Sarcopenia and myokines profile as risk factors in cardiovascular diseases?
Mariusz Ciołkiewicz 1 , Anna Kuryliszyn-Moskal 1 , Anna Hryniewicz 1 , Karol Kamiński 1Abstract
Skeletal muscles and substances released during physical activity (myokines) have a beneficial influence on the functioning of the organism. Myokines (released also by myocardium) together with hepatokines and adipokines play an important role not only in energetic metabolism, but they also influence, among others, the function of the circulatory and nervous systems, modulation of inflammatory state and atherogenesis. Under pathological conditions connected with the presence of chronic diseases, chronic inflammatory state, low physical activity, long-term immobility the following consequences are observed: reduction of muscle mass and strength (sarcopenia) and changed profile of released myokines. The incidence of sarcopenia is connected with an unfavorable course of the aging process, often leading to disability and multiple morbidities. Sarcopenia can also lead to frailty syndrome, which not only worsens the prognosis of various diseases, but it can also increase the risk of medical procedures. Sarcopenia and adverse przymyokine profile are modifiable risk factors of cardiovascular diseases and affecting them may improve functional status and prognosis. An important intervention to improve muscles function and myokine profile, apart from nutritional treatment and pharmacotherapy, is regular physical activity as a component of cardiac rehabilitation. In our paper we focused on a review of the newest research regarding the association of sarcopenia and the profile of released myokines with incidence and course of cardiovascular diseases such as chronic heart failure, coronary artery disease, carotid artery atherosclerosis or ischemic cerebral stroke.
References
- 1. Ali S., Garcia J.M.: Sarcopenia, cachexia and aging: Diagnosis, mechanisms and therapeutic options. Gerontology, 2014; 60: 294–305
Google Scholar - 2. Anastasilakis A.D., Koulaxis D., Kefala N., Polyzos S.A., Upadhyay J., Pagkalidou E., Economou F., Anastasilakis C.D., Mantzoros C.S.: Circulating irisin levels are lower in patients with either stable coronary artery disease (CAD) or myocardial infarction (MI) versus healthy controls, whereas follistatin and activin A levels are higher and can discriminate MI from CAD with similar to CK-MB accuracy. Metabolism, 2017; 73: 1–8
Google Scholar - 3. Aronis K.N., Moreno M., Polyzos S.A., Moreno-Navarrete J.M., Ricart W., Delgado E., de la Hera J., Sahin-Efe A., Chamberland J.P., Berman R., Spiro A., Vokonas P., Fernández-Real J.M., Mantzoros C.S.: Circulating irisin levels and coronary heart disease: association with future acute coronary syndrome and major adverse cardiovascular events. Int. J. Obes., 2015; 39: 156–61
Google Scholar - 4. Aydin S., Aydin S., Kobat M.A., Kalayci M, Eren M.N., Yilmaz M., Kuloglu T., Gul E., Secen O., Alatas O.D., Baydas A.: Decreased saliva/serum irisin concentrations in the acute myocardial infarction promising for being a new candidate biomarker for diagnosis of this pathology. Peptides, 2014; 56: 141–45
Google Scholar - 5. Aydin S., Kuloglu T., Aydin S., Eren M.N., Celik A., Yilmaz M., Kalayci M., Sahin I., Gungor O., Gurel A., Ogeturk M., Dabak O.: Cardiac, skeletal muscle and serum irisin responses to with or without water exercise in young and old male rats: cardiac muscle produces more irisin than skeletal muscle. Peptides, 2014; 52: 68–73
