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Anabolism to Catabolism: Serologic Clues to Nutritional Status in Heart Failure

  • Biomarkers of Heart Failure (J. Grodin & W.H.W. Tang, Section Editors)
  • Published:
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Abstract

Purpose of Review

Malnutrition, sarcopenia, and cachexia are areas of increasing interest in the management of patients with heart failure (HF). This review aims to examine the serological markers useful in guiding the physician in identification of these patients.

Recent Findings

Traditional nutritional biomarkers including albumin/prealbumin, iron, and vitamin D deficiencies predict poor prognosis in malnutrition and HF. Novel biomarkers including ghrelin, myostatin, C-terminal agrin fragment, and adiponectin have been identified as possible substrates and/or therapeutic targets in cardiac patients with sarcopenia and cachexia, though clinical trial data is limited to date.

Summary

Increased focus on nutritional deficiency syndromes in heart failure has led to the use of established markers of malnutrition as well as the identification of novel biomarkers in the management of these patients, though to date, their usage has been confined to the academic domain and further research is required to establish their role in the clinical setting.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Benjamin EJ, Blaha MJ, Chiuve SE, Cushman M, Das SR, Deo R, et al. Heart disease and stroke Statistics-2017 update: a report from the American Heart Association. Circulation. 2017;135(10):e146–603. https://doi.org/10.1161/cir.0000000000000485.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Heidenreich PA, Albert NM, Allen LA, Bluemke DA, Butler J, Fonarow GC, et al. Forecasting the impact of heart failure in the United States: a policy statement from the American Heart Association. Circ Heart Fail. 2013;6(3):606–19. https://doi.org/10.1161/HHF.0b013e318291329a.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Crespo-Leiro MG, Anker SD, Maggioni AP, Coats AJ, Filippatos G, Ruschitzka F, et al. European Society of Cardiology Heart Failure Long-Term Registry (ESC-HF-LT): 1-year follow-up outcomes and differences across regions. Eur J Heart Fail. 2016;18(6):613–25. https://doi.org/10.1002/ejhf.566.

    Article  PubMed  Google Scholar 

  4. Raposo André T, Lopes-Santos A. I GN. Cardiac Cachexia syndrome. Eur Med J Cardiol. 2017;5(1):101–7.

    Google Scholar 

  5. Goyal P, Almarzooq ZI, Horn EM, Karas MG, Sobol I, Swaminathan RV, et al. Characteristics of Hospitalizations for Heart Failure with Preserved Ejection Fraction. Am J Med. 2016;129(6):635.e15–26. https://doi.org/10.1016/j.amjmed.2016.02.007.

    Article  Google Scholar 

  6. McNallan SM, Chamberlain AM, Gerber Y, Singh M, Kane RL, Weston SA, et al. Measuring frailty in heart failure: a community perspective. Am Heart J. 2013;166(4):768–74. https://doi.org/10.1016/j.ahj.2013.07.008.

    Article  PubMed  Google Scholar 

  7. Vidan MT, Sanchez E, Fernandez-Aviles F, Serra-Rexach JA, Ortiz J, Bueno H. FRAIL-HF, a study to evaluate the clinical complexity of heart failure in nondependent older patients: rationale, methods and baseline characteristics. Clin Cardiol. 2014;37(12):725–32. https://doi.org/10.1002/clc.22345.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146–56. https://doi.org/10.1093/gerona/56.3.m146.

    Article  CAS  PubMed  Google Scholar 

  9. Cederholm T, Bosaeus I, Barazzoni R, Bauer J, Van Gossum A, Klek S, et al. Diagnostic criteria for malnutrition - An ESPEN Consensus Statement. Clin Nutr (Edinburgh, Scotland). 2015;34(3):335–40. https://doi.org/10.1016/j.clnu.2015.03.001.

    Article  CAS  Google Scholar 

  10. Tevik K, Thurmer H, Husby MI, de Soysa AK, Helvik AS. Nutritional risk screening in hospitalized patients with heart failure. Clin Nutr (Edinburgh, Scotland). 2015;34(2):257–64. https://doi.org/10.1016/j.clnu.2014.03.014.

    Article  Google Scholar 

  11. Ponikowski P, van Veldhuisen DJ, Comin-Colet J, Ertl G, Komajda M, Mareev V, et al. Beneficial effects of long-term intravenous iron therapy with ferric carboxymaltose in patients with symptomatic heart failure and iron deficiencydagger. Eur Heart J. 2015;36(11):657–68. https://doi.org/10.1093/eurheartj/ehu385.

    Article  CAS  PubMed  Google Scholar 

  12. Lin H, Zhang H, Lin Z, Li X, Kong X, Sun G. Review of nutritional screening and assessment tools and clinical outcomes in heart failure. Heart Fail Rev. 2016;21(5):549–65. https://doi.org/10.1007/s10741-016-9540-0.

