of rest intervals between sets and exercises, this variable was not described in almost all investigations. This is curious because in our clinical practice, as well as in the laboratory, this issue has been extensively discussed because an unsatisfactory rest interval may negatively interfere with expected benefits. As Fleck [37], Kraemer et al. [40], and Ratamess et al. [42] have pointed out, cardiorespiratory and metabolic responses are affected by the duration of intervals of rest between exercises and sets. In addition, rest intervals have a key role in the neuromuscular adaptations as stated by Robinson et al. [44], who demonstrated that greater rest intervals were associated with greater strength gain when compared to shorter intervals.

In the RT protocols of Ouellette et al. [49] and Lee et al. [51, 52], for example, researchers failed to describe the rest intervals among the sets and exercises. However, authors reported that RT sessions were performed at 70–80% of 1RM, which may elicit accumulation of metabolites. This phenomenon might be a problem in the context of stroke, because patients present exacerbated fatigue and muscle weakness, impairing the clearance of metabolic debris. Therefore, it is possible to infer that authors used ≥2 minutes of interval among the series, as recommended for this kind of RT [79]. However, a long interval may not be enough to elicit the necessary stress to cause muscular adaptations. Consequently, the replicability of these studies would be compromised.

Another meaningful aspect is the description of the exercises that were used in the RT program. This occurs because hemiparesis markedly impairs the pattern of movement and, in the clinical practice, the use of specific exercises is not always possible. In fact, we have observed that several adaptations should be performed in the pattern of movement/exercise in order to contemplate the muscular action that can be performed by the patients.

If the purpose of the session of RT was to exercise the pectoralis major, for example, it is possible to infer that researchers had to adapt the exercise to contemplate the muscle group, since stroke patients present several limitations that may make it impossible to conduct the exercise in the machines. Thus, future studies should describe the name of the exercises that were used in the experiments, as well as indicating if any kind of adaptations was performed.

The method used for prescription of RT intensity has been widely discussed not only in the context of exercise as medicine, but also in the sports science field. This occurs because evidence suggests that results on 1RM test for lower limb may variate until 14% of a series of nonsuccessive tests [80].

Curiously, Severinsen et al. [48] reported problems to work with the 1RM method, so that researchers realized that values could be under- and/or overestimated, making the inferences about the zone of intensity difficult where individuals have performed the RT program. Alternatively, Lee et al. [51] in addition to 1RM used a Borg Perceived Exertion Scale, which has been indicated as a valuable tool to exercise prescription [81, 82]. Indeed, RPE allows the adjustment of the load in each session of exercise, differently from the 1RM method, which needs a new battery of evaluations.

However, most researchers have discussed that a previous period of adaptation is necessary before the use of subjective scales. This deserves to be reinforced in patients with stroke because a longer period might be necessary for them since, as aforementioned, they commonly present cognitive impairment. Nevertheless, this issue still must to be investigated.

Lastly, it is noteworthy that some concepts have been wrongly stated. This may lead to wrong conclusions and prescriptions between healthcare consumers. In some studies [49], authors declared that a progressive RT was performed. However, RT intensity was maintained during the whole period. It is important to clarify that a progressive RT is not based on the adjustments on load due to muscular adaptation, but a progressive increase in load—from 50% to 80%, for example—is necessary. This kind of RT was demonstrated in the study by Lee et al. [52]. Furthermore, some authors declared that the RT program was performed at high intensity when the load was around 70% of 1RM. Inferences about high-intensity RT must be made carefully based on these data because most authors declare that training loads at 70% of 1 RM correspond to moderate intensity [83, 84].

Figure 1 shows the minimal amount of information that should be described in experiments that use RT programs.

4. Conclusions

After analyzing the 12 randomized controlled trials, we found that only 5 studies may indeed help health and physical conditioning professionals in exercise prescription for stroke patients, since they did detail and control the main RT variables.

More randomized controlled trials with tight control of the main variables of the RT should be undertaken so that health professionals may be more scientifically informed when prescribing resistance exercises for individuals with stroke. Individuals with stroke may be considered patients at risk; therefore, it is critical to be cautious in exercise prescription. The findings of the present study may further inform health professionals on the importance and necessity of using the main variables (rest interval between sets and exercises, number of sets, number of repetitions, intensity, duration of training, and weekly frequency) in the search for benefits for individuals with stroke.

