Sarcopenia and Heart Failure

Francesco Curcio, Gianluca Testa, Ilaria Liguori, Martina Papillo, Veronica Flocco, Veronica Panicara, Gianluigi Galizia, David Della-Morte, Gaetano Gargiulo, Francesco Cacciatore, Domenico Bonaduce, Francesco Landi, Pasquale Abete, Francesco Curcio, Gianluca Testa, Ilaria Liguori, Martina Papillo, Veronica Flocco, Veronica Panicara, Gianluigi Galizia, David Della-Morte, Gaetano Gargiulo, Francesco Cacciatore, Domenico Bonaduce, Francesco Landi, Pasquale Abete

Abstract

Modifications of lean mass are a frequent critical determinant in the pathophysiology and progression of heart failure (HF). Sarcopenia may be considered one of the most important causes of low physical performance and reduced cardiorespiratory fitness in older patients with HF. Sarcopenia is frequently misdiagnosed as cachexia. However, muscle wasting in HF has different pathogenetic features in sarcopenic and cachectic conditions. HF may induce sarcopenia through common pathogenetic pathways such as hormonal changes, malnutrition, and physical inactivity; mechanisms that influence each other. In the opposite way, sarcopenia may favor HF development by different mechanisms, including pathological ergoreflex. Paradoxically, sarcopenia is not associated with a sarcopenic cardiac muscle, but the cardiac muscle shows a hypertrophy which seems to be "not-functional." First-line agents for the treatment of HF, physical activity and nutritional interventions, may offer a therapeutic advantage in sarcopenic patients irrespective of HF. Thus, sarcopenia is highly prevalent in patients with HF, contributing to its poor prognosis, and both conditions could benefit from common treatment strategies based on pharmacological, physical activity, and nutritional approaches.

Keywords: cachexia; elderly; heart failure; malnutrition; physical activity; sarcopenia.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Figure 1
Figure 1
Skeletal muscle histological alterations in sarcopenia and cachexia adapted from von Haehling et al. [4].
Figure 2
Figure 2
Factors related to heart failure, potentially leading to sarcopenia.
Figure 3
Figure 3
A typical example of sarcopenia and echocardiographic evaluation in an 82-year-old male patient. A reduction of strength and mass muscle is associated to “non-functional” cardiac hypertrophy (LV = left ventricular; E/e1 = echocardiographic transmitral early peak velocity (E) by pulsed wave Doppler over e1 (E/e1) represent a noninvasive surrogate for LV diastolic pressures for grading a diastolic dysfunction).
Figure 4
Figure 4
Increase of left ventricular mass [LVM, g] and reduction of left ventricular ejection fraction (LVEF, %) associated with a reduction of handgrip strength [modified by Beyer et al. [72]).

References

    1. Ponikowski P., Voors Adriaan A., Anker S.D., Bueno H., Cleland J.G.F., Coats A.J.S., Falk V., Gonzlez-Juanatey J.R., Harjola V.-P., Jankowska E.A., et al. ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure: The Task Force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC). Developed with the special contribution of the Heart Failure Association (HFA) of the ESC. Eur. J. Heart Fail. 2016;18:891–975.
    1. Go A.S., Mozaffarian D., Roger V.L., Benjamin E.J., Berry J.D., Blaha M.J., Dai S., Ford E.S., Fox C.S., Franco S., et al. Heart disease and stroke statistics—2014 update: A report from the American Heart Association. Circulation. 2014;129:e28–e292. doi: 10.1161/01.cir.0000441139.02102.80.
    1. Carbone S., Lavie C.J., Arena R. Obesity and heart failure: Focus on the obesity paradox. Mayo. Clin. Proc. 2017;92:266–279. doi: 10.1016/j.mayocp.2016.11.001.
    1. Muscaritoli M., Anker S.D., Argilés J., Aversa Z., Bauer J.M., Biolo G., Boirie Y., Bosaeus I., Cederholm T., Costelli P., et al. Consensus definition of sarcopenia, cachexia and pre-cachexia: Joint document elaborated by Special Interest Groups (SIG) “cachexia-anorexia in chronic wasting diseases” and “nutrition in geriatrics”. Clin. Nutr. 2010;29:154–159. doi: 10.1016/j.clnu.2009.12.004.
    1. Cruz-Jentoft A.J., Bahat G., Bauer J., Boirie Y., Bruyère O., Cederholm T., Cooper C., Landi F., Rolland Y., Sayer A.A., et al. Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31. doi: 10.1093/ageing/afy169.
    1. Von Haehling S. The wasting continuum in heart failure: From sarcopenia to cachexia. Proc. Nutr. Soc. 2015;74:367–377. doi: 10.1017/S0029665115002438.
    1. Emami A., Saitoh M., Valentova M., Sandek A., Evertz R., Ebner N., Loncar G., Springer J., Doehner W., Lainscak M., et al. Comparison of sarcopenia and cachexia in men with chronic heart failure: Results from the Studies Investigating Co-Morbidities Aggravating Heart Failure (SICA-HF) Eur. J. Heart Fail. 2018;20:1580–1587. doi: 10.1002/ejhf.1304.
    1. Lin J., Lopez E.F., Jin Y., Van Remmen H., Bauch T., Han H.C., Lindsey M.L. Age-related cardiac muscle sarcopenia: Combining experimental and mathematical modelling to identify mechanism. Exp. Gerontol. 2008;43:296–306. doi: 10.1016/j.exger.2007.12.005.
    1. Narici M.V., Maffulli N. Sarcopenia: Characteristics, mechanisms and functional significance. Br. Med. Bull. 2010;95:139–159. doi: 10.1093/bmb/ldq008.
    1. Zamboni M., Rossi A.P., Corzato F., Bambace C., Mazzali G., Fantin F. Sarcopenia, cachexia and congestive heart failure in the elderly. Endocr. Metab. Immune Disord. Drug. Targets. 2013;13:58–67. doi: 10.2174/1871530311313010008.
    1. Drexler H., Riede U., Münzel T., König H., Funke E., Just H. Alterations of skeletal muscle in chronic heart failure. Circulation. 1992;85:1751–1759. doi: 10.1161/01.CIR.85.5.1751.
    1. Basile C., Della-Morte D., Cacciatore F., Gargiulo G., Galizia G., Roselli M., Curcio F., Bonaduce D., Abete P. Phase angle as bioelectrical marker to identify elderly patients at risk of sarcopenia. Exp. Gerontol. 2014;58:43–46. doi: 10.1016/j.exger.2014.07.009.
    1. Von Haehling S., Ebner N., Dos Santos M.R., Springer J., Anker S.D. Muscle wasting and cachexia in heart failure: Mechanisms and therapies. Nat. Rev. Cardiol. 2017;14:323–341. doi: 10.1038/nrcardio.2017.51.
    1. Bristow M.R. The adrenergic nervous system in heart failure. N. Engl. J. Med. 1984;311:850–851. doi: 10.1056/NEJM198409273111310.
    1. Brink M., Price S.R., Chrast J., Bailey J.L., Anwar A., Mitch W.E., Delafontaine P. Angiotensin II induces skeletal muscle wasting through enhanced protein degradation and down-regulates autocrine insulin-like growth factor I. Endocrinology. 2001;142:1489–1496. doi: 10.1210/endo.142.4.8082.
    1. Delafontaine P., Yoshida T. The renin-angiotensin system and the biology of skeletal muscle: Mechanisms of muscle wasting in chronic disease states. Trans. Am. Clin. Climatol. Assoc. 2016;127:245–258.
    1. Marzetti E., Calvani R., DuPree J., Lees H.A., Giovannini S., Seo D.O., Buford T.W., Sweet K., Morgan D., Strehler K.Y., et al. Late-life enalapril administration induces nitric oxide-dependent and independent metabolic adaptations in the rat skeletal muscle. Age. 2013;35:1061–1075. doi: 10.1007/s11357-012-9428-4.
    1. Brown D.A., Perry J.B., Allen M.E., Sabbah H.N., Stauffer B.L., Shaikh S.R., Cleland J.G., Colucci W.S., Butler J., Voors A.A., et al. Expert consensus document: Mitochondrial function as a therapeutic target in heart failure. Nat. Rev. Cardiol. 2017;14:238–250. doi: 10.1038/nrcardio.2016.203.
    1. Lee J.F., Barrett-O’Keefe Z., Nelson A.D., Garten R.S., Ryan J.J., Nativi-Nicolau J.N., Richardson R.S., Wray D.W. Impaired skeletal muscle vasodilation during exercise in heart failure with preserved ejection fraction. Int. J. Cardiol. 2016;211:14–21. doi: 10.1016/j.ijcard.2016.02.139.
    1. Bossone E., Arcopinto M., Iacoviello M., Triggiani V., Cacciatore F., Maiello C., Limongelli G., Masarone D., Perticone F., Sciacqua A., et al. TOSCA Investigators. Multiple hormonal and metabolic deficiency syndrome in chronic heart failure: Rationale, design, and demographic characteristics of the TOSCA. Registry. Intern. Emerg. Med. 2018;13:661–671. doi: 10.1007/s11739-018-1844-8.
    1. Onder G., Liperoti R., Russo A., Soldato M., Capoluongo E., Volpato S., Cesari M., Ameglio F., Bernabei R., Landi F. Body mass index, free insulin-like growth factor I, and physical function among older adults: Results from the ilSIRENTE study. Am. J. Physiol. Endocrinol. Metab. 2006;291:E829–E834. doi: 10.1152/ajpendo.00138.2006.
    1. Josiak K., Jankowska E.A., Piepoli M.F., Banasiak W., Ponikowski P. Skeletal myopathy in patients with chronic heart failure: Significance of anabolic-androgenic hormones. J. Cachexia Sarcopenia Muscle. 2014;5:287–296. doi: 10.1007/s13539-014-0152-z.
    1. Kontoleon P.E., Anastasiou-Nana M.I., Papapetrou P.D., Alexopoulos G., Ktenas V., Rapti A.C., Tsagalou E.P., Nanas J.N. Hormonal profile in patients with congestive heart failure. Int. J. Cardiol. 2003;87:179–183. doi: 10.1016/S0167-5273(02)00212-7.
    1. Storer T.W., Magliano L., Woodhouse L., Lee M.L., Dzekov C., Dzekov J., Casaburi R., Bhasin S. Testosterone dose-dependently increases maximal voluntary strength and leg power, but does not affect fatigability or specific tension. J. Clin. Endocrinol. Metab. 2003;88:1478–1485. doi: 10.1210/jc.2002-021231.
    1. Müller T.D., Nogueiras R., Andermann M.L., Andrews Z.B., Anker S.D., Argente J., Batterham R.L., Benoit S.C., Bowers C.Y., Broglio F., et al. Ghrelin. Mol. Metab. 2015;4:437–460. doi: 10.1016/j.molmet.2015.03.005.
    1. Lee S.J., McPherron A.C. Regulation of myostatin activity and muscle growth. Proc. Natl. Acad. Sci. USA. 2001;98:9306–9311. doi: 10.1073/pnas.151270098.
    1. LeBrasseur N.K., Schelhorn T.M., Bernardo B.L., Cosgrove P.G., Loria P.M., Brown T.A. Myostatin inhibition enhances the effects of exercise on performance and metabolic outcomes in aged mice. J. Gerontol. A Biol. Sci. Med. Sci. 2009;64:940–948. doi: 10.1093/gerona/glp068.
    1. Gruson D., Ahn S.A., Ketelslegers J.M., Rousseau M.F. Increased plasma myostatin in heart failure. Eur. J. Heart Fail. 2011;13:734–736. doi: 10.1093/eurjhf/hfr024.
    1. Breitbart A., Auger-Messier M., Molkentin J.D., Heineke J. Myostatin from the heart: Local and systemic actions in cardiac failure and muscle wasting. Am. J. Physiol. Heart Circ. Physiol. 2011;300:H1973–H1982. doi: 10.1152/ajpheart.00200.2011.
    1. Heineke J., Auger-Messier M., Xu J., Sargent M., York A., Welle S., Molkentin J.D. Genetic deletion of myostatin from the heart prevents skeletal muscle atrophy in heart failure. Circulation. 2010;121:419–425. doi: 10.1161/CIRCULATIONAHA.109.882068.
    1. Liguori I., Curcio F., Russo G., Cellurale M., Aran L., Bulli G., Della-Morte D., Gargiulo G., Testa G., Cacciatore F., et al. Risk of Malnutrition Evaluated by Mini Nutritional Assessment and Sarcopenia in Noninstitutionalized Elderly People. Nutr. Clin. Pract. 2018;33:879–886. doi: 10.1002/ncp.10022.
    1. İlhan B., Bahat G., Erdoğan T., Kılıç C., Karan M.A. Anorexia Is Independently Associated with Decreased Muscle Mass and Strength in Community Dwelling Older Adults. J. Nutr. Health Aging. 2019;23:202–206. doi: 10.1007/s12603-018-1119-0.
    1. Hussain Z., Swindle J., Hauptman P.J. Digoxin use and digoxin toxicity in the post-DIG trial era. J. Card. Fail. 2006;12:343–346. doi: 10.1016/j.cardfail.2006.02.005.
    1. Cacciatore F., Della-Morte D., Basile C., Curcio F., Liguori I., Roselli M., Gargiulo G., Galizia G., Bonaduce D., Abete P. Butyryl-cholinesterase is related to muscle mass and strength. A new biomarker to identify elderly subjects at risk of sarcopenia. Biomark. Med. 2015;9:669–678. doi: 10.2217/bmm.15.28.
    1. Schaap L.A., Pluijm S.M., Deeg D.J., Harris T.B., Kritchevsky S.B., Newman A.B., Colbert L.H., Pahor M., Rubin S.M., Tylavsky F.A., et al. Higher inflammatory marker levels in older persons: Associations with 5-year change in muscle mass and muscle strength. J. Gerontol. A Biol. Sci. Med. Sci. 2009;64:1183–1189. doi: 10.1093/gerona/glp097.
    1. Morley J.E., Thomas D.R., Wilson M.M. Cachexia: Pathophysiology and clinical relevance. Am. J. Clin. Nutr. 2006;83:735–743. doi: 10.1093/ajcn/83.4.735.
    1. Curcio F., Ferro G., Basile C., Liguori I., Parrella P., Pirozzi F., Della-Morte D., Gargiulo G., Testa G., Tocchetti C.G., et al. Biomarkers in sarcopenia: A multifactorial approach. Exp. Gerontol. 2016;85:1–8. doi: 10.1016/j.exger.2016.09.007.
    1. Liguori I., Russo G., Curcio F., Bulli G., Aran L., Della-Morte D., Gargiulo G., Testa G., Cacciatore F., Bonaduce D., et al. Oxidative stress, aging, and diseases. Clin. Interv. Aging. 2018;26:757–772. doi: 10.2147/CIA.S158513.
    1. Nishiyama Y., Ikeda H., Haramaki N., Yoshida N., Imaizumi T. Oxidative stress is related to exercise intolerance in patients with heart failure. Am. Heart J. 1998;135:115–120. doi: 10.1016/S0002-8703(98)70351-5.
    1. Das U.N. Free radicals, cytokines and nitric oxide in cardiac failure and myocardial infarction. Mol. Cell. Biochem. 2000;215:145–152. doi: 10.1023/A:1026579422132.
    1. Bouzid M.A., Filaire E., McCall A., Fabre C. Radical Oxygen Species, Exercise and Aging: An Update. Sports Med. 2015;45:1245–1261. doi: 10.1007/s40279-015-0348-1.
    1. Fulle S., Protasi F., Di Tano G., Pietrangelo T., Beltramin A., Boncompagni S., Vecchiet L., Fanò G. The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp. Gerontol. 2004;39:17–24. doi: 10.1016/j.exger.2003.09.012.
    1. Marzetti E., Privitera G., Simili V., Wohlgemuth S.E., Aulisa L., Pahor M., Leeuwenburgh C. Multiple pathways to the same end: Mechanisms of myonuclear apoptosis in sarcopenia of aging. Sci. World J. 2010;10:340–349. doi: 10.1100/tsw.2010.27.
    1. Filippatos G.S., Kanatselos C., Manolatos D.D., Vougas B., Sideris A., Kardara D., Anker S.D., Kardaras F., Uhal B. Studies on apoptosis and fibrosis in skeletal musculature: A comparison of heart failure patients with and without cardiac cachexia. Int. J. Cardiol. 2003;90:107–113. doi: 10.1016/S0167-5273(02)00535-1.
    1. Saitoh M., Ishida J., Doehner W. Sarcopenia, cachexia, and muscle performance in heart failure Review update 2016. Int. J. Cardiol. 2017;238:5–11. doi: 10.1016/j.ijcard.2017.03.155.
    1. Gumucio J.P., Mendias C.L. Atrogin-1, MuRF-1, and sarcopenia. Endocrine. 2013;43:12–21. doi: 10.1007/s12020-012-9751-7.
    1. Sakuma K., Yamaguchi A. Sarcopenia and cachexia: The adaptations of negative regulators of skeletal muscle mass. J. Cachexia Sarcopenia Muscle. 2012;3:77–94. doi: 10.1007/s13539-011-0052-4.
    1. Gielen S., Sandri M., Kozarez I., Kratzsch J., Teupser D., Thiery J., Erbs S., Mangner N., Lenk K., Hambrecht R., et al. Exercise training attenuates MuRF-1expression in the skeletal muscle of patients with chronic heart failure independent of age: The randomized Leipzig Exercise Intervention in Chronic Heart Failure and Aging catabolism study. Circulation. 2012;125:2716–2727. doi: 10.1161/CIRCULATIONAHA.111.047381.
    1. Forbes S.C., Little J.P., Candow D.G. Exercise and nutritional interventions for improving aging muscle health. Endocrine. 2012;42:29–38. doi: 10.1007/s12020-012-9676-1.
    1. Curcio F., Liguori I., Cellulare M., Sasso G., Della-Morte D., Gargiulo G., Testa G., Cacciatore F., Bonaduce D., Abete P. Physical Activity Scale for the Elderly (PASE) Score Is Related to Sarcopenia in Noninstitutionalized Older Adults. J. Geriatr. Phys. Ther. 2019;42:130–135. doi: 10.1519/JPT.0000000000000139.
    1. Coker R.H., Hays N.P., Williams R.H., Xu L., Wolfe R.R., Evans W.J. Bed rest worsens impairments in fat and glucose metabolism in older, overweight adults. J. Gerontol. A Biol. Sci. Med. Sci. 2014;69:363–370. doi: 10.1093/gerona/glt100.
    1. Sjöblom S., Suuronen J., Rikkonen T., Honkanen R., Kröger H., Sirola J. Relationship between postmenopausal osteoporosis and the components of clinical sarcopenia. Maturitas. 2013;75:175–180. doi: 10.1016/j.maturitas.2013.03.016.
    1. Drummond M.J., Timmerman K.L., Markofski M.M., Walker D.K., Dickinson J.M., Jamaluddin M., Brasier A.R., Rasmussen B.B., Volpi E. Short-term bed rest increases TLR4 and IL-6 expression in skeletal muscle of older adults. Am. J. Physiol Regul Integr Comp. Physiol. 2013;305:R216–R223. doi: 10.1152/ajpregu.00072.2013.
    1. Wilson J.R., Fink L., Maris J., Ferraro N., Power-Vanwart J., Eleff S., Chance B. Evaluation of energy metabolism in skeletal muscle of patients with heart failure with gated phosphorus-31 nuclear magnetic resonance. Circulation. 1985;71:57–62. doi: 10.1161/01.CIR.71.1.57.
    1. Schaufelberger M., Eriksson B.O., Grimby G., Held P., Swedberg K. Skeletal muscle fiber composition and capillarization in patients with chronic heart failure: Relation to exercise capacity and central hemodynamics. J. Card. Fail. 1995;1:267–272. doi: 10.1016/1071-9164(95)90001-2.
    1. Dos Santos M.R., Saitoh M., Ebner N., Valentova M., Konishi M., Ishida J., Emami A., Springer J., Sandek A., Doehner W., et al. Sarcopenia and Endothelial Function in Patients With Chronic Heart Failure: Results From the Studies Investigating Comorbidities Aggravating HF (SICA-HF) J. Am. Med. Dir. Assoc. 2017;18:240–245. doi: 10.1016/j.jamda.2016.09.006.
    1. Khan H., Kunutsor S., Rauramaa R., Savonen K., Kalogeropoulos A.P., Georgiopoulou V.V., Butler J., Laukkanen J.A. Cardiorespiratory fitness and risk of heart failure: A population-based follow-up study. Eur. J. Heart Fail. 2014;16:180–188. doi: 10.1111/ejhf.37.
    1. Franciosa J.A., Park M., Levine T.B. Lack of correlation between exercise capacity and indexes of resting left ventricular performance in heart failure. Am. J. Cardiol. 1981;47:33–39. doi: 10.1016/0002-9149(81)90286-1.
    1. Calvani R., Marini F., Cesari M., Tosato M., Anker S.D., Von Haehling S., Miller R.R., Bernabei R., Landi F., Marzetti E., et al. Biomarkers for physical frailty and sarcopenia: State of the science and future developments. J. Cachexia Sarcopenia Muscle. 2015;6:278–286. doi: 10.1002/jcsm.12051.
    1. Liguori I., Russo G., Aran L., Bulli G., Curcio F., Della-Morte D., Gargiulo G., Testa G., Cacciatore F., Bonaduce D., et al. Sarcopenia: Assessment of disease burden and strategies to improve outcomes. Clin. Interv. Aging. 2018;13:913–927. doi: 10.2147/CIA.S149232.
    1. Coats A.J., Clark A.L., Piepoli M., Volterrani M. Poole-Wilson PA Symptoms and quality of life in heart failure: The muscle hypothesis. Br. Heart J. 1994;72:S36–S39. doi: 10.1136/hrt.72.2_Suppl.S36.
    1. Piepoli M., Clark A., Volterrani M., Adamopoulos S., Sleight P., Coats A.J.S. Contribution of muscle afferents to the hemodynamic, autonomic and ventilatory responses to exercise in patients with chronic heart failure. Circulation. 1996;93:940–952. doi: 10.1161/01.CIR.93.5.940.
    1. Nichols S., O’Doherty A.F., Taylor C., Clark A.L., Carroll S., Ingle L. Low skeletal muscle mass is associated with low aerobic capacity and increased mortality risk in patients with coronary heart disease-a CARE CR study. Clin. Physiol. Funct. Imaging. 2019;39:93–102. doi: 10.1111/cpf.12539.
    1. Wilson J.R., Mancini D.M. Factors contributing to the exercise limitation of heart failure. J. Am. Coll. Cardiol. 1993;22:93A–98A. doi: 10.1016/0735-1097(93)90469-H.
    1. Carbone S., Billingsley H.E., Rodriguez-Miguelez P., Kirkman D.L., Garten R., Franco R.L., Lee D.C., Lavie C.J. Lean Mass Abnormalities in Heart Failure: The Role of Sarcopenia, Sarcopenic Obesity, and Cachexia. Curr. Probl. Cardiol. 2019 doi: 10.1016/j.cpcardiol.2019.03.006.
    1. Shimizu I., Minamino T. Physiological and pathological cardiac hypertrophy. J. Mol. Cell. Cardiol. 2016;97:245–262. doi: 10.1016/j.yjmcc.2016.06.001.
    1. Bekfani T., Pellicori P., Morris D.A., Ebner N., Valentova M., Steinbeck L., Wachter R., Elsner S., Sliziuk V., Schefold J.C., et al. Sarcopenia in patients with heart failure with preserved ejection fraction: Impact on muscle strength, exercise capacity and quality of life. Int. J. Cardiol. 2016;222:41–46. doi: 10.1016/j.ijcard.2016.07.135.
    1. Haykowsky M.J., Brubaker P.H., John J.M., Stewart K.P., Morgan T.M., Kitzman D.W. Determinants of exercise intolerance in elderly heart failure patients with preserved ejection fraction. J. Am. Coll. Cardiol. 2011;58:265–274. doi: 10.1016/j.jacc.2011.02.055.
    1. Haykowsky M.J., Tomczak C.R., Scott J.M., Paterson D.I., Kitzman D.W. Determinants of exercise intolerance in patients with heart failure and reduced or preserved ejection fraction. J. Appl. Physiol. 2015;119:739–744. doi: 10.1152/japplphysiol.00049.2015.
    1. Testa G., Cacciatore F., Galizia G., Della-Morte D., Mazzella F., Langellotto A., Russo S., Gargiulo G., De Santis D., Ferrara N., et al. Waist circumference but not body mass index predicts long-term mortality in elderly subjects with chronic heart failure. J. Am. Geriatr. Soc. 2010;58:1433–1440. doi: 10.1111/j.1532-5415.2010.02979.x.
    1. Bianchi L., Abete P., Bellelli G., Bo M., Cherubini A., Corica F., Di Bari M., Maggio M., Manca G.M., Rizzo M.R., et al. Prevalence and Clinical Correlates of Sarcopenia, Identified According to the EWGSOP Definition and Diagnostic Algorithm, in Hospitalized Older People: The GLISTEN Study. J. Gerontol. A Biol. Sci. Med. Sci. 2017;72:1575–1581. doi: 10.1093/gerona/glw343.
    1. Beyer S.E., Sanghvi M.M., Aung N., Hosking A., Cooper J.A., Paiva J.M., Lee A.M., Fung K., Lukaschuk E., Carapella V., et al. Prospective association between handgrip strength and cardiac structure and function in UK adults. PLoS ONE. 2018;13:e0193124. doi: 10.1371/journal.pone.0193124.
    1. Sartiani L., Spinelli V., Laurino A., Blescia S., Raimondi L., Cerbai E., Mugelli A. Pharmacological perspectives in sarcopenia: A potential role for renin-angiotensin system blockers? Clin. Cases Miner. Bone Metab. 2015;12:135–138. doi: 10.11138/ccmbm/2015.12.2.135.
    1. Carter C.S., Giovannini S., Seo D.O., DuPree J., Morgan D., Chung H.Y., Lees H., Daniels M., Hubbard G.B., Lee S., et al. Differential effects of enalapril and losartan on body composition and indices of muscle quality in aged male Fischer 344 × Brown Norway rats. Age. 2011;33:167–183. doi: 10.1007/s11357-010-9196-y.
    1. Burks T.N., Andres-Mateos E., Marx R., Mejias R., Van Erp C., Simmers J.L., Walston J.D., Ward C.W., Cohn R.D. Losartan restores skeletal muscle remodeling and protects against disuse atrophy in sarcopenia. Sci. Transl. Med. 2011;3:82ra37. doi: 10.1126/scitranslmed.3002227.
    1. Zhou L.S., Xu L.J., Wang X.Q., Huang Y.H., Xiao Q. Effect of Angiotensin-Converting Enzyme Inhibitors on Physical Function in Elderly Subjects: A Systematic Review and Meta-Analysis. Drugs Aging. 2015;32:727–735. doi: 10.1007/s40266-015-0288-3.
    1. Lainscak M., Keber I., Anker S.D. Body composition changes in patients with systolic heart failure treated with beta blockers: A pilot study. Int. J. Cardiol. 2006;106:319–322. doi: 10.1016/j.ijcard.2005.01.061.
    1. Hryniewicz K., Androne A.S., Hudaihed A., Katz S.D. Partial reversal of cachexia by beta-adrenergic receptor blocker therapy in patients with chronic heart failure. J. Card. Fail. 2003;9:464–468. doi: 10.1016/S1071-9164(03)00582-7.
    1. Burton L.A., Mcmurdo M.E., Struthers A.D. Mineralocorticoid antagonism: A novel way to treat sarcopenia and physical impairment in older people? Clin. Endocrinol. 2011;75:725–729. doi: 10.1111/j.1365-2265.2011.04148.x.
    1. Cunha T.F., Bacurau A.V., Moreira J.B., Paixão N.A., Campos J.C., Ferreira J.C., Leal M.L., Negrão C.E., Moriscot A.S., Wisløff U., et al. Exercise training prevents oxidative stress and ubiquitin–proteasome system overactivity and reverse skeletal muscle atro-phy in heart failure. PLoS ONE. 2012;7:e41701. doi: 10.1371/journal.pone.0041701.
    1. Smart N.A., Steele M. The effect of physical training on systemic proinflammatory cytokine expression in heart failure patients: A systematic review. Congest. Heart Fail. 2011;17:110–114. doi: 10.1111/j.1751-7133.2011.00217.x.
    1. Lenk K., Erbs S., Höllriegel R., Beck E., Linke A., Gielen S., Winkler S.M., Sandri M., Hambrecht R., Schuler G., et al. Exercise training leads to a reduction of elevated myostatin levels in patients with chronic heart failure. Eur. J. Prev. Cardiol. 2012;19:404–411. doi: 10.1177/1741826711402735.
    1. Murphy C.H., Oikawa S.Y., Phillips S.M. Dietary protein to maintain muscle mass in aging: A case for per-meal protein recommendations. J. Frailty Aging. 2016;5:49–58.
    1. Holeček M. Beta-hydroxy-beta-methylbutyrate supplementation and skeletal muscle in healthy and muscle-wasting conditions. J. Cachexia Sarcopenia Muscle. 2017;8:529–541. doi: 10.1002/jcsm.12208.
    1. Deutz N.E., Matheson E.M., Matarese L.E., Luo M., Baggs G.E., Nelson J.L., Hegazi R.A., Tappenden K.A., Ziegler T.R., NOURISH Study Group Readmission and mortality in malnourished, older, hospitalized adults treated with a specialized oral nutritional supplement: A randomized clinical trial. Clin. Nutr. 2016;35:18–26. doi: 10.1016/j.clnu.2015.12.010.
    1. Boxer R.S., Dauser D.A., Walsh S.J., Hager W.D., Kenny A.M. The association between vitamin D and inflammation with the 6-minute walk and frailty in patients with heart failure. J. Am. Geriatr. Soc. 2008;56:454–461. doi: 10.1111/j.1532-5415.2007.01601.x.
    1. Witham M.D. Vitamin D in chronic heart failure. Curr. Heart Fail. Rep. 2011;8:123–130. doi: 10.1007/s11897-011-0048-6.
    1. Saitoh M., Ebner N., von Haehling S., Anker S.D., Springer J. Therapeutic considerations of sarcopenia in heart failure patients. Expert Rev. Cardiovasc. Ther. 2018;16:133–142. doi: 10.1080/14779072.2018.1424542.
    1. Martone A.M., Marzetti E., Calvani R., Picca A., Tosato M., Santoro L., Di Giorgio A., Nesci A., Sisto A., Santoliquido A., et al. Exercise and Protein Intake: ASynergistic Approach against Sarcopenia. Biomed Res Int. 2017;2017:2672435. doi: 10.1155/2017/2672435.

Source: PubMed

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