Google Scholar - 6. Baumgartner R.N., Koehler K.M., Gallagher D., Romero L, Heymsfield S.B., Ross R.R., Garry P.J., Lindeman R.D.: Epidemiology of sarcopenia among elderly in New Mexico. Am. J. Epidemiol., 1998; 147: 755–63
Google Scholar - 7. Bellumkonda L., Tyrrell D., Hummel S.L., Goldstein D.R.: Pathophysiology of heart failure and frailty: a common inflammatory origin? Aging Cell, 2017; 16: 444–50
Google Scholar - 8. Biesemann N., Mendler L., Kostin S., Wietelmann A., Borchardt T., Braun T.: Myostatin induces interstitial fibrosis in the heart via TAK1 and p38. Cell Tissue Res., 2015; 361: 779–87
Google Scholar - 9. Brailoiu E., Deliu E., Sporici R.A., Brailoiu G.C.: Irisin evokes bradycardia by activating cardiac-projecting neurons of nucleus ambiguus. Physiol. Rep., 2015; 3: e12419
Google Scholar - 10. Butcher J.T., Ali M.I., Ma M.W., McCarthy C.G., Islam B.N., Fox L.G., Mintz J.D., Larion S., Fulton D.J., Stepp D.W.: Effect of myostatin deletion on cardiac and microvascular function. Physiol. Rep., 2017; 5: e13525
Google Scholar - 11. Campos A.M., Moura F.A., Santos S.N., Freitas W.M., Sposito A.C.: Sarcopenia, but not excess weight or increased caloric intake, is associated with coronary subclinical atherosclerosis in the very elderly. Atherosclerosis, 2017; 258: 138–44
Google Scholar - 12. Cao L., Zhang L., Chen S., Yuan Z., Liu S., Shen X., Zheng X., Qi X., Lee K.K., Chan J.Y., Cai D.: BDNF-mediated migration of cardiac microvascular endothelial cells is impaired during ageing. J. Cell. Mol. Med., 2012; 16: 3105–115
Google Scholar - 13. Carnethon M.R., Khan S.S.: An apparent obesity paradox in cardiac surgery. Circulation, 2017; 135: 864–866
Google Scholar - 14. Carson B.P.: The potential role of contraction-induced myokines in the regulation of metabolic function for the prevention and treatment of type 2 diabetes. Front. Endocrinol., 2017; 8: 97
Google Scholar - 15. Castillero E., Akashi H., Wang C., Najjar M., Ji R., Kennel P., Sweeney H.L., Schulze P.C., Georg I.: Cardiac myostatin upregulation occurs immediately after myocardial ischemia and is involved in skeletal muscle activation of atrophy. Biochem. Biophys. Res. Commun., 2015; 457: 106–11
Google Scholar - 16. Chang W.T., Wu C.H., Hsu L.W., Chen P.W., Yu J.R., Chang C.S., Tsai W.C., Liu P.Y.: Serum vitamin D, intact parathyroid hormone, and Fetuin A concentrations were associated with geriatric sarcopenia and cardiac hypertrophy. Sci Rep., 2017; 7: 40996
Google Scholar - 17. Chen K., Xu Z., Liu Y., Wang Z., Li Y., Xu X., Chen C., Xia T., Liao Q., Yao Y., Zeng C., He D., Yang Y., Tan T., Yi J. i wsp.: Irisin protects mitochondria function during pulmonary ischemia/reperfusion injury. Sci. Transl. Med., 2017; 9: eaao6298
Google Scholar - 18. Choi K.M.: The impact of organokines on insulin resistance, inflammation, and atherosclerosis. Endocrinol. Metab., 2016; 31: 1–6
Google Scholar - 19. Coin A., Sarti S., Ruggiero E., Giannini S., Pedrazzoni M., Minisola S., Rossini M., Del Puente A., Inelmen E.M., Manzato E., Sergi G.: Prevalence of sarcopenia based on different diagnostic criteria using DEXA and appendicular skeletal muscle mass reference values in an Italian population aged 20 to 80. J. Am. Med. Dir. Assoc., 2013; 14: 507–12
Google Scholar - 20. Collamati A., Marzetti E., Calvani R., Tosato M., D’Angelo E., Sisto A.N., Landi F.: Sarcopenia in heart failure: mechanisms and therapeutic strategies. J. Geriatr. Cardiol., 2016; 13: 615–624
Google Scholar - 21. Consitt L.A., Clark B.C.: The vicious cycle of myostatin signaling in sarcopenic obesity: Myostatin role in skeletal muscle growth, insulin signaling and implications for clinical trials. J. Frailty Aging, 2018; 7: 21–27