    Article  CAS  PubMed  Google Scholar 

  13. Kruizenga HM, Seidell JC, de Vet HC, Wierdsma NJ, van Bokhorst-de van der Schueren MA. Development and validation of a hospital screening tool for malnutrition: the short nutritional assessment questionnaire (SNAQ). Clin Nutr (Edinburgh, Scotland). 2005;24(1):75–82. https://doi.org/10.1016/j.clnu.2004.07.015.

    Article  CAS  Google Scholar 

  14. Hajahmadi M, Shemshadi S, Khalilipur E, Amin A, Taghavi S, Maleki M, et al. Muscle wasting in young patients with dilated cardiomyopathy. J Cachexia Sarcopenia Muscle. 2017;8(4):542–8. https://doi.org/10.1002/jcsm.12193.

    Article  PubMed  PubMed Central  Google Scholar 

  15. • Iwakami N, Nagai T, Furukawa TA, Sugano Y, Honda S, Okada A, et al. Prognostic value of malnutrition assessed by controlling nutritional status score for long-term mortality in patients with acute heart failure. Int J Cardiol. 2017;230:529–36. https://doi.org/10.1016/j.ijcard.2016.12.064 This study highlights the importance of assessing nutritional status in acute HF patients due to the significant association with increased mortality identified in this group.

    Article  PubMed  Google Scholar 

  16. Sargento L, Satendra M, Almeida I, Sousa C, Gomes S, Salazar F, et al. Nutritional status of geriatric outpatients with systolic heart failure and its prognostic value regarding death or hospitalization, biomarkers and quality of life. J Nutr Health Aging. 2013;17(4):300–4. https://doi.org/10.1007/s12603-013-0030-y.

    Article  CAS  PubMed  Google Scholar 

  17. • Lewis GD, Malhotra R, Hernandez AF, SE MN, Smith A, Felker GM, et al. Effect of Oral Iron Repletion on Exercise Capacity in Patients With Heart Failure With Reduced Ejection Fraction and Iron Deficiency: The IRONOUT HF Randomized Clinical TrialOral Iron for Heart FailureOral Iron for Heart Failure. JAMA. 2017;317(19):1958–66. https://doi.org/10.1001/jama.2017.5427 The results for IV iron have previously been promising with improvements in exercise capacity in HF patients however, this study examines the use of oral iron and found it to be of little benefit in the treatment group.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Chiarantini D, Volpato S, Sioulis F, Bartalucci F, Del Bianco L, Mangani I, et al. Lower extremity performance measures predict long-term prognosis in older patients hospitalized for heart failure. J Card Fail. 2010;16(5):390–5. https://doi.org/10.1016/j.cardfail.2010.01.004.

    Article  PubMed  Google Scholar 

  19. Chung CJ, Wu C, Jones M, Kato TS, Dam TT, Givens RC, et al. Reduced handgrip strength as a marker of frailty predicts clinical outcomes in patients with heart failure undergoing ventricular assist device placement. J Card Fail. 2014;20(5):310–5. https://doi.org/10.1016/j.cardfail.2014.02.008.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Adejumo OL, Koelling TM, Hummel SL. Nutritional risk index predicts mortality in hospitalized advanced heart failure patients. J Heart Lung Transplant : the official publication of the International Society for Heart Transplantation. 2015;34(11):1385–9. https://doi.org/10.1016/j.healun.2015.05.027.

    Article  Google Scholar 

  21. Santilli V, Bernetti A, Mangone M, Paoloni M. Clinical definition of sarcopenia. Clin Cases Mineral Bone Metab : the official journal of the Italian Society of Osteoporosis, Mineral Metabolism, and Skeletal Diseases. 2014;11(3):177–80.

    Google Scholar 

  22. Fulster S, Tacke M, Sandek A, Ebner N, Tschope C, Doehner W, et al. Muscle wasting in patients with chronic heart failure: results from the studies investigating co-morbidities aggravating heart failure (SICA-HF). Eur Heart J. 2013;34(7):512–9. https://doi.org/10.1093/eurheartj/ehs381.

    Article  CAS  PubMed  Google Scholar 

  23. Yost G, Bhat G. Relationship between handgrip strength and length of stay for left ventricular assist device implantation. Nutr Clin Pract : official publication of the American Society for Parenteral and Enteral Nutrition. 2017;32(1):98–102. https://doi.org/10.1177/0884533616665926.

    Article  Google Scholar 

  24. Anker SD, Sharma R. The syndrome of cardiac cachexia. Int J Cardiol. 2002;85(1):51–66.

    Article  PubMed  Google Scholar 

  25. Evans WJ, Morley JE, Argiles J, Bales C, Baracos V, Guttridge D, et al. Cachexia: a new definition. Clin Nutr (Edