Skeletal myopathy in patients with chronic heart failure: significance of anabolic-androgenic hormones

Journal of Cachexia, Sarcopenia and Muscle

Volumn 5, Issue 4, 2014, Pages 287-296

  Josiak, Krystian ^a,b   Jankowska, Ewa A ^a,b   Piepoli, Massimo F ^c   Banasiak, Waldemar ^b   Ponikowski, Piotr ^a,b  

^a WROCLAW MEDICAL UNIVERSITY   (Poland)

^b MILITARY HOSPITAL   (Poland)

^c GUGLIELMO DA SALICETO HOSPITAL   (Italy)

Author keywords

Anabolic androgens; Heart failure; Myopathy; Skeletal muscles; Testosterone

Indexed keywords

ANABOLIC ANDROGENIC HORMONE; HORMONES AND HORMONE ANALOGS; INSULIN; TESTOSTERONE; UNCLASSIFIED DRUG;

ANDROGEN DEFICIENCY; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; HEART FAILURE; HUMAN; INSULIN SENSITIVITY; METABOLIC CAPACITY; MUSCLE CELL; MUSCLE MASS; MUSCLE METABOLISM; MUSCLE REFLEX; MYOPATHY; PATHOGENESIS; REVIEW;

EID: 84951557362     PISSN: 21905991     EISSN: None     Source Type: Journal    
DOI: 10.1007/s13539-014-0152-z     Document Type: Review

References (95)

1. Al C, Poole-Wilson PA, Coats AJ. Exercise limitation in chronic heart failure: central role of the periphery. J Am Coll Cardiol. 1996;28:1092–102.
2. Piepoli MF, Ponikowski P, Clark AL, et al. A neural link to explain the “muscle hypothesis” of exercise intolerance in chronic heart failure. Am Heart J. 1999;137:1050–6.
3. Cicoira M, Davos CH, Francis DP, et al. Prediction of mortality in chronic heart failure from peak oxygen consumption adjusted for either body weight or lean tissue. J Card Fail. 2004;10:421–62.
4. De Groote P, Dagorn J, Soudan B, et al. B-type natriuretic peptide and peak exercise oxygen consumption provide independent information for risk stratification in patients with stable congestive heart failure. J Am Coll Cardiol. 2004;43:1584–9.
5. Lipkin DP, Canepa-Anson R, Stephens MR, Poole-Wilson PA. Factors determining symptoms in heart failure: comparison of fast and slow exercise test. Br Heart J. 1986;55:439–45.
6. Anker SD, Coots AJ. Metabolic, functional, and hemodynamic staging for CHF? Lancet. 1996;348:1530–1.
7. Coats AJS. What causes the symptoms of heart failure? Heart. 2001;86:574–8.
8. Coats AJS, Clark AL, Piepoli M, et al. Symptoms and quality of life in heart failure: the muscle hypothesis. Br Heart J. 1994;72(Suppl):536–9.
9. Coats AJS. The “muscle hypothesis” of chronic heart failure. J Mol Cell Cardiol. 1996;28:2255–62.
10. Piepoli MF, Coats AJS. The ‘skeletal muscle hypothesis in heart failure’ revised. Eur Heart J. 2013;34:486–8.
11. Anker SD, Chua TP, Ponikowski P, et al. Hormonal changes and catabolic/anabolic imbalance in chronic heart failure and their importance for cardiac cachexia. Circulation. 1997;96:526–34.
12. Wilson JR, Wiener DH, Fink LI, Ferraro N. Vasodilatatory behavior of skeletal muscle arteriole in patients with nonedematous chronic heart failure. Circulation. 1986;74:775–9.
13. Zelis R, Nellis S, Longhust J, et al. Abnormalities in the regional circulations accompanying congestive heart failure. Prog Cardiovasc Dis. 1975;18:181–99.
14. Anker SD, Swan JW, Volterrani M, et al. The influence of muscle mass, strength, fatigability and blood flow on exercise capacity in cachectic and non-cachectic patients with chronic heart failure. Eur Heart J. 1997;18:259–69.
15. Harrington D, Anker SD, Chua TP, et al. Skeletal muscle function and its relation to exercise tolerance in chronic heart failure. J Am Coll Cardiol. 1997;30:1758–64.
16. Suzuki K, Omiya K, Yamada S, et al. Relations between strength and endurance of leg skeletal muscle and cardiopulmonary exercise testing parameters in patients with chronic heart failure. J Cardiol. 2004;43:59–68.
17. Vescovo G, Volterrani M, Zennaro R, et al. Apoptosis in the skeletal muscle of patients with heart failure: investigation of clinical and biochemical changes. Heart. 2000;84:431–7.
18. Vescovo G, Zennaro R, Sandri M, et al. Apoptosis of skeletal muscle myofibers and interstitial cells in experimental heart failure. J Moll Cell Cardiol. 1998;30:2449–59.
19. Adams V, Jiang H, Yu J, et al. Apoptosis in skeletal myocytes of patients with chronic heart failure is associated with exercise intolerance. J Am Coll Cardiol. 1999;33:959–65.
20. Vescovo G, Ambrosio GB, Dalla Libera L. Apoptosis and changes in contractile protein pattern in the skeletal muscle in heart failure. Acta Physiol Scand. 2001;171:305–10.
21. Libera LD, Vescovo G. Muscle wastage in chronic heart failure, between apoptosis, catabolism and altered anabolism: a chimaeric view of inflammation? Curr Opin Clin Nutr Metab Care. 2004;7:435–41.
22. Vescovo G, Dalla Libera L. Skeletal muscle apoptosis in experimental heart failure: the only link between inflammation and skeletal muscle wastage? Curr Opin Clin Nutr Metab Care. 2006;9:416–22.
23. Conraads VM, Hoymans VY, Vermeulen T, et al. Exercise capacity in chronic heart failure patients is related to active gene transcription in skeletal muscles and not apoptosis. Eur J Cardiovasc Prev Rehabil. 2009;16:325–32.
24. Vescovo G, Serafini L, Facchin L, et al. Specific changes in skeletal muscle myosin heavy chain composition in cardiac failure: differences compared with disuse atrophy as assessed on microbiopsies by high resolution electrophoresis. Heart. 1996;76:337–43.
25. Lindsay DC, Lovegrove CA, Dunn M, et al. Histological abnormalities of diaphragmatic muscle may contribute to dyspnea in heart failure. Circulation. 1992;86(SupplI):1–514.
26. Sullivan MJ, Green HJ, Cobb FR. Skeletal muscle biochemistry and histology in ambulatory patients with long-term heart failure. Circulation. 1990;81:518–27.
27. Weber KT, Janicki JS. Lactate production during maximal and submaximal exercise in patients with chronic heart failure. J Am Coll Cardiol. 1985;6:717–24.
28. Ponikowski P, Chua TP, Francis D, et al. Muscle ergoreceptor overactivity reflects deterioration in clinical status and cardiorespiratory reflex control in chronic heart failure. Circulation. 2001;104:2324–30.
29. Scott AC, Wensel R, Davos CH, et al. Skeletal muscle reflex in heart failure patients: role of hydrogen. Circulation. 2003;107:300–6.
30. Scott AC, Wensel R, Davos CH, et al. Putative contribution of prostaglandin and bradykinin to muscle reflex hyperactivity in patients on ACE-inhibitor therapy for chronic heart failure. Eur Heart J. 2004;25:1806–13.
31. Mark AL, Victor RG, Nerhed C, Walkin BG. Microneurographic studies of the mechanisms of sympathetic nerve responses to static exercise in humans. Circ Res. 1985;57:461–9.
32. Piepoli MF, Kaczmarek A, Darrel P, et al. Reduced peripheral skeletal muscle mass and abnormal reflex physiology in chronic heart failure. Circulation. 2006;114:126–34.
33. von Haehling S, Steinbeck L, Doehner W, et al. Muscle wasting in heart failure: an overview. Int J Biochem Cell Biol. 2013;45:2257–65.
34. Bhasin S, Storer TW, Berman N, et al. The effects of supraphysiologic doses of testosterone on muscle size and strength in normal men. N Engl J Med. 1996;335:1–7.
35. Bahrke MS, Yesalis CE. Abuse of anabolic androgenic steroids and related substances in sport and exercise. Curr Opin Pharmacol. 2004;4:614–20.
36. Kadi F. Cellular and molecular mechanism responsible for the action of testosterone on human skeletal muscle. A basis for illegal performance enhancement. Br J Pharmacol. 2008;154:522–8.
37. Ottenbacher KJ, Ottenbacher ME, Ottenbacher AJ, et al. Androgen treatment and muscle strength in elderly men: a meta-analysis. J Am Geriatr Soc. 2006;54:1666–73.
38. Casaburi R, Bhasin S, Cosntino L, et al. Effects of testosterone and resistance training in men with chronic obstructive pulmonary disease. Am Respir Crit Care Med. 2004;170:870–8.
39. de Delenmarre-van de Waal HA, van Coeverden SC, Rotteveel J. Hormonal determinants of pubertal growth. J Pediatr Endocrinol Metab. 2001;14 suppl 6:1521–6.
40. Nieschlag E, Swerdloff R, Behere HM, et al. Investigation, treatment and monitoring of late-onset hypogonadism in males: ISA, ISSAM and EAU recommendations. Int J Androl. 2005;28:125–7.
41. Araujo AB, O’Donnell AB, Brambilla DJ, et al. Prevalence and incidence of androgen deficiency in middle-aged and older men: estimates from the Massachusetts Male Aging Study. J Clin Endocrinol Metab. 2004;89:5920–6.
42. Zitzmann M, Faber S, Nieschlag E. Association of specific symptoms and metabolic risks with serum testosterone in older men. J Clin Endocrinol Metab. 2006;91:4335–43.
43. Jankowska EA, Biel B, Majda J, et al. Anabolic deficiency in men with chronic heart failure: prevalence and detrimental impact n survival. Circulation. 2006;114:1829–37.
44. Anker SD, Sharma R. The syndrome of cardia cachexia. Int J Cardiol. 2002;85:51–66.
45. Jankowska EA, Jakubaszko J, Cwynar A, et al. Bone mineral status and bone loss over time in men with chronic systolic heart failure and their clinical and hormonal determinants. Eur J Heart Fail. 2009;11:28–38.
46. Jankowska EA. Znaczenie kliniczne i prognostyczne niedoboru hormonów anabolicznych u mężczyzn z niewydolnością serca [dissertation]. Akademia Medyczna we Wrocławiu 2008
47. Jankowska EA, Filippatos G, Ponikowska B, et al. Reduction in circulating testosterone relates to exercise capacity in men with chronic heart failure. J Card Fail. 2009;15:442–50.
48. Aizawa K, Iemitsu M, Maeda S, et al. Expression of steroidogenic enzymes and synthesis of sex steroid hormones from DHEA in skeletal muscle of rats. Am J Physiol Endorinol Metab. 2007;292:E577–84.
49. Labrie F, Belanger A, Luu-The V, et al. DHEA ad the intracrine formation of androgens and estrogens in peripheral target tissues: its role during aging. Steroids. 1998;63:322–8.
50. Ferrando AA, Sheffield-Moore M, Yeckel CW, et al. Testosterone administration to older men improves muscle function: molecular and physiological mechanisms. Am J Physiol Endocrinol Metab. 2002;282:E601–7.
51. Urban RJ, Bodenberg YH, Gilkison C, et al. Testosterone administration to elderly men increases skeletal muscle strength and protein synthesis. Am J Physiol. 1995;269:E820–6.
52. Herbst KL, Bhasin S. Testosterone action on skeletal muscle. Curr Opin Clin Nutr Metab Care. 2004;7:271–7.
53. Gruenewald DA, Matsumoto AM. Testosterone supplementation therapy for older men: potential benefits and risks. J Am Geriatr Soc. 2003;51:101–15.
54. Isidori AM, Giannetta E, Greco E, et al. Effects of testosterone on body composition, bone metabolism and serum lipid profile in middle-aged men: a meta-analysis. Clin Endocrinol. 2005;63:280–93.
55. Ferreira IM, Verreschi IT, Nery LE. The influence of 6 months of oral anabolic steroids on body mass and respiratory muscles in undernourished COPD patients. Chest. 1998;114:19–28.
56. Strawford A, Barbieri T, Neesa R, et al. Effects of nandrolone decanoate therapy in borderline hypogonadal men with HIV-associated weight loss. J Acquir Immune Defic Syndr Hum Retroviral. 1999;20:137–46.
57. Miller K, Biller B, Beauregard C, et al. Effects of testosterone replacement in androgen-deficient women with hypopituitarism: a randomized, double-blind, placebo-controlled study. J Clin Endocrinol Metab. 2006;91:1683–90.
58. Bhasin S, Calof O, Strorer T, et al. Drug insight: testosterone and selective androgen receptor modulators as anabolic therapies for chronic illness and aging. Nat Clin Pract Endocrinol Metab. 2006;2:146–59.
59. Bhasin S, Taylo WE, Singh R, et al. The mechanisms of androgen effects on body composition: mesenchymal pluripotent cell as the target of androgen action. J Gerontol A: Biol Med Sci. 2003;58:M1103–10.
60. Mendler L, Baka Z, Kovacs-Simon A, Dux L. Androgens negatively regulate myostatin expression in an androgen-dependent skeletal muscle. Biochem Biophys Res Commun. 2007;361:237–42.
61. Pires-Oliveira M, Margano AL, Perreiros-e-Silva LT, et al. Testosterone represses ubiquitin ligases atrogin-1 and Murf-1 expression in an androgen sensitive rat skeletal muscle in vivo. J Appl Physiol. 2010;108:266–73.
62. Wu Y, Zhao W, Zhao J, et al. Identification of androgen response elements in the insulin-like growth factor I upstream promoter. Endocrinology. 2007;148:2984–93.
63. Mauras N, Hayes V, Welch S, et al. Testosterone deficiency in young men: marked alterations in whole body protein kinetics, strength, and adiposity. J Clin Endocrinol Metab. 1998;83:1886–92.
64. Mourkioti F, Rosenthal N. IGF-1, inflammation and stem cells: interactions during muscle regeneration. Trends Immunol. 2005;26:535–42.
65. Kooijman R. Regulation of apoptosis by insulin-like growth factor (IGF)-I. Cytkine Growth Factor Rev. 2006;17:305–23.
66. Fernandez-Celemin L, Pasko N, Blomant V, Thissen JP. Inhibition of muscle insulin-like growth factor I expression by tumor necrosis factor-alpha. Am J Physiol Endocrinol Metab. 2002;283:E1279–90.
67. Schulze PC, Gielen S, Adams V, et al. Muscular levels of proinflammatory cytokines correlate with a reduced expression f insulin-like growth factor-I in chronic heart failure. Basic Res Cardiol. 2003;98:267–74.
68. Corrales JJ, Almeida M, Burgo R, et al. Androgen-replacement therapy depresses the ex vivo production of inflammatory cytokines by circulating antigen-resenting cells i aging type-2 diabetic men with partial androgen deficiency. J Endocrinol. 2006;189:595–604.
69. Liva SM, Voskuhl RR. Testosterone acts directly on CD4+ T lymphocytes to increase IL-10 production. J Immunol. 2001;167:2060–7.
70. Kapoor D, Goodwin E, Channer KS, Jones TH. Testosterone replacement therapy improves insulin resistance, glycaemic control, visceral adiposity and hypercholesterolaemia in hypogonadal men with type 2 diabetes. Eur J Endocrinol. 2006;154:899–906.
71. Perrini S, Natalicchio A, Laviola L, et al. Dehydroepiandrosterone stimulates glucose uptake in human and murine adipocytes by inducing GLUT1 and GLUT4 translocation to the plasma membrane. Diabetes. 2004;53:41–52.
72. Simon P, Charles MA, Lahlou N, et al. Androgen therapy improves insulin sensitivity and decreases leptin level in healthy adult men with low plasma total testosterone: a 3-mont randomized placebo-controlled trial. Diabetes Care. 2001;24:2149–51.
73. Doehner W, Rauchhaus M, Ponikowski P, et al. Impaired insulin sensitivity as an independent risk factor for mortality in patients with stable chronic heart failure. J Am Coll Cardiol. 2005;46:1019–26.
74. Wang X, Hu Z, Hu J, et al. Insulin resistance accelerates muscle protein degradation: activation of the ubiquitin-proteasome pathway by defects in muscle cell signaling. Endocrinology. 2006;147:4160–8.
75. Muthusamy T, Dhevika S, Murugeson P, Balasubramanian K. Testosterone deficiency impairs glucose oxidation through defective insulin and receptor gene expression in target tissues of adult male rats. Life Sci. 2007;81:534–42.
76. Miller VM, Mulvagh SL. Sex steroids and endothelial function: translating basic science to clinical practice. Trends Pharmacol Sci. 2007;28:263–70.
77. Svartberg J, Schirmer H, Medbo A, et al. Reduced pulmonary function is associated with lower levels of endogenous total and free testosterone. The Tromso study. Eur J Epidemiol. 2007;22:107–12.
78. El-Mas MM, Aify EA, Mohy El-Din MM, et al. Testosterone facilitates the baroreceptor control o reflex bradycardia: role of cardiac sympathetic and parasympathetic compartments. J Cardiovasc Pharmacol. 2001;38:754–63.
79. Jaimovich E, Espinosa A. Possible link of different slow calcium signals generated by membrane potential and hormones to differential gene expression in cultured muscle cells. Biol Res. 2004;37:625–33.
80. Jones RD, Jones TH, Channer KS. The influence of testosterone upon vascular reactivity. Eur J Endocrinol. 2004;151:29–37.
81. Lapauw B, Goemaere S, Crabbe P, et al. Is the effect of testosterone on body composition modulated by the androgen receptor gene CAG repeat polymorphism in elderly men? Eur J Endocrinol. 2007;156:395–401.
82. Lundin KB, Giwercman A, Dizeyi N, Giwercman YL. Functional in vitro characterization of the androgen receptor GGN polymorphism. Mol Cell Endocrinol. 2007;264:184–7.
83. Zitzmann M, Nieschlag E. The CAG repeat polymorphism within the androgen receptor gene and maleness. Int J Androl. 2003;26:76–83.
84. Lombardi G, Zarilli S, Colao A, et al. Estrogens and health in males. Mol Cel Endocrinol. 2001;178:51–5.
85. Larinov AA, Vasyliev DA, Mason J, et al. Aromatase in skeletal muscle. J Steroid Biochem Mol Biol. 2003;84:485–92.
86. Coodley GO, Coodley MK. A trial of testosterone therapy for HIV-associated weight loss. AIDS. 1997;11:1347–52.
87. Wolf SE, Thomas SJ, Dasu MR, et al. Improved net protein balance, lean mass, and gene expression changes with oxandrolone treatment in the severely burned. Ann Surg. 2003;237:801–10.
88. Pugh PJ, Jones RD, West JN, et al. Testosterone treatment for men with chronic heart failure. Heart. 2004;90:446–7.
89. Malkin CJ, Pugh PJ, West JN, et al. Testosterone therapy in men with moderate severity heart failure: a double-blind randomized placebo controlled trial. Eur Heart J. 2006;27:57–64.
90. Malkin CJ, Jones TH, Channer KS. The effect of testosterone on insulin sensitivity in men with heart failure. Eur JHeart Fail. 2007;9:44–50.
91. Caminiti G, Volterrani M, Iellamo F, et al. Effect of long-acting testosterone treatment on functional capacity, skeletal muscle performance, and baroreflex sensitivity in elderly patients with chronic heart failure. J Am Coll Cardiol. 2009;54:919–27.
92. Iellamo F, Volterrani M, Calminti G, et al. Testosterone therapy in women with chronic heart failure. A pilot double-blind, randomized, placebo-controlled study. J Am Coll Cardiol. 2010;56:1310–6.
93. Bronson FH, Matherre CM. Exposure to anabolic-androgenic steroids shortens life span of ale mice. Med Sci Sports Exerc. 1997;29:615–9.
94. Hartgens F, Kuipers H. Effects of androgenic-anabolic steroids in athletes. Sports Med. 2004;34:513–54.
95. Sullivan ML, Martinez CM, Gennis P, Gallagher EJ. The cardiac toxicity of anabolic steroids. Prog Cardiovasc Dis. 1998;41:1–15.