Google Scholar - 22. Cruz-Jentoft A.J., Baeyens J.P, Bauer J.M., Boirie Y., Cederholm T., Landi F., Martin F.C., Michel J.P., Rolland Y., Schneider S.M., Topinková E., Vandewoude M., Zamboni M.: Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing, 2010; 39: 412–23
Google Scholar - 23. Damatto R.L., Lima A.R., Martinez P.F., Cezar M.D., Okoshi K., Okoshi M.P.: Myocardial myostatin in spontaneously hypertensive rats with heart failure. Int. J. Cardiol., 2016; 215: 384–87
Google Scholar - 24. 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: 245–58
Google Scholar - 25. Desgeorges M.M., Devillard X., Toutain J., Castells J., Divoux D., Arnould D.F., Haqq C., Bernaudin M., Durieux A.C., Touzani O., Freyssenet D.G.: Pharmacological inhibition of myostatin improves skeletal muscle mass and function in a mouse model of stroke. Sci. Rep., 2017; 7: 14000
Google Scholar - 26. Desgeorges M.M., Devillard X., Toutain J., Divoux D., Castells J., Bernaudin M., Touzani O., Freyssenet D.G.: Molecular mechanisms of skeletal muscle atrophy in a mouse model of cerebral ischemia. Stroke, 2015; 46: 1673–680
Google Scholar - 27. Dong J., Dong Y., Dong Y., Chen F., Mitch W.E., Zhang L.: Inhibition of myostatin in mice improves insulin sensitivity via irisin-mediated cross talk between muscle and adipose tissues. Int. J. Obes., 2016; 40: 434–442
Google Scholar - 28. Efe T.H., Açar B., Ertem A.G., Yayla K.G., Algül E., Yayla Ç., Ünal S., Bilgin M., Çimen T., Kirbaş Ö., Yeter E.: Serum irisin level can predict the severity of coronary artery disease in patients with stable angina. Korean Circ. J., 2017; 47: 44–49
Google Scholar - 29. Emanuele E., Minoretti P., Pareja-Galeano H., Sanchis-Gomar F., Garatachea N., Lucia A.: Serum irisin levels, precocious myocardial infarction, and healthy exceptional longevity. Am. J. Med., 2014; 127: 888–90
Google Scholar - 30. Fielding R.A., Vellas B., Evans W.J., Bhasin S., Morley J.E., Newman A.B., Abellan van Kan G., Andrieu S., Bauer J., Breuille D., Cederholm T., Chandler J., De Meynard C., Donini L., Harris T. i wsp.: Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J. Am. Med. Dir. Assoc., 2011; 12: 249–256
Google Scholar - 31. Fried L.P., Tangen C.M., Walston J., Newman A.B., Hirsch C., Gottdiener J., Seeman T., Tracy R., Kop W.J., Burke G., McBurnie M.A., Cardiovascular Health Study Collaborative Research Group: Frailty in older adults: evidence for a phenotype. J. Gerontol. A. Biol. Sci. Med. Sci., 2001; 56: M146–M156
Google Scholar - 32. Fu J., Han Y., Wang J., Liu Y., Zheng S., Zhou L., Jose P.A., Zeng C.: Irisin lowers blood pressure by improvement of endothelial dysfunction via AMPK-Akt-eNOS-NO pathway in the spontaneously hypertensive rat. J. Am. Heart Assoc., 2016; 5: e003433
Google Scholar - 33. Fukushima A., Kinugawa S., Homma T., Masaki Y., Furihata T., Yokota T., Matsushima S., Abe T., Suga T., Takada S., Kadoguchi T., Katsuyama R., Oba K., Okita K., Tsutsui H.: Decreased serum brain-derived neurotrophic factor levels are correlated with exercise intolerance in patients with heart failure. Int. J. Cardiol., 2013; 168: e142–e144
Google Scholar - 34. Fukushima A., Kinugawa S., Homma T., Masaki Y., Furihata T., Yokota T., Matsushima S., Takada S., Kadoguchi T., Oba K., Okita K., Tsutsui H.: Serum brain-derived neurotropic factor level predicts adverse clinical outcomes in patients with heart failure. J. Card. Fail., 2015; 21: 300–06
Google Scholar - 35. Fulgenzi G., Tomassoni-Ardori F., Babini L., Becker J., Barrick C., Puverel S., Tessarollo L.: BDNF modulates heart contraction force and long-term homeostasis through truncated TrkB.T1 receptor activation. J. Cell Biol., 2015; 210: 1003–012
Google Scholar - 36. Furihata T., Kinugawa S., Fukushima A., Takada S., Homma T., Masaki Y., Abe T., Yokota T., Oba K., Okita K., Tsutsui H.: Serum myostatin levels are independently associated with skeletal muscle wasting in patients with heart failure. Int. J. Cardiol., 2016; 220: 483–87
Google Scholar - 37. Gamas L., Matafome P., Seiça R.: Irisin and myonectin regulation in the insulin resistant muscle: implications to adipose tissue: muscle crosstalk. J. Diabetes Res., 2015; 2015: 359159
Google Scholar - 38. Giudice J., Taylor J.M.: Muscle as a paracrine and endocrine organ. Curr. Opin. Pharmacol., 2017; 34: 49–55
Google Scholar - 39. Goel K., Gulati R., Reeder G.S., Lennon R.J., Lewis B.R, Behfar A., Sandhu G.S., Rihal C.S., Singh M..: Low body mass index, serum creatinine, and cause of death in patients undergoing percutaneous coronary intervention. J. Am. Heart Assoc., 2016; 5: e003633
Google Scholar - 40. Han A., Bokshan S.L, Marcaccio S.E., DePasse J.M., Daniels A.H.: Diagnostic criteria and clinical outcomes in sarcopenia research: A literature review. J. Clin. Med., 2018; 7: E70
Google Scholar - 41. Han D.S., Hsiao M.Y., Wang T.G., Chen S.Y., Yang W.S.: Relation between serum myokines and phase II cardiac rehabilitation. Medicine, 2017; 96: e6579
Google Scholar - 42. Han F., Zhang S., Hou N., Wang D., Sun X.: Irisin improves endothelial function in obese mice through the AMPK-eNOS pathway. Am. J. Physiol. Heart Circ. Physiol., 2015; 309: H1501–H1508
Google Scholar - 43. Hang P., Zhao J., Cai B., Tian S., Huang W., Guo J., Sun C., Li Y., Du Z.: Brain-derived neurotrophic factor regulates TRPC3/6 channels and protects against myocardial infarction in rodents. Int. J. Biol. Sci., 2015; 11: 536–545
Google Scholar - 44. Harada K., Suzuki S., Ishii H., Aoki T., Hirayama K., Shibata Y., Negishi Y., Sumi T., Kawashima K., Kunimura A., Shimbo Y., Tatami Y., Kawamiya T., Yamamoto D., Morimoto R. i wsp.: Impact of skeletal muscle mass on long-term adverse cardiovascular outcomes in patients with chronic kidney disease. Am. J. Cardiol. 2017; 119: 1275–1280
Google Scholar - 45. Hashimoto K.: Sigma-1 receptor chaperone and brain-derived neurotrophic factor: emerging links between cardiovascular disease and depression. Prog. Neurobiol., 2013; 100: 15–29
Google Scholar - 46. 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: 419–25
Google Scholar - 47. Ishida J., Konishi M., Saitoh M., Anker M., Anker S.D., Springer J.: Myostatin signaling is up-regulated in female patients with advanced heart failure. Int. J. Cardiol., 2017; 238: 37–42
Google Scholar - 48. Jiang R., Babyak M.A., Brummett B.H., Hauser E.R., Shah S.H., Becker R.C., Siegler I.C., Singh A., Haynes C., Chryst-Ladd M., Craig D.M., Williams R.B.: Brain-derived neurotrophic factor rs6265 (Val66Met) polymorphism is associated with disease severity and incidence of cardiovascular events in a patient cohort. Am. Heart J., 2017; 190: 40–45
Google Scholar - 49. Kalinkovich A., Livshits G.: Sarcopenic obesity or obese sarcopenia: A cross talk between age-associated adipose tissue and skeletal muscle inflammation as a main mechanism of the pathogenesis. Ageing Res. Rev. 2017; 35: 200–221
Google Scholar - 50. Kuloglu T., Aydin S., Eren M.N., Yilmaz M., Sahin I., Kalayci M., Sarman E., Kaya N., Yilmaz O.F., Turk A., Aydin Y., Yalcin M.H., Uras N., Gurel A., Ilhan S. i wsp.: Irisin: a potentially candidate marker for myocardial infarction. Peptides, 2014; 55: 85–91
Google Scholar - 51. Lecker S.H., Zavin A., Cao P., Arena R., Allsup K., Daniels K.M., Joseph J., Schulze P.C., Forman D.E.: Expression of the irisin precursor FNDC5 in skeletal muscle correlates with aerobic exercise performance in patients with heart failure. Circ. Heart Fail., 2012; 5: 812–18
Google Scholar - 52. Lee H.W., Ahmad M., Wang H.W., Leenen F.H.: Effects of exercise training on brain-derived neurotrophic factor in skeletal muscle and heart of rats post myocardial infarction. Exp. Physiol., 2017; 102: 314–328
Google Scholar - 53. Li D.J., Li Y.H., Yuan H.B., Qu L.F., Wang P.: The novel exercise-induced hormone irisin protects against neuronal injury via activation of the Akt and ERK1/2 signaling pathways and contributes to the neuroprotection of physical exercise in cerebral ischemia. Metabolism, 2017; 68: 31–42
Google Scholar - 54. Lim S., McMahon C.D., Matthews K.G., Devlin G.P., Elston M.S., Conaglen J.V.: Absence of myostatin improves cardiac function following myocardial infarction. Heart Lung Circ., 2018; 27: 693–701
Google Scholar - 55. Mariscalco G., Wozniak M.J., Dawson A.G. Serraino G.F., Porter R., Nath M., Klersy C., Kumar T., Murphy G.J.: Body mass index and mortality among adults undergoing cardiac surgery: A nationwide study with a systematic review and meta-analysis. Circulation, 2017; 135: 850–63
Google Scholar - 56. Marty E., Liu Y., Samuel A., Or O., Lane J.: A review of sarcopenia: Enhancing awareness of an increasingly prevalent disease. Bone, 2017; 105: 276–86
Google Scholar - 57. Masanes F., Culla A., Navarro-Gonzalez M., Navarro-Lopez M., Sacanella E., Torres B., Lopez-Soto A.: Prevalence of sarcopenia in healthy community-dwelling elderly in an urban area of Barcelona (Spain). J. Nutr. Health Aging, 2012; 16: 184–87
Google Scholar - 58. Minn Y.K., Suk S.H.: Higher skeletal muscle mass may protect against ischemic stroke in community-dwelling adults without stroke and dementia: The PRESENT project. BMC Geriatr., 2017; 17: 45
Google Scholar - 59. Morley J.E, Abbatecola A.M., Argiles J.M., Baracos V., Bauer J.,Bhasin S., Cederholm T., Coats A.J., Cummings S.R., Evans W.J., FearonK., Ferrucci L., Fielding R.A., Guralnik J.M., Harris T.B. i wsp.:Sarcopenia with limited mobility: An international consensus. J. Am.Med. Dir. Assoc., 2011; 12: 403–09
Google Scholar - 60. Narumi T., Watanabe T., Kadowaki S., Takahashi T., YokoyamaM., Kinoshita D., Honda Y., Funayama A., Nishiyama S., TakahashiH., Arimoto T., Shishido T., Miyamoto T., Kubota I.: Sarcopenia evaluatedby fat-free mass index is an important prognostic factor inpatients with chronic heart failure. Eur. J. Int. Med., 2015; 26: 118–22
Google Scholar - 61. Newman A.B., Kupelian V., Visser M., Simonsick E., GoodpasterB., Nevitt M., Kritchevsky S.B., Tylavsky F.A., Rubin S.M., HarrisT.B.: Sarcopenia: alternative definitions and associations with lowerextremity function. J. Am. Geriatr. Soc., 2003; 51: 1602–609
Google Scholar - 62. Niedziela J., Hudzik B., Niedziela N., Gąsior M., Gierlotka M.,Wasilewski J., Myrda K., Lekston A., Poloński L., Rozentryt P.: Theobesity paradox in acute coronary syndrome: a meta-analysis. Eur.J. Epidemiol., 2014; 29: 801–12
Google Scholar - 63. Okada S., Yokoyama M., Toko H., Tateno K., Moriya J., ShimizuI., Nojima A., Ito T., Yoshida Y., Kobayashi Y., Katagiri H., MinaminoT., Komuro I.: Brain-derived neurotrophic factor protects againstcardiac dysfunction after myocardial infarction via a central nervoussystem-mediated pathway. Arterioscler. Thromb. Vasc. Biol.,2012; 32: 1902–1909
Google Scholar - 64. Oreopoulos A., Padwal R., Kalantar-Zadeh K., Fonarow G.C., NorrisC.M., McAlister F.A.: Body mass index and mortality in heart failure:a meta-analysis. Am. Heart J., 2008; 156: 13–22
Google Scholar - 65. Park J., Ahmadi S.F., Streja E., Molnar M.Z., Flegal K.M., Gillen D.,Kovesdy C.P., Kalantar-Zadeh K.: Obesity paradox in end-stage kidneydisease patients. Prog. Cardiovasc. Dis., 2014; 56: 415–25
Google Scholar - 66. Park S., Ham J.O., Lee B.K.: A positive association between strokerisk and sarcopenia in men aged ≥ 50 years, but not women: resultsfrom the Korean National Health and Nutrition Examination Survey2008-2010. J. Nutr. Health Aging, 2014; 18: 806–12
Google Scholar - 67. Peng J., Deng X., Huang W, Yu J.H., Wang J.X., Wang J.P., YangS.B., Liu X., Wang L., Zhang Y., Zhou X.Y., Yang H., He Y.Z., Xu F.Y.:Irisin protects against neuronal injury induced by oxygen-glucosedeprivation in part depends on the inhibition of ROS-NLRP3 inflammatorysignaling pathway. Mol. Immunol., 2017; 91: 185–94
Google Scholar - 68. Perakakis N., Triantafyllou G.A., Fernández-Real J.M., Huh J.Y.,Park K.H., Seufert J., Mantzoros C.S.: Physiology and role of irisin inglucose homeostasis. Nat. Rev. Endocrinol., 2017; 13: 324–37
Google Scholar - 69. Phillips C., Baktir M.A., Srivatsan M., Salehi A.: Neuroprotectiveeffects of physical activity on the brain: a closer look at trophicfactor signaling. Front. Cell. Neurosci., 2014; 8: 170
Google Scholar - 70. Piepoli M.F., Hoes A.W., Agewall S., Albus C., Brotons C., CatapanoA.L., Cooney M.T., Corrà U., Cosyns B., Deaton C., Graham I., HallM.S., Hobbs F.D.R., Løchen M.L., Löllgen H. i wsp.: 2016 EuropeanGuidelines on cardiovascular disease prevention in clinical practice:The Sixth Joint Task Force of the European Society of Cardiologyand Other Societies on Cardiovascular Disease Prevention in ClinicalPractice (constituted by representatives of 10 societies and byinvited experts) Developed with the special contribution of the EuropeanAssociation for Cardiovascular Prevention & Rehabilitation(EACPR). Eur. Heart J., 2016; 37: 2315–381
Google Scholar - 71. Pius-Sadowska E., Machaliński B.: BDNF – A key player in cardiovascularsystem. J. Mol. Cell. Cardiol., 2017; 110: 54–60
Google Scholar - 72. Pratesi A., Tarantini F., Di Bari M.: Skeletal muscle: an endocrineorgan. Clin. Cases Miner. Bone Metab., 2013; 10: 11–14
Google Scholar - 73. Rosenberg I.H.: Sarcopenia: origins and clinical relevance. J.Nutr., 1997; 127: 990S–991S
Google Scholar - 74. Ryan A.S., Ivey F.M., Prior S., Li G., Hafer-Macko C.: Skeletalmuscle hypertrophy and muscle myostatin reduction after resistivetraining in stroke survivors. Stroke, 2011; 42: 416–420
Google Scholar - 75. Saitoh M., Ebner N., von Haehling S., Anker S.D., SpringerJ.: Therapeutic considerations of sarcopenia in heart failure patients.Expert Rev. Cardiovasc. Ther., 2018; 16: 133–142
Google Scholar - 76. Sesti G., Andreozzi F., Fiorentino T.V., Mannino G.C., SciacquaA., Marini M.A., Perticone F.: High circulating irisin levels areassociated with insulin resistance and vascular atherosclerosisin a cohort of nondiabetic adult subjects. Acta Diabetol., 2014;51: 705–13
Google Scholar - 77. Shen S., Gao R., Bei Y., Li J., Zhang H., Zhou Y., Yao W., Xu D.,Zhou F., Jin M., Wei S., Wang K., Xu X., Li Y., Xiao J. i wsp.: Serumirisin predicts mortality risk in acute heart failure patients. Cell.Physiol. Biochem., 2017; 42: 615–22
Google Scholar - 78. So B., Kim H.J., Kim J., Song W.: Exercise-induced myokines inhealth and metabolic diseases. Integr. Med. Res., 2014; 3: 172–79
Google Scholar - 79. Springer J., Springer J.I., Anker S.D.: Muscle wasting andsarcopenia in heart failure and beyond: update 2017. ESC HeartFail.; 2017; 4: 492–98
Google Scholar - 80. Sueta D., Hokimoto S., Sakamoto K., Akasaka T., Tabata N.,Kaikita K., Honda O., Naruse M., Ogawa H.: Validation of the highmortality rate of malnutrition-inflammation-atherosclerosis syndrome:Community-based observational study. Int. J. Cardiol.,2017; 230: 97–102
Google Scholar - 81. Sundarrajan L, Yeung C., Hahn L., Weber L.P., Unniappan S.:Irisin regulates cardiac physiology in zebrafish. PLoS One, 2017;12: e0181461
Google Scholar - 82. Suzuki H., Matsumoto Y., Ota H., Sugimura K., Takahashi J.,Ito K., Miyata S., Arai H., Taki Y., Furukawa K., Fukumoto Y., ShimokawaH.: Reduced brain-derived neurotrophic factor is associatedwith cognitive dysfunction in patients with chronic heartfailure. Geriatr. Gerontol. Int., 2017; 17: 852–54
Google Scholar - 83. Takashio S., Sugiyama S., Yamamuro M., Takahama H., HayashiT., Sugano Y., Izumiya Y., Hokimoto S., Minamino N., YasudaS., Anzai T., Ogawa H.: Significance of low plasma levels of brainderivedneurotrophic factor in patients with heart failure. Am. J.Cardiol., 2015; 116: 243–49
Google Scholar - 84. ter Maaten J.M., Damman K., Hillege H.L., Bakker S.J., AnkerS.D., Navis G., Voors A.A.: Creatinine excretion rate, a markerof muscle mass, is related to clinical outcome in patients withchronic systolic heart failure. Clin. Res. Cardiol., 2014; 103: 976–83
Google Scholar - 85. Tichet J., Vol S., Salle A., Goxe A., Berrut G., Ritz P.: Prevalenceof sarcopenia in the French senior population. J. Nutr. Health Aging,2008; 12: 202–206
Google Scholar - 86. Vaughan R.A., Gannon N.P., Mermier C.M., Conn C.A.: Irisin,a unique non-inflammatory myokine in stimulating skeletal musclemetabolism. J. Physiol. Biochem., 2015; 71: 679–89
Google Scholar - 87. von Haehling S.: The wasting continuum in heart failure:from sarcopenia to cachexia. Proc. Nutr. Soc., 2015; 74: 367–377
Google Scholar - 88. Wang H., Zhao Y.T., Zhang S., Dubielecka P.M., Du J., Yano N.,Chin Y.E., Zhuang S., Qin G., Zhao T.C.: Irisin plays a pivotal roleto protect the heart against ischemia and reperfusion injury. J.Cell. Physiol., 2017; 232: 3775–3785
Google Scholar - 89. Wu H., Guo P., Jin Z., Li X., Yang X., Tang C., Wang Y., Ke J.:Serum levels of irisin predict short-term outcomes in ischemicstroke. Cytokine, 2018 (w druku)
Google Scholar - 90. Zembron-Lacny A., Dziubek W., Rynkiewicz M., Morawin B.,Woźniewski M.: Peripheral brain-derived neurotrophic factor isrelated to cardiovascular risk factors in active and inactive elderlymen. Braz. J. Med. Biol. Res., 2016; 49: e5253
Google Scholar - 91. Zeng N., Xu J., Yao W., Li S., Ruan W., Xiao F.: Brain-derived neurotrophicfactor attenuates septic myocardial dysfunction via eNOS/NO pathway in rats. Oxid. Med. Cell. Longev., 2017; 2017: 1721434
Google Scholar - 92. Zhang J., Zhang W.: Can irisin be a linker between physical activityand brain function? Biomol. Concepts, 2016; 7: 253–58
Google Scholar - 93. Zhang W., Chang L., Zhang C., Zhang R., Li Z., Chai B., Li J.,Chen E., Mulholland M.: Central and peripheral irisin differentiallyregulate blood pressure. Cardiovasc. Drugs Ther., 2015;29: 121–27
Google Scholar - 94. Zhang W., Chang L, Zhang C., Zhang R., Li Z., Chai B., Li J., ChenE., Mulholland M.: Irisin: a myokine with locomotor activity. Neurosci.Lett., 2015; 595: 7–11
Google Scholar - 95. Zhang Y., Song H., Zhang Y., Wu F., Mu Q., Jiang M., Wang F.,Zhang W., Li L., Shao L., Li S., Yang L., Zhang M., Wu Q., Tang D.:Irisin inhibits atherosclerosis by promoting endothelial proliferationthrough microRNA126-5p. J. Am. Heart Assoc., 2016; 5: e004031
Google Scholar