Abbreviations

1RM:	1-Repetition Maximum
ACSM:	American College of Sports and Medicine
AHA:	American Heart Association
CSA:	Cross-sectional area
GLUT4:	Glucose transporter 4
HDL:	High density lipoprotein
HOMA-IR:	Homeostatic model assessment-insulin resistance
LDL:	Low density lipoprotein
PEDro:	Physiotherapy Evidence Database
PEH:	Postexercise hypotension
PICO:	Population, intervention, control/comparison, and outcome variables
PRISMA:	Preferred Reporting Items for Systematic Reviews and Meta-Analyses
RT:	Resistance training
TUG:	Timed “Up and Go.”

Disclosure

The authors alone are responsible for the content and writing of the paper.

Conflicts of Interest

The authors declare that there are no conflicts of interest regarding the publication of this article

Authors’ Contributions

All authors participated in the development of the research project, analysis and interpretation of the data, and preparation of the manuscript.

Acknowledgments

Bruno Bavaresco Gambassi is grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). Bruno Rodrigues received financial support from CNPq-BPQ.

References

R. L. Sacco, S. E. Kasner, J. P. Broderick et al., “An updated definition of stroke for the 21st century: a statement for healthcare professionals from the American heart association/American stroke association,” Stroke, vol. 44, no. 7, pp. 2064–2089, 2013.
View at: Publisher Site | Google Scholar
D. Mozaffarian, E. J. Benjamin, A. S. Go et al., “Heart Disease and Stroke Statistics2016 Update,” Circulation, vol. 133, no. 4, pp. e38–e360, 2016.
View at: Google Scholar
H. J. Coelho Junior, B. B. Gambassi, T. A. Diniz et al., “Inflammatory mechanisms associated with skeletal muscle sequelae after stroke: role of physical exercise,” Mediators of Inflammation, vol. 2016, Article ID 3957958, 19 pages, 2016.
View at: Publisher Site | Google Scholar
C. English, H. McLennan, K. Thoirs, A. Coates, and J. Bernhardt, “Loss of skeletal muscle mass after stroke: a systematic review,” International Journal of Stroke, vol. 5, no. 5, pp. 395–402, 2010.
View at: Publisher Site | Google Scholar
N. Scherbakov, A. Sandek, and W. Doehner, “Stroke-related sarcopenia: specific characteristics,” Journal of the American Medical Directors Association, vol. 16, no. 4, pp. 272–276, 2015.
View at: Publisher Site | Google Scholar
J. C. Khoury, D. Kleindorfer, K. Alwell et al., “Diabetes mellitus: a risk factor for ischemic stroke in a large biracial population,” Stroke, vol. 44, no. 6, pp. 1500–1504, 2013.
View at: Publisher Site | Google Scholar
P. A. Wolf, R. D. Abbott, and W. B. Kannel, “Atrial fibrillation as an independent risk factor for stroke: the Framingham study,” Stroke, vol. 22, no. 8, pp. 983–988, 1991.
View at: Publisher Site | Google Scholar
R. G. Wieberdink, M. M. F. Poels, M. W. Vernooij et al., “Serum lipid levels and the risk of intracerebral hemorrhage: The Rotterdam study,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 12, pp. 2982–2989, 2011.
View at: Publisher Site | Google Scholar
I. E. Albertsen, L. H. Rasmussen, D. A. Lane et al., “The impact of smoking on thromboembolism and mortality in patients with incident atrial fibrillation :Insights from the danish diet, cancer, and health study,” Chest, vol. 145, no. 3, pp. 559–566, 2014.
View at: Publisher Site | Google Scholar
M. N. McDonnell, S. L. Hillier, S. P. Hooker, A. Le, S. E. Judd, and V. J. Howard, “Physical activity frequency and risk of incident stroke in a National US study of blacks and whites,” Stroke, vol. 44, no. 9, pp. 2519–2524, 2013.
View at: Publisher Site | Google Scholar
R. Estruch, E. Ros, J. Salas-Salvadó et al., “Primary prevention of cardiovascular disease with a Mediterranean diet,” The New England Journal of Medicine, vol. 368, no. 14, pp. 1279–1290, 2013.
View at: Publisher Site | Google Scholar
C. Bellenguez, S. Bevan, A. Gschwendtner et al., “Genome-wide association study identifies a variant in HDAC9 associated with large vessel ischemic stroke,” Nature genetics, vol. 44, no. 3, pp. 328–333, 2012.
View at: Google Scholar
O. M. Gutiérrez, S. E. Judd, P. Muntner et al., “Racial differences in albuminuria, kidney function, and risk of stroke,” Neurology, vol. 79, no. 16, pp. 1686–1692, 2012.
View at: Publisher Site | Google Scholar
S. Redline, G. Yenokyan, D. J. Gottlieb et al., “Obstructive sleep apnea-hypopnea and incident stroke: the sleep heart health study,” American Journal of Respiratory and Critical Care Medicine, vol. 182, no. 2, pp. 269–277, 2010.
View at: Publisher Site | Google Scholar
S. Seshadri, A. Beiser, M. Kelly-Hayes et al., “The lifetime risk of stroke: estimates from the framingham study,” Stroke, vol. 37, no. 2, pp. 345–350, 2006.
View at: Publisher Site | Google Scholar
B. I. Lee, H. S. Nam, J. H. Heo, and D. I. Kim, “Yonsei Stroke Registry. Analysis of 1,000 patients with acute cerebral infarctions,” Cerebrovascular Disease, vol. 12, no. 3, pp. 145–151, 2001.
View at: Publisher Site | Google Scholar
C. D. Lee, A. R. Folsom, and S. N. Blair, “Physical activity and stroke risk: A meta-analysis,” Stroke, vol. 34, no. 10, pp. 2475–2481, 2003.
View at: Publisher Site | Google Scholar
D. H. Saunders, C. A. Greig, and G. E. Mead, “Physical activity and exercise after stroke: review of multiple meaningful benefits,” Stroke, vol. 45, no. 12, pp. 3742–3747, 2014.
View at: Publisher Site | Google Scholar
D. H. Saunders, M. Sanderson, S. Hayes et al., “Physical Fitness Training for Patients with Stroke,” Stroke, vol. 47, no. 9, pp. e219–e220, 2016.
View at: Publisher Site | Google Scholar
J. E. Harris and J. J. Eng, “Strength training improves upper-limb function in individuals with stroke: A meta-analysis,” Stroke, vol. 41, no. 1, pp. 136–140, 2010.
View at: Publisher Site | Google Scholar
S. Mehta, S. Pereira, R. Viana et al., “Resistance training for gait speed and total distance walked during the chronic stage of stroke: A meta-analysis,” Topics in Stroke Rehabilitation, vol. 19, no. 6, pp. 471–478, 2012.
View at: Publisher Site | Google Scholar
S. Wist, J. Clivaz, and M. Sattelmayer, “Muscle strengthening for hemiparesis after stroke: A meta-analysis,” Annals of Physical and Rehabilitation Medicine, vol. 59, no. 2, pp. 114–124, 2016.
View at: Publisher Site | Google Scholar
M. R. Deschenes, “Effects of aging on muscle fibre type and size,” Sports Medicine, vol. 34, no. 12, pp. 809–824, 2004.
View at: Publisher Site | Google Scholar
P. Aagaard, C. Suetta, P. Caserotti, S. P. Magnusson, and M. Kjær, “Role of the nervous system in sarcopenia and muscle atrophy with aging: Strength training as a countermeasure,” Scandinavian Journal of Medicine & Science in Sports, vol. 20, no. 1, pp. 49–64, 2010.
View at: Publisher Site | Google Scholar
V. I. Kalapotharakos, M. Michalopoulos, S. P. Tokmakidis, G. Godolias, and V. Gourgoulis, “Effects of a heavy and a moderate resistance training on functional performance in older adults,” Journal of Strength & Conditioning Research, vol. 19, no. 3, pp. 652–657, 2005.
View at: Publisher Site | Google Scholar
V. A. Cornelissen and N. A. Smart, “Exercise training for blood pressure: a systematic review and meta-analysis,” Journal of the American Heart Association, vol. 2, no. 1, Article ID e004473, 2013.
View at: Publisher Site | Google Scholar
W. J. Chodzko-Zajko, D. N. Proctor, M. A. Fiatarone Singh et al., “Exercise and physical activity for older adults,” Medicine & Science in Sports & Exercise, vol. 41, no. 7, pp. 1510–1530, 2009.
View at: Publisher Site | Google Scholar
C. E. Garber, B. Blissmer, M. R. Deschenes et al., “Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise,” Medicine & Science in Sports & Exercise, vol. 43, no. 7, pp. 1334–1359, 2011.
View at: Publisher Site | Google Scholar
F. J. Aidar, R. J. De Oliveira, A. J. Silva et al., “The influence of resistance exercise training on the levels of anxiety in ischemic stroke,” Stroke Research and Treatment, vol. 2012, Article ID 298375, 6 pages, 2012.
View at: Publisher Site | Google Scholar
F. J. Aidar, R. J. de Oliveira, D. G. de Matos et al., “A randomized trial investigating the influence of strength training on quality of life in ischemic stroke,” Topics in Stroke Rehabilitation, vol. 23, no. 2, pp. 84–89, 2016.
View at: Publisher Site | Google Scholar
R. Fernandez-Gonzalo, S. Fernandez-Gonzalo, M. Turon, C. Prieto, P. A. Tesch, and M. D. C. García-Carreira, “Muscle, functional and cognitive adaptations after flywheel resistance training in stroke patients: A pilot randomized controlled trial,” Journal of NeuroEngineering and Rehabilitation, vol. 13, no. 1, 2016.
View at: Publisher Site | Google Scholar
U.-B. Flansbjer, M. Miller, D. Downham, and J. Lexell, “Progressive resistance training after stroke: effects on muscle strength, muscle tone, gait performance and perceived participation,” Journal of Rehabilitation Medicine, vol. 40, no. 1, pp. 42–48, 2008.
View at: Publisher Site | Google Scholar
U.-B. Flansbjer, J. Lexell, and C. Brogårdh, “Long-term benefits of progressive resistance training in chronic stroke: a 4-year follow-up,” Journal of Rehabilitation Medicine, vol. 44, no. 3, pp. 218–221, 2012.
View at: Publisher Site | Google Scholar
J. P. Ahtiainen, A. Pakarinen, M. Alen, W. J. Kraemer, and K. Häkkinen, “Short vs. long rest period between the sets in hypertrophic resistance training: Influence on muscle strength, size, and hormonal adaptations in trained men,” The Journal of Strength and Conditioning Research, vol. 19, no. 3, pp. 572–582, 2005.
View at: Publisher Site | Google Scholar
American college of sports medicine, “American College of Sports Medicine position stand, Progression models in resistance training for healthy adults,” Medicine and Science in Sports And Exercise, vol. 41, no. 3, pp. 687–708, 2009.
View at: Publisher Site | Google Scholar
B. A. Comstock, G. A. Thomas, C. Dunn-Lewis et al., “Effects of acute resistance exercise on muscle damage and perceptual measures between men WHO are lean and obese,” The Journal of Strength and Conditioning Research, vol. 27, no. 12, pp. 3488–3494, 2013.
View at: Publisher Site | Google Scholar
S. J. Fleck, “Cardiovascular adaptations to resistance training,” Medicine & Science in Sports & Exercise, vol. 20, no. 5, pp. S146–S151, 1988.
View at: Publisher Site | Google Scholar
K. R. Heavens, T. K. Szivak, D. R. Hooper et al., “The effects of high intensity short rest resistance exercise on muscle damage markers in men and women,” The Journal of Strength and Conditioning Research, vol. 28, no. 4, pp. 1041–1049, 2014.
View at: Publisher Site | Google Scholar
W. J. Kraemer, B. J. Noble, M. J. Clark, and B. W. Culver, “Physiologic responses to heavy-resistance exercise with very short rest periods,” International Journal of Sports Medicine, vol. 8, no. 4, pp. 247–252, 1987.
View at: Publisher Site | Google Scholar
W. J. Kraemer, N. A. Ratamess, and B. C. Nindl, “Recovery responses of testosterone, growth hormone, and IGF-1 after resistance exercise,” Journal of Applied Physiology, vol. 122, no. 3, pp. 549–558, 2017.
View at: Publisher Site | Google Scholar
D. L. Mayhew, J. P. Thyfault, and A. J. Koch, “Rest-interval length affects leukocyte levels during heavy resistance exercise,” The Journal of Strength and Conditioning Research, vol. 19, no. 1, pp. 16–22, 2005.
View at: Publisher Site | Google Scholar
N. A. Ratamess, M. J. Falvo, G. T. Mangine, J. R. Hoffman, A. D. Faigenbaum, and J. Kang, “The effect of rest interval length on metabolic responses to the bench press exercise,” European Journal of Applied Physiology, vol. 100, no. 1, pp. 1–17, 2007.
View at: Publisher Site | Google Scholar
N. A. Ratamess, C. M. Chiarello, A. J. Sacco et al., “The effects of rest interval length manipulation of the first upper-body resistance exercise in sequence on acute performance of subsequent exercises in men and women,” The Journal of Strength and Conditioning Research, vol. 26, no. 11, pp. 2929–2938, 2012.
View at: Publisher Site | Google Scholar
J. M. Robinson, M. H. Stone, and R. L. Johnson, “Effects of Different Weight Training Exercise/Rest Intervals on Strength, Power, and High Intensity Exercise Endurance,” The Journal of Strength Conditioning Research, vol. 9, no. 4, pp. 216–221, 1995.
View at: Google Scholar
F. E. Rossi, J. Gerosa-Neto, N. E. Zanchi, J. M. Cholewa, and F. S. Lira, “Impact of Short and Moderate Rest Intervals on the Acute Immunometabolic Response to Exhaustive Strength Exercise: Part i,” The Journal of Strength and Conditioning Research, vol. 30, no. 6, pp. 1563–1569, 2016.
View at: Publisher Site | Google Scholar
T. K. Szivak, D. R. Hooper, C. Dunn-Lewis et al., “Adrenal cortical responses to high-intensity, short rest, resistance exercise in men and women,” The Journal of Strength and Conditioning Research, vol. 27, no. 3, pp. 748–760, 2013.
View at: Publisher Site | Google Scholar
F. M. Ivey, S. J. Prior, C. E. Hafer-Macko, L. I. Katzel, R. F. Macko, and A. S. Ryan, “Strength Training for Skeletal Muscle Endurance after Stroke,” Journal of Stroke and Cerebrovascular Diseases, vol. 26, no. 4, pp. 787–794, 2017.
View at: Publisher Site | Google Scholar
K. Severinsen, J. K. Jakobsen, A. R. Pedersen, K. Overgaard, and H. Andersen, “Effects of resistance training and aerobic training on ambulation in chronic stroke,” American Journal of Physical Medicine & Rehabilitation, vol. 93, no. 1, pp. 29–42, 2014.
View at: Publisher Site | Google Scholar
M. M. Ouellette, N. K. LeBrasseur, J. F. Bean et al., “High-intensity resistance training improves muscle strength, self-reported function, and disability in long-term stroke survivors,” Stroke, vol. 35, no. 6, pp. 1404–1409, 2004.
View at: Publisher Site | Google Scholar
D. J. Clark and C. Patten, “Eccentric versus concentric resistance training to enhance neuromuscular activation and walking speed following stroke,” Neurorehabilitation and Neural Repair, vol. 27, no. 4, pp. 335–344, 2013.
View at: Publisher Site | Google Scholar
M. J. Lee, S. L. Kilbreath, M. F. Singh et al., “Comparison of effect of aerobic cycle training and progressive resistance training on walking ability after stroke: a randomized sham exercise-controlled study,” Journal of the American Geriatrics Society, vol. 56, no. 6, pp. 976–985, 2008.
View at: Publisher Site | Google Scholar
M.-J. Lee, S. L. Kilbreath, M. F. Singh, B. Zeman, and G. M. Davis, “Effect of Progressive Resistance Training on Muscle Performance after Chronic Stroke,” Medicine & Science in Sports & Exercise, vol. 42, no. 1, pp. 23–34, 2010.
View at: Publisher Site | Google Scholar
B. P. B. Carvalho-Pinto and C. D. C. M. Faria, “Health, function and disability in stroke patients in the community,” Brazilian Journal of Physical Therapy, vol. 20, no. 4, pp. 355–366, 2016.
View at: Publisher Site | Google Scholar
M. A. Muren, M. Hütler, and J. Hooper, “Functional capacity and health-related quality of life in individuals post stroke,” Topics in Stroke Rehabilitation, vol. 15, no. 1, pp. 51–58, 2008.
View at: Publisher Site | Google Scholar
C. T. Pu, M. T. Johnson, D. E. Forman et al., “Randomized trial of progressive resistance training to counteract the myopathy of chronic heart failure,” Journal of Applied Physiology, vol. 90, no. 6, pp. 2341–2350, 2001.
View at: Google Scholar
N. Scherbakov, S. von Haehling, S. D. Anker, U. Dirnagl, and W. Doehner, “Stroke induced Sarcopenia: muscle wasting and disability after stroke,” International Journal of Cardiology, vol. 170, no. 2, pp. 89–94, 2013.
View at: Publisher Site | Google Scholar
B. J. Schoenfeld, “The mechanisms of muscle hypertrophy and their application to resistance training,” Journal of Strength & Conditioning Research, vol. 24, no. 10, pp. 2857–2872, 2010.
View at: Publisher Site | Google Scholar
R. Barroso, H. Roschel, C. Ugrinowitsch, R. Araújo, K. Nosaka, and V. Tricoli, “Effect of eccentric contraction velocity on muscle damage in repeated bouts of elbow flexor exercise,” Applied Physiology, Nutrition, and Metabolism, vol. 35, no. 4, pp. 534–540, 2010.
View at: Publisher Site | Google Scholar
H. Roschel, C. Ugrinowistch, R. Barroso et al., “Effect of eccentric exercise velocity on akt/mtor/p70s6k signaling in human skeletal muscle,” Applied Physiology, Nutrition, and Metabolism, vol. 36, no. 2, pp. 283–290, 2011.
View at: Publisher Site | Google Scholar
J. Peake, K. Nosaka, and K. Suzuki, “Characterization of inflammatory responses to eccentric exercise in humans,” Exercise Immunology Review, vol. 11, pp. 64–85, 2005.
View at: Google Scholar
J. M. Peake, O. Neubauer, P. A. D. Gatta, and K. Nosaka, “Muscle damage and inflammation during recovery from exercise,” Journal of Applied Physiology, vol. 122, no. 3, pp. 559–570, 2017.
View at: Publisher Site | Google Scholar
M. Roig, K. O'Brien, G. Kirk et al., “The effects of eccentric versus concentric resistance training on muscle strength and mass in healthy adults: a systematic review with meta-analysis,” British Journal of Sports Medicine, vol. 43, no. 8, pp. 556–568, 2009.
View at: Publisher Site | Google Scholar
J.-H. Sun, L. Tan, and J.-T. Yu, “Post-stroke cognitive impairment: epidemiology, mechanisms and management,” Annals of Translational Medicine, vol. 2, no. 8, article 80, 2014.
View at: Publisher Site | Google Scholar
S. M. Borges, M. Radanovic, and O. V. Forlenza, “Functional mobility in a divided attention task in older adults with cognitive impairment,” Journal of Motor Behavior, vol. 47, no. 5, pp. 378–385, 2015.
View at: Publisher Site | Google Scholar
D. A. Levine, A. T. Galecki, K. M. Langa et al., “Trajectory of cognitive decline after incident stroke,” Journal of the American Medical Association, vol. 314, no. 1, pp. 41–51, 2015.
View at: Publisher Site | Google Scholar
J. Zou, Z. Wang, Q. Qu, and L. Wang, “Resistance Training Improves Hyperglycemia and Dyslipidemia, Highly Prevalent Among Nonelderly, Nondiabetic, Chronically Disabled Stroke Patients,” Archives of Physical Medicine and Rehabilitation, vol. 96, no. 7, Article ID 56144, pp. 1291–1296, 2015.
View at: Publisher Site | Google Scholar
M. Macedo, A. S. Silva, R. R. Olher, H. J. Coelho Junior, R. Palmeira, and R. Y. Asano, “Post-exercise hypotension between different protocols of resistance training for beginners,” Journal of Exercise Physiology-online, vol. 17, no. 6, pp. 58–65, 2014.
View at: Google Scholar
T. Figueiredo, J. M. Willardson, H. Miranda, C. M. Bentes, V. M. Reis, and R. Simão, “Influence of load intensity on postexercise hypotension and heart rate variability after a strength training session,” The Journal of Strength and Conditioning Research, vol. 29, no. 10, pp. 2941–2948, 2015.
View at: Publisher Site | Google Scholar
B. B. Gambassi, B. Rodrigues, F. de Jesus Furtado Almeida et al., “Acute effect of resistance training without recovery intervals on the blood pressure of comorbidity-free elderly women: a pilot study,” Sport Sciences for Health, vol. 12, no. 3, pp. 315–320, 2016.
View at: Publisher Site | Google Scholar
H. J. Coelho-J, M. C. Irigoyen, da. Silva Aguiar et al., “Acute effects of power and resistance exercises on hemodynamic measurements of older women,” Clinical Interventions in Aging, vol. 12, p. 1103, 2017.
View at: Publisher Site | Google Scholar
T. Liu-Ambrose and M. G. Donaldson, “Exercise and cognition in older adults: Is there a role for resistance training programmes?” British Journal of Sports Medicine, vol. 43, no. 1, pp. 25–27, 2009.
View at: Publisher Site | Google Scholar
C. J. Liu and N. K. Latham, Progressive resistance strength training for improving physical function in older adults, The Cochrane Library, 2009.
T. Liu-Ambrose, L. S. Nagamatsu, P. Graf, B. L. Beattie, M. C. Ashe, and T. C. Handy, “Resistance training and executive functions: a 12-month randomized controlled trial,” JAMA Internal Medicine, vol. 170, no. 2, pp. 170–178, 2010.
View at: Publisher Site | Google Scholar
T. Liu-Ambrose, L. S. Nagamatsu, M. W. Voss, K. M. Khan, and T. C. Handy, “Resistance training and functional plasticity of the aging brain: a 12-month randomized controlled trial,” Neurobiology of Aging, vol. 33, no. 8, pp. 1690–1698, 2012.
View at: Publisher Site | Google Scholar
R. C. Cassilhas, V. A. R. Viana, V. Grassmann et al., “The impact of resistance exercise on the cognitive function of the elderly,” Medicine & Science in Sports and Exercise, vol. 39, no. 8, pp. 1401–1407, 2007.
View at: Publisher Site | Google Scholar
C. G. S. de Araújo, C. V. Duarte, F. D. A. Gonçalves, H. B. de Oliveira Medeiros, F. A. Lemos, and A. L. Gouvêa, “Hemodynamic responses to an isometric handgrip training protocol,” Arquivos Brasileiros de Cardiologia, vol. 97, no. 5, pp. 413–418, 2011.
View at: Publisher Site | Google Scholar
S. J. Fleck and L. S. Dean, “Resistance-training experience and the pressor response during resistance exercise,” Journal of Applied Physiology, vol. 63, no. 1, pp. 116–120, 1987.
View at: Google Scholar
A. C. Paulo, V. Tricoli, and A. C. Queiroz, “Blood pressure response during resistance training of different work to rest ratio,” The Journal of Strength Conditioning Research, 2017.
View at: Publisher Site | Google Scholar
W. J. Kraemer and N. A. Ratamess, “Fundamentals of resistance training: progression and exercise prescription,” Medicine & Science in Sports & Exercise, vol. 36, no. 4, pp. 674–688, 2004.
View at: Publisher Site | Google Scholar
M. J. Benton, P. D. Swan, and M. D. Peterson, “Evaluation of multiple one repetition maximum strength trials in untrained women,” The Journal of Strength and Conditioning Research, vol. 23, no. 5, pp. 1503–1507, 2009.
View at: Publisher Site | Google Scholar
M. L. Day, M. R. McGuigan, G. Brice, and C. Foster, “Monitoring exercise intensity during resistance training using the session RPE scale,” The Journal of Strength and Conditioning Research, vol. 18, no. 2, pp. 353–358, 2004.
View at: Publisher Site | Google Scholar
M. C. Uchida, L. F. Teixeira, V. J. Godoi et al., “Does the timing of measurement alter session-RPE in boxers?” Journal of Sports Science and Medicine, vol. 13, no. 1, pp. 59–65, 2014.
View at: Google Scholar
J. J. Hulmi, S. Walker, J. P. Ahtiainen, K. Nyman, W. J. Kraemer, and K. Häkkinen, “Molecular signaling in muscle is affected by the specificity of resistance exercise protocol,” Scandinavian Journal of Medicine & Science in Sports, vol. 22, no. 2, pp. 240–248, 2012.
View at: Publisher Site | Google Scholar
H. V. MacDonald, B. T. Johnson, T. B. Huedo-Medina et al., “Dynamic resistance training as stand-alone antihypertensive lifestyle therapy: A meta-analysis,” Journal of the American Heart Association, vol. 5, no. 10, Article ID e003231, 2016.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2017 Bruno Bavaresco Gambassi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies