Aerobic, Resistance, and Cognitive Exercise Training Poststroke
2015; Lippincott Williams & Wilkins; Volume: 46; Issue: 7 Linguagem: Inglês
10.1161/strokeaha.114.006649
ISSN1524-4628
AutoresEduard Tiozzo, Mehdi Youbi, Kunjan R. Dave, Miguel A. Pérez‐Pinzón, Tatjana Rundek, Ralph L. Sacco, David Loewenstein, John E. Lewis, Clinton B. Wright,
Tópico(s)Balance, Gait, and Falls Prevention
ResumoHomeStrokeVol. 46, No. 7Aerobic, Resistance, and Cognitive Exercise Training Poststroke Free AccessResearch ArticlePDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessResearch ArticlePDF/EPUBAerobic, Resistance, and Cognitive Exercise Training Poststroke Eduard Tiozzo, PhD, Mehdi Youbi, MD, Kunjan Dave, PhD, Miguel Perez-Pinzon, PhD, Tatjana Rundek, MD, PhD, Ralph L. Sacco, MD, MS, David Loewenstein, PhD, John E. Lewis, PhD and Clinton B. Wright, MD, MS Eduard TiozzoEduard Tiozzo From the Evelyn F. McKnight Brain Institute (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and the Departments of Neurology (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and Psychiatry and Behavioral Sciences (E.T., D.L., J.E.L.), University of Miami Miller School of Medicine, Miami, FL. , Mehdi YoubiMehdi Youbi From the Evelyn F. McKnight Brain Institute (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and the Departments of Neurology (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and Psychiatry and Behavioral Sciences (E.T., D.L., J.E.L.), University of Miami Miller School of Medicine, Miami, FL. , Kunjan DaveKunjan Dave From the Evelyn F. McKnight Brain Institute (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and the Departments of Neurology (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and Psychiatry and Behavioral Sciences (E.T., D.L., J.E.L.), University of Miami Miller School of Medicine, Miami, FL. , Miguel Perez-PinzonMiguel Perez-Pinzon From the Evelyn F. McKnight Brain Institute (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and the Departments of Neurology (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and Psychiatry and Behavioral Sciences (E.T., D.L., J.E.L.), University of Miami Miller School of Medicine, Miami, FL. , Tatjana RundekTatjana Rundek From the Evelyn F. McKnight Brain Institute (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and the Departments of Neurology (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and Psychiatry and Behavioral Sciences (E.T., D.L., J.E.L.), University of Miami Miller School of Medicine, Miami, FL. , Ralph L. SaccoRalph L. Sacco From the Evelyn F. McKnight Brain Institute (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and the Departments of Neurology (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and Psychiatry and Behavioral Sciences (E.T., D.L., J.E.L.), University of Miami Miller School of Medicine, Miami, FL. , David LoewensteinDavid Loewenstein From the Evelyn F. McKnight Brain Institute (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and the Departments of Neurology (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and Psychiatry and Behavioral Sciences (E.T., D.L., J.E.L.), University of Miami Miller School of Medicine, Miami, FL. , John E. LewisJohn E. Lewis From the Evelyn F. McKnight Brain Institute (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and the Departments of Neurology (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and Psychiatry and Behavioral Sciences (E.T., D.L., J.E.L.), University of Miami Miller School of Medicine, Miami, FL. and Clinton B. WrightClinton B. Wright From the Evelyn F. McKnight Brain Institute (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and the Departments of Neurology (E.T., M.Y., K.D., M.P.-P., T.R., R.L.S., C.B.W.) and Psychiatry and Behavioral Sciences (E.T., D.L., J.E.L.), University of Miami Miller School of Medicine, Miami, FL. Originally published26 May 2015https://doi.org/10.1161/STROKEAHA.114.006649Stroke. 2015;46:2012–2016Other version(s) of this articleYou are viewing the most recent version of this article. Previous versions: January 1, 2015: Previous Version 1 Stroke may cause physical or cognitive impairments. Approximately 50% to 75% of all stroke survivors have residual motor or cognitive disabilities that prevent them from living independently. Muscle weakness is considered a major cause of motor disability in stroke patients.1 Impaired walking occurs in as many as 80% of individuals immediately after stroke,2 with muscle weakness in the paretic limb explaining ≤50% of the variance in gait among individuals with chronic mild-to-moderate poststroke hemiparesis.3 As a result, gait patterns become asymmetrical and gait speed reduced.4 Additionally, impaired walking is commonly observed beyond 6 months after stroke.5 This lack of walking competency can precipitate and exacerbate a sedentary lifestyle and cardiovascular deconditioning.Previous work has shown that maximal oxygen consumption (VO2max), as a measurement of cardiovascular fitness, is reduced to 10 to 17 mL/kg/min within the first month after stroke6 and remains below 20 mL/kg/min beyond 6 months.7 The same values can be 45% lower than in age-matched and healthy individuals.8 The implication of low VO2max becomes even more important knowing that a minimum of 20 mL/kg/min is needed for performing daily activities9 and for independent living among older stroke patients.10 In addition to stroke-related decline in cardiovascular fitness, a natural decline in VO2max occurs after the age of 50, averaging a 5% to 10% (or ≈ 5 mL/kg/min) loss per decade. Therefore, elderly stroke patients may face disease- and age-related declines in cardiorespiratory fitness.In a meta-analysis of 11 studies (n=1105), low physical activity (PA) levels, for example, 4355 daily steps taken, have been observed among stroke patients.11 People with other chronic diseases, such as chronic pulmonary obstructive disease, have reported as few as 2237 steps a day.12 The medical establishment, including the American Heart Association, recommends 10 000 steps a day, which is not easily achievable through routine daily activities, and requires additional effort even by healthy individuals. Observational data from America on the Move reported that over 1000 healthy adults took an average of 5117 steps per day.13 Thus, reduced physical inactivity in stroke patients, compared with healthy individuals, can further compromise their cardiorespiratory fitness and walking ability.Impaired cognitive processes in perception, attention, executive function, memory, and language affect almost two-thirds of stroke patients.14 It is also estimated that ≤32% of patients can have persistent cognitive impairment ≤3 years after the first stroke.15 Such impairments can reduce a person's independence in performing basic (eg, eating and dressing) and instrumental (eg, housework and social interaction) activities of daily living (ADLs)16 and increase risk of mortality17 and dementia.18As a vulnerable patient population that is at risk for accelerated functional decline, stroke survivors may benefit from cognitive training and increased PA. However, the extent of those benefits and the ability of stroke patients to tolerate physical exercise programs of varying intensity after stroke are less understood, as is the optimal timing after the event. Similarly, the potential benefits of cognitive training after stroke need further study regarding timing, key cognitive domains to be emphasized, and duration of therapy. In this review, we summarize the effects of increased PA and exercise or cognitive training poststroke.Exercise ModalitiesThe effectiveness of increased PA and exercise in the primary and secondary prevention of a variety of conditions and diseases is evident. More specifically, these benefits include lower body weight, better control of hypertension, glucose tolerance, improved lipid profiles, and an overall reduction in the risk of cardiovascular disease, diabetes mellitus, colon and breast cancer, osteoporosis, osteoarthritis, depression, and anxiety.19 The benefits of increased PA have also been observed in stroke prevention, with highly active individuals exhibiting a 21% lower risk of ischemic strokes and a 34% lower risk of hemorrhagic stroke.20 Despite a considerable effect of increased PA on stroke, the overall evidence of its therapeutic effect on morbidity and mortality after stroke is still surprisingly weak.21Exercise training programs are classified as aerobic exercise (AE) for improving cardiovascular fitness, resistance exercise (RE) for improving muscular strength and power, and combined AE and RE training (CARET). Based on epidemiological studies, it is clear that AE and RE independently have distinct clinical and public health implications. For example, mechanical loading forces on the bones are essential for osteogenic responses that can lead to improved bone mineral density and reduced risk of osteoporosis. Although mechanical loading with RE results in enhanced bone metabolism, the same benefits of AE are often absent or modest.22 Conversely, a meta-analysis of the effect of different types of exercise on visceral adipose tissue, responsible for a cascade of metabolic disturbances, reported effective lowering of visceral adipose tissue with AE, whereas RE failed to induce significant reduction.23 Moreover, CARET results in greater reduction of glycosylated hemoglobin and risk of diabetes mellitus, compared with AE or RE alone.24 For that reason, public health guidelines recommend that adults engage in both exercise modalities.Regardless of the proven benefits of RE, most exercise interventions primarily implement AE training protocols. However, it is still unclear whether CARET or AE or RE alone demonstrate better improvements among stroke patient populations.Exercise and Cognitive FunctionExercise may have physiological effects capable of reducing the risk of cognitive decline, but data on stroke survivors are limited. Several beneficial mechanisms have been hypothesized in the relatively small number of human clinical trials, including a reduction of stress-related damage and attenuation of vascular risk. The social interaction of exercise may also have a positive impact on cognition.25 Finally, it has been suggested that exercise training enhances brain plasticity through increased cerebral perfusion and upregulation of brain-derived neurotrophic factor, a protein strongly linked to neurogenesis and dendritic expansion. Elevated levels of brain-derived neurotrophic factor have also been associated with larger hippocampal volumes and enhanced learning and memory function.26 A positive association between aerobic fitness and hippocampal volumes has been observed predominantly in animal models with less evidence from human studies.27 However, one randomized controlled trial (n=120)28 and one observational study (n=165)29 demonstrated AE-induced increases in hippocampal volumes as well as improved memory among older adults (>55 years) without dementia. The literature on the specific pathways through which RE may influence cognition is limited, and one meta-analysis found greater improvements in cognition from CARET over AE training alone.30 Despite the well-known benefits of exercise on multiple organ systems, our knowledge about the link between exercise and the brain is limited with some evidence that increased PA enhances cognitive performance poststroke.31Large well-designed clinical trials are needed to address the extent of potential benefits from different exercise programs and their parameters (ie, intensity, frequency, and duration) for cognition after stroke.Aerobic ExerciseMost exercise interventions in stroke survivors still predominantly implement AE protocols with a cycle ergometer as the preferred mode. Evidence shows that many stroke patients do not walk well enough to achieve sufficient improvements in cardiovascular function.32 Lower values of both VO2max and maximum heart rate (HRmax) have been consistently observed during cycle ergometer versus treadmill exercise.33 For that reason, the training intensities implemented in AE have been lowered for the cycle ergometer, compared with treadmill protocols (50% to 70% HRmax versus 50% to 85% HRmax), and the same finding should be translated into the clinical setting. Overall, cardiorespiratory fitness improves after AE training protocols of at least 8 to 12 weeks (intensity 50% to 80% of HRmax; 3–5 days/week; 20–40 minutes) in patients with mild to moderate stroke.9,34 The magnitude of changes in VO2max among stroke patients is similar to healthy sedentary adults or participants in cardiac rehabilitation (12.5% versus 10% to 30% versus 13% to 15%, respectively).35 Even if the observed improvements are small in absolute terms (eg, ≈1 mL/kg/min),36 considering low baseline fitness levels, the same improvements can have significant functional carryover for stroke survivors. In addition to improved cardiorespiratory capacity, one systematic review36 supported the idea that AE improves gait velocity and capacity in randomized trials involving ≤133 mildly to moderately affected stroke patients. This benefit may be even more evident with task-oriented therapy (ie, strengthening the lower extremities, enhancing walking balance and speed, or treadmill walking at higher intensity) reported in 2 randomized controlled trials with exercise sessions performed for 6 weeks (n=91; >1 year poststroke)37 and 6 months (n=91; >6 months poststroke).38 Although AE seems to lead to improvements in functional capacity, the effect of the same training modality on cognition is still unclear and insufficiently investigated.Safety is an important concern in exercise studies involving stroke patients. A 6% recurrent stroke rate has been reported in an AE intervention group,39 with the same rate being comparable to the recurrent stroke risk in the general population.40 The fact that major adverse events in stroke studies have not been directly attributed to AE training is encouraging and raises the possibility of starting exercise training (and testing) in the early period after stroke (<7 days poststroke).Future stroke studies involving AE training should determine optimal protocols for individuals with different physical limitations and cardiovascular risk. The research should focus on feasibility and the long-term effects of AE on cardiorespiratory fitness and functional capacity, as well as on cognitive functioning and health-related quality of life.Resistance ExerciseRoughly twice as many AE training studies, compared with RE protocols, have been performed in stroke patients.9 Even though RE has been included in national guidelines and recommended for general health promotion, it remains an understudied and underappreciated exercise modality in stroke. Exercise frequency in RE studies of stroke has varied from 2 to 5 weekly sessions and from 4 to 12 weeks in length. These studies incorporated progressive RE, a method that increases the overload of resistance, thus demanding additional muscle force production. RE training in stroke has been shown to improve muscle strength in the lower extremities in 24 stroke participants (mean age 61 years; ≈20 months poststroke) after 10 weeks and in 42 stroke participants (mean age 66 years; 6 months to 6 years poststroke) after 12 weeks.41,42 Increased weight-bearing (on the affected leg) and gait speed were demonstrated in subacute poststroke after only 4 weeks of RE. The same improvements were greater in individuals (n=8) undergoing functional strength training that focused on power, balance, and weight-bearing exercises compared with a traditional RE protocol (n=10) that focused on improving muscle tone and avoiding excessive muscle power.1 However, the increase in muscle strength does not always translate into significant improvements in walking and health-related quality of life.43In a 1-year randomized controlled trial involving over 100 healthy individuals, RE compensated for the equivalent age-related strength losses over 3 to 5 years. Interestingly, the training-induced benefits of the same RE training extended to 7 years after cessation of the study.44 In addition to being understudied, RE interventions involving stroke patients have been shorter in duration and smaller in sample size compared with AE intervention studies. Because no adverse effects have been reported from this training modality,9 safety concerns should be minimal in conducting large-scale trials involving RE training among stroke patients.The same future trials should focus on their feasibility and their immediate and residual health-related effects.Combined Exercise and StrokeThe beneficial relationship between RE and health and chronic disease was recognized only recently.45 The American College of Sports Medicine first introduced RE into its guidelines in 1990 as a beneficial component of comprehensive fitness programs for healthy adults of all ages. However, RE should serve as a complement to AE, rather than as a replacement, for therapeutic exercise.A combined exercise program seems to be well-tolerated by stroke patients. In a randomized controlled trial involving multiple healthcare sites, 92 stroke survivors (mean age 69 years; 1 year poststroke). A more recent study by Marzolini et al47 consisted of a 6-month CARET program (60 minutes sessions, 3 times/week, for 19 weeks) in 41 patients with motor impairments (mean age 63 years; ≥10 weeks poststroke) showed significant gains on the Montreal Cognitive Assessment and in cognitive subdomains of attention/concentration and visuospatial/executive function. The number of individuals meeting criteria for mild cognitive impairment also decreased. Thus, it is conceivable that CARET in stroke patients could affect multiple domains of disabilities compared with more isolated gains achieved from AE or RE alone.Future stroke studies involving CARET should focus on examining their additive and synergistic effects on multiple health outcomes compared with AE or RE alone.Cognitive Training After StrokeThe cognitive effects of stroke are as varied as their topography might suggest with any cognitive domain potentially affected.48 However, dysphasia, slowed information processing, and executive dysfunction are arguably the most common.31 In a 10-year prospective study involving close to 100 young patients with ischemic stroke (median age 43 years), mental slowness was present even ≤10 years after stroke.49 A recent large trial also demonstrated that even small infarcts are commonly associated with cognitive impairment.50 Any form of cognitive decline after stroke places a burden on stroke patients and their caregivers, and strategies for cognitive rehabilitation, or training, with a goal to improve function and ameliorate disability are critical. A recent systematic review51 of a limited number of studies did not report extended benefits of cognitive training to function and basic and instrumental ADLs. However, positive transfer effects of cognitive training in performing ADLs were observed in 29 stroke patients with apraxia (duration 8 weeks; 2 years poststroke).52 Another review53 identified only 2 small randomized trials (n= 4 months poststroke) underwent combined cognitive and exercise training over 12 weeks. The primary objective of the study was to evaluate the effect of cognitive training alone and combined training on psychological and physical variables associated with stroke, such as fatigue, depression, and sleep. The greatest improvements were seen in poststroke fatigue when cognitive training was combined with exercise.The amount of literature on the isolated effects of cognitive therapies on specific impairments in stroke patients is limited, involves small sample sizes, and has methodological limitations and inconclusive results. Although cognitive training/rehabilitation may result in improvements in specific cognitive domains, the data are insufficient relating such interventions to real world cognitive processes and proficiency in everyday functional ADLs.Further work with sufficiently large samples is required to allow exploration of these issues and to reach reliable conclusions. A greater emphasis should involve the examination of transfer effects to ADLs that improve function and quality of life after stroke. Finally, potential additive or synergistic effects of cognitive training, combined with therapeutic exercise, should be explored.Conclusion and Future DirectionsOverall, studies demonstrate that stroke-related impairments can be improved from properly designed and supervised therapeutic exercise programs. A most recent review confirmed the beneficial role of exercise on multiple effects on life after stroke, such as improved cognition, arm function, and balance and gait.56 However, more research is needed to quantify optimal intensities, frequencies, and durations in different exercise modalities. Additionally, a paucity of research has investigated the effect of exercise alone, or combined with cognitive training, on restorative cognitive rehabilitation after stroke. After effective exercise and cognitive modalities are clearly identified, perceived barriers to adherence and the sustainability of interventions need to be better understood before widespread implementation can be attempted.It is important to note that even if therapeutic exercise fails to restore physical and cognitive impairments to prestroke levels, increased PA and exercise can enhance overall well-being and reduce multiple risk factors (Figure) responsible for recurrent strokes and coronary events among stroke patients.Download figureDownload PowerPointFigure. General recommendations and complementary health benefits of combined exercise training. ↑ indicates values increase; ↓ indicates values decrease; Bold indicates strong evidence, considering causality and dose response, in adults and older adults (US Department of Health and Human Services, 2008 Physical Activity Guidelines for Americans).Sources of FundingWe are funded by the American Stroke Association/Bugher Foundation Centers of Excellence in Stroke Collaborative Research for a randomized clinical trial on the effects of exercise and cognitive training poststroke.DisclosuresNone.FootnotesCorrespondence to Clinton Wright, MD, MS, 1120 NW 14th St, CRB 1349, Miami, FL 33136. E-mail [email protected]References1. Bale M, Strand LI.Does functional strength training of the leg in subacute stroke improve physical performance? A pilot randomized controlled trial.Clin Rehabil. 2008; 22:911–921. doi: 10.1177/0269215508090092.CrossrefMedlineGoogle Scholar2. Quaney BM, Boyd LA, McDowd JM, Zahner LH, He J, Mayo MS, et al. Aerobic exercise improves cognition and motor function poststroke.Neurorehabil Neural Repair. 2009; 23:879–885. doi: 10.1177/1545968309338193.CrossrefMedlineGoogle Scholar3. Flansbjer UB, Downham D, Lexell J.Knee muscle strength, gait performance, and perceived participation after stroke.Arch Phys Med Rehabil. 2006; 87:974–980. doi: 10.1016/j.apmr.2006.03.008.CrossrefMedlineGoogle Scholar4. Meijer R, Plotnik M, Zwaaftink EG, van Lummel RC, Ainsworth E, Martina JD, et al. Markedly impaired bilateral coordination of gait in post-stroke patients: Is this deficit distinct from asymmetry? A cohort study.J Neuroeng Rehabil. 2011; 8:23. doi: 10.1186/1743-0003-8-23.CrossrefMedlineGoogle Scholar5. Jørgensen HS, Nakayama H, Raaschou HO, Olsen TS.Recovery of walking function in stroke patients: the Copenhagen Stroke Study.Arch Phys Med Rehabil. 1995; 76:27–32.CrossrefMedlineGoogle Scholar6. Tang A, Sibley KM, Thomas SG, McIlroy WE, Brooks D.Maximal exercise test results in subacute stroke.Arch Phys Med Rehabil. 2006; 87:1100–1105. doi: 10.1016/j.apmr.2006.04.016.CrossrefMedlineGoogle Scholar7. Eng JJ, Dawson AS, Chu KS.Submaximal exercise in persons with stroke: test-retest reliability and concurrent validity with maximal oxygen consumption.Arch Phys Med Rehabil. 2004; 85:113–118.CrossrefMedlineGoogle Scholar8. Ramas J, Courbon A, Roche F, Bethoux F, Calmels P.Effect of training programs and exercise in adult stroke patients: literature review.Ann Readapt Med Phys. 2007; 50:438–444, 430. doi: 10.1016/j.annrmp.2007.04.006.CrossrefMedlineGoogle Scholar9. Brogårdh C, Lexell J.Effects of cardiorespiratory fitness and muscle-resistance training after stroke.PM R. 2012; 4:901–907; quiz 907. doi: 10.1016/j.pmrj.2012.09.1157.CrossrefMedlineGoogle Scholar10. Cress ME, Meyer M.Maximal voluntary and functional performance levels needed for independence in adults aged 65 to 97 years.Phys Ther. 2003; 83:37–48.MedlineGoogle Scholar11. Field M, Gebruers N, Sundaram T, Nicholson S, Mead G.Physical activity after stroke: A systematic review and meta-analysis.ISRN Stroke. 2013; 2013:1–13.CrossrefGoogle Scholar12. Tudor-Locke C, Washington TL, Hart TL.Expected values for steps/day in special populations.Prev Med. 2009; 49:3–11. doi: 10.1016/j.ypmed.2009.04.012.CrossrefMedlineGoogle Scholar13. Bassett DR, Wyatt HR, Thompson H, Peters JC, Hill JO.Pedometer-measured physical activity and health behaviors in US adults.Med Sci Sports Exerc. 2010; 42:1819–1825. doi: 10.1249/MSS.0b013e3181dc2e54.CrossrefMedlineGoogle Scholar14. Jin YP, Di Legge S, Ostbye T, Feightner JW, Hachinski V.The reciprocal risks of stroke and cognitive impairment in an elderly population.Alzheimers Dement. 2006; 2:171–178. doi: 10.1016/j.jalz.2006.03.006.CrossrefMedlineGoogle Scholar15. Patel M, Coshall C, Rudd AG, Wolfe CD.Natural history of cognitive impairment after stroke and factors associated with its recovery.Clin Rehabil. 2003; 17:158–166.CrossrefMedlineGoogle Scholar16. Zinn S, Dudley TK, Bosworth HB, Hoenig HM, Duncan PW, Horner RD.The effect of poststroke cognitive impairment on rehabilitation process and functional outcome.Arch Phys Med Rehabil. 2004; 85:1084–1090.CrossrefMedlineGoogle Scholar17. Hobson P, Meara J.Cognitive function and mortality in a community-based elderly cohort of first-ever stroke survivors and control subjects.J Stroke Cerebrovasc Dis. 2010; 19:382–387. doi: 10.1016/j.jstrokecerebrovasdis.2009.07.006.CrossrefMedlineGoogle Scholar18. Yip AG, Brayne C, Matthews FE; MRC Cognitive Function and Ageing Study. Risk factors for incident dementia in England and Wales: The Medical Research Council Cognitive Function and Ageing Study. A population-based nested case-control study.Age Ageing. 2006; 35:154–160. doi: 10.1093/ageing/afj030.CrossrefMedlineGoogle Scholar19. Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee IM, et al; American College of Sports Medicine. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise.Med Sci Sports Exerc. 2011; 43:1334–1359. doi: 10.1249/MSS.0b013e318213fefb.CrossrefMedlineGoogle Scholar20. Lee CD, Folsom AR, Blair SN.Physical activity and stroke risk: a meta-analysis.Stroke. 2003; 34:2475–2481. doi: 10.1161/01.STR.0000091843.02517.9D.LinkGoogle Scholar21. Brazzelli M, Saunders DH, Greig CA, Mead GE.Physical fitness training for stroke patients.Cochrane Database Syst Rev. 2011;CD003316.MedlineGoogle Scholar22. Marques EA, Wanderley F, Machado L, Sousa F, Viana JL, Moreira-Gonçalves D, et al. Effects of resistance and aerobic exercise on physical function, bone mineral density, OPG and RANKL in older women.Exp Gerontol. 2011; 46:524–532. doi: 10.1016/j.exger.2011.02.005.CrossrefMedlineGoogle Scholar23. Ismail I, Keating SE, Baker MK, Johnson NA.A systematic review and meta-analysis of the effect of aerobic vs. resistance exercise training on visceral fat.Obes Rev. 2012; 13:68–91. doi: 10.1111/j.1467-789X.2011.00931.x.CrossrefMedlineGoogle Scholar24. Church TS, Blair SN, Cocreham S, Johannsen N, Johnson W, Kramer K, et al. Effects of aerobic and resistance training on hemoglobin A1c levels in patients with type 2 diabetes: a randomized controlled trial.JAMA. 2010; 304:2253–2262. doi: 10.1001/jama.2010.1710.CrossrefMedlineGoogle Scholar25. Sharma A, Madaan V, Petty FD.Exercise for mental health.Prim Care Companion J Clin Psychiatry. 2006; 8:106.CrossrefMedlineGoogle Scholar26. Bherer L, Erickson KI, Liu-Ambrose T.A review of the effects of physical activity and exercise on cognitive and brain functions in older adults.J Aging Res. 2013; 2013:657508. doi: 10.1155/2013/657508.MedlineGoogle Scholar27. Cotman CW, Berchtold NC, Christie LA.Exercise builds brain health: key roles of growth factor cascades and inflammation.Trends Neurosci. 2007; 30:464–472. doi: 10.1016/j.tins.2007.06.011.CrossrefMedlineGoogle Scholar28. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. Exercise training increases size of hippocampus and improves memory.Proc Natl Acad Sci U S A. 2011; 108:3017–3022. doi: 10.1073/pnas.1015950108.CrossrefMedlineGoogle Scholar29. Erickson KI, Prakash RS, Voss MW, Chaddock L, Hu L, Morris KS, et al. Aerobic fitness is associated with hippocampal volume in elderly humans.Hippocampus. 2009; 19:1030–1039. doi: 10.1002/hipo.20547.CrossrefMedlineGoogle Scholar30. Colcombe S, Kramer AF.Fitness effects on the cognitive function of older adults: a meta-analytic study.Psychol Sci. 2003; 14:125–1
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