Aging after stroke: how to define post-stroke sarcopenia and what are its risk factors?

Sheng Li, Javier Gonzalez-Buonomo, Jaskiran Ghuman, Xinran Huang, Aila Malik, Nuray Yozbatiran, Elaine Magat, Gerard E Francisco, Hulin Wu, Walter R Frontera, Sheng Li, Javier Gonzalez-Buonomo, Jaskiran Ghuman, Xinran Huang, Aila Malik, Nuray Yozbatiran, Elaine Magat, Gerard E Francisco, Hulin Wu, Walter R Frontera

Abstract

Background: Sarcopenia, generally described as "aging-related loss of skeletal muscle mass and function", can occur secondary to a systemic disease.

Aim: This project aimed to study the prevalence of sarcopenia in chronic ambulatory stroke survivors and its associated risk factors using the two most recent diagnostic criteria.

Design: A cross-sectional observational study.

Setting: A scientific laboratory.

Population: Chronic stroke.

Methods: Twenty-eight ambulatory chronic stroke survivors (12 females; mean age=57.8±11.8 years; time after stroke=76±45 months), hand-grip strength, gait speed, and appendicular skeletal muscle mass (ASM) were measured to define sarcopenia. Risk factors, including motor impairment and spasticity, were identified using regression analysis.

Results: The prevalence of sarcopenia varied between 18% and 25% depending on the diagnostic criteria used. A significant difference was seen in the prevalence of low hand grip strength on the affected side (96%) when compared to the contralateral side (25%). The prevalence of slow gait speed was 86% while low ASM was present in 89% of the subjects. Low ASM was marginally negatively correlated with time since stroke and gait speed, but no correlation was observed with age, motor impairment, or spasticity. ASM loss, bone loss and fat deposition were significantly greater in the affected upper limb than in the affected lower limb. Regression analyses showed that time since stroke was a factor associated with bone and muscle loss in the affected upper limb, spasticity had a protective role for muscle loss in the affected lower limb, and walking had a protective role for bone loss in the lower limb.

Conclusions: The prevalence of sarcopenia in stroke survivors is high and is a multifactorial process that is not age-related. Different risk factors contribute to muscle loss in the upper and lower limbs after stroke.

Clinical rehabilitation impact: Clinicians need to be aware of high prevalence of sarcopenia in chronic stroke survivors. Sarcopenia is more evident in the upper than lower limbs. Clinicians also need to understand potential protective roles of some factors, such as spasticity and walking for the muscles in the lower limb.

Conflict of interest statement

Conflicts of interest.—The authors certify that there is no conflict of interest with any financial organization regarding the material discussed in the manuscript.

Figures

Figure 1
Figure 1
—Muscle mass (A), bone mineral density (BMD) (B) and percent fat (C) of the affected and unaffected upper (UL) and lower (LL) limbs. Mean and standard errors are shown. *statistical significance.
Figure 2
Figure 2
—Bone loss and muscle loss in the UL and LL and leg. Mean and standard errors are shown. *statistical significance.

References

    1. Rosenberg IH. Summary comments. Am J Clin Nutr 1989;50:1231–3. 10.1093/ajcn/50.5.1231
    1. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. ; Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), and the Extended Group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019;48:16–31. 10.1093/ageing/afy169
    1. Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima K, et al. Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment. J Am Med Dir Assoc 2020;21:300–307.e2. 10.1016/j.jamda.2019.12.012
    1. Reijnierse EM, Trappenburg MC, Leter MJ, Blauw GJ, Sipilä S, Sillanpää E, et al. The Impact of Different Diagnostic Criteria on the Prevalence of Sarcopenia in Healthy Elderly Participants and Geriatric Outpatients. Gerontology 2015;61:491–6. 10.1159/000377699
    1. Mas MF, González J, Frontera WR. Stroke and sarcopenia. Curr Phys Med Rehabil Rep 2020;8:452–60. 10.1007/s40141-020-00284-2
    1. Scherbakov N, Sandek A, Doehner W. Stroke-related sarcopenia: specific characteristics. J Am Med Dir Assoc 2015;16:272–6. 10.1016/j.jamda.2014.12.007
    1. Scherbakov N, von Haehling S, Anker SD, Dirnagl U, Doehner W. Stroke induced Sarcopenia: muscle wasting and disability after stroke. Int J Cardiol 2013;170:89–94. 10.1016/j.ijcard.2013.10.031
    1. Bernhardt J, Dewey H, Thrift A, Donnan G. Inactive and alone: physical activity within the first 14 days of acute stroke unit care. Stroke 2004;35:1005–9. 10.1161/01.STR.0000120727.40792.40
    1. Kortebein P, Ferrando A, Lombeida J, Wolfe R, Evans WJ. Effect of 10 days of bed rest on skeletal muscle in healthy older adults. JAMA 2007;297:1772–4. 10.1001/jama.297.16.1772-b
    1. Arasaki K, Igarashi O, Ichikawa Y, Machida T, Shirozu I, Hyodo A, et al. Reduction in the motor unit number estimate (MUNE) after cerebral infarction. J Neurol Sci 2006;250:27–32. 10.1016/j.jns.2006.06.024
    1. Carda S, Cisari C, Invernizzi M. Sarcopenia or muscle modifications in neurologic diseases: a lexical or patophysiological difference? Eur J Phys Rehabil Med 2013;49:119–30.
    1. De Deyne PG, Hafer-Macko CE, Ivey FM, Ryan AS, Macko RF. Muscle molecular phenotype after stroke is associated with gait speed. Muscle Nerve 2004;30:209–15. 10.1002/mus.20085
    1. Ryan AS, Buscemi A, Forrester L, Hafer-Macko CE, Ivey FM. Atrophy and intramuscular fat in specific muscles of the thigh: associated weakness and hyperinsulinemia in stroke survivors. Neurorehabil Neural Repair 2011;25:865–72. 10.1177/1545968311408920
    1. Chang KV, Wu WT, Huang KC, Han DS. Segmental body composition transitions in stroke patients: trunks are different from extremities and strokes are as important as hemiparesis. Clin Nutr 2020;39:1968–73. 10.1016/j.clnu.2019.08.024
    1. Ciciliot S, Rossi AC, Dyar KA, Blaauw B, Schiaffino S. Muscle type and fiber type specificity in muscle wasting. Int J Biochem Cell Biol 2013;45:2191–9. 10.1016/j.biocel.2013.05.016
    1. Ryan AS, Ivey FM, Serra MC, Hartstein J, Hafer-Macko CE. Sarcopenia and Physical Function in Middle-Aged and Older Stroke Survivors. Arch Phys Med Rehabil 2017;98:495–9. 10.1016/j.apmr.2016.07.015
    1. Shiraishi A, Yoshimura Y, Wakabayashi H, Tsuji Y. Prevalence of stroke-related sarcopenia and its association with poor oral status in post-acute stroke patients: implications for oral sarcopenia. Clin Nutr 2018;37:204–7. 10.1016/j.clnu.2016.12.002
    1. Yoshimura Y, Bise T, Nagano F, Shimazu S, Shiraishi A, Yamaga M, et al. Systemic Inflammation in the Recovery Stage of Stroke: Its Association with Sarcopenia and Poor Functional Rehabilitation Outcomes. Prog Rehabil Med 2018;3:20180011. 10.2490/prm.20180011
    1. Matsushita T, Nishioka S, Taguchi S, Yamanouchi A. Sarcopenia as a predictor of activities of daily living capability in stroke patients undergoing rehabilitation. Geriatr Gerontol Int 2019;19:1124–8. 10.1111/ggi.13780
    1. Jang Y, Im S, Han Y, Koo H, Sohn D, Park GY. Can initial sarcopenia affect poststroke rehabilitation outcome? J Clin Neurosci 2020;71:113–8. 10.1016/j.jocn.2019.08.109
    1. Park JG, Lee KW, Kim SB, Lee JH, Kim YH. Effect of Decreased Skeletal Muscle Index and Hand Grip Strength on Functional Recovery in Subacute Ambulatory Stroke Patients. Ann Rehabil Med 2019;43:535–43. 10.5535/arm.2019.43.5.535
    1. Aydin T, Kesiktaş FN, Oren MM, Erdogan T, Ahisha YC, Kizilkurt T, et al. Sarcopenia in patients following stroke: an overlooked problem. Int J Rehabil Res 2021;44:269–75. 10.1097/MRR.0000000000000487
    1. Su Y, Yuki M, Otsuki M. Prevalence of stroke-related sarcopenia: A systematic review and meta-analysis. J Stroke Cerebrovasc Dis 2020;29:105092. 10.1016/j.jstrokecerebrovasdis.2020.105092
    1. Andersson SA, Danielsson A, Ohlsson F, Wipenmyr J, Alt Murphy M. Arm impairment and walking speed explain real-life activity of the affected arm and leg after stroke. J Rehabil Med 2021;53:jrm00210. 10.2340/16501977-2838
    1. Li S, Francisco GE, Rymer WZ. A New Definition of Poststroke Spasticity and the Interference of Spasticity With Motor Recovery From Acute to Chronic Stages. Neurorehabil Neural Repair 2021;35:601–10. 10.1177/15459683211011214
    1. Lindsay C, Ispoglou S, Helliwell B, Hicklin D, Sturman S, Pandyan A. Can the early use of botulinum toxin in post stroke spasticity reduce contracture development? A randomised controlled trial. Clin Rehabil 2021;35:399–409. 10.1177/0269215520963855
    1. Sunnerhagen KS, Opheim A, Alt Murphy M. Onset, time course and prediction of spasticity after stroke or traumatic brain injury. Ann Phys Rehabil Med 2019;62:431–4. 10.1016/j.rehab.2018.04.004
    1. Sommerfeld DK, Eek EU, Svensson AK, Holmqvist LW, von Arbin MH. Spasticity after stroke: its occurrence and association with motor impairments and activity limitations. Stroke 2004;35:134–9.
    1. Dorňák T, Justanová M, Konvalinková R, Říha M, Mužík J, Hoskovcová M, et al. Prevalence and evolution of spasticity in patients suffering from first-ever stroke with carotid origin: a prospective, longitudinal study. Eur J Neurol 2019;26:880–6. 10.1111/ene.13902
    1. Pundik S, McCabe J, Skelly M, Tatsuoka C, Daly JJ. Association of spasticity and motor dysfunction in chronic stroke. Ann Phys Rehabil Med 2019;62:397–402. 10.1016/j.rehab.2018.07.006
    1. Francisco GE, Li S. Spasticity. In: Cidu DX, editor. Braddom Physical Medicine and Rehabilitation. Sixth Edition. New York, NY, Elsevier; 2020.
    1. Li S, Chen YT, Francisco GE, Zhou P, Rymer WZ. A Unifying Pathophysiological Account for Post-stroke Spasticity and Disordered Motor Control. Front Neurol 2019;10:468. 10.3389/fneur.2019.00468
    1. Adams V. Electromyostimulation to fight atrophy and to build muscle: facts and numbers. J Cachexia Sarcopenia Muscle 2018;9:631–4. 10.1002/jcsm.12332
    1. Ansari NN, Naghdi S, Arab TK, Jalaie S. The interrater and intrarater reliability of the Modified Ashworth Scale in the assessment of muscle spasticity: limb and muscle group effect. NeuroRehabilitation 2008;23:231–7. 10.3233/NRE-2008-23304
    1. Fugl-Meyer AR, Jääskö L, Leyman I, Olsson S, Steglind S. The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. Scand J Rehabil Med 1975;7:13–31.
    1. See J, Dodakian L, Chou C, Chan V, McKenzie A, Reinkensmeyer DJ, et al. A standardized approach to the Fugl-Meyer assessment and its implications for clinical trials. Neurorehabil Neural Repair 2013;27:732–41. 10.1177/1545968313491000
    1. Veerbeek JM, Winters C, van Wegen EE, Kwakkel G. Is the proportional recovery rule applicable to the lower limb after a first-ever ischemic stroke? PLoS One 2018;13:e0189279. 10.1371/journal.pone.0189279
    1. Prabhakaran S, Zarahn E, Riley C, Speizer A, Chong JY, Lazar RM, et al. Inter-individual variability in the capacity for motor recovery after ischemic stroke. Neurorehabil Neural Repair 2008;22:64–71. 10.1177/1545968307305302
    1. Mahendran N, Kuys SS, Brauer SG. Recovery of ambulation activity across the first six months post-stroke. Gait Posture 2016;49:271–6. 10.1016/j.gaitpost.2016.06.038
    1. Li S, Francisco GE, Zhou P. Post-stroke Hemiplegic Gait: New Perspective and Insights. Front Physiol 2018;9:1021. 10.3389/fphys.2018.01021
    1. Wheeler A, Smith HS. Botulinum toxins: mechanisms of action, antinociception and clinical applications. Toxicology 2013;306:124–46. 10.1016/j.tox.2013.02.006
    1. Jankovic J. Botulinum toxin: state of the art. Mov Disord 2017;32:1131–8. 10.1002/mds.27072
    1. Pirazzini M, Rossetto O, Eleopra R, Montecucco C. Botulinum neurotoxins: Biology, pharmacology, and toxicology. Pharmacol Rev 2017;69:200–35. 10.1124/pr.116.012658
    1. Andringa A, van de Port I, van Wegen E, Ket J, Meskers C, Kwakkel G. Effectiveness of botulinum toxin treatment for upper limb spasticity after stroke over different ICF domains: a systematic review and meta-analysis. Arch Phys Med Rehabil 2019;100:1703–25. 10.1016/j.apmr.2019.01.016
    1. Multani I, Manji J, Tang MJ, Herzog W, Howard JJ, Graham HK. Sarcopenia, Cerebral Palsy, and Botulinum Toxin Type A. JBJS Rev 2019;7:e4. 10.2106/JBJS.RVW.18.00153
    1. Li S. Ankle and Foot Spasticity Patterns in Chronic Stroke Survivors with Abnormal Gait. Toxins (Basel) 2020;12:12. 10.3390/toxins12100646

Source: PubMed

赞助者和合作者

医疗条件

药物干预

3
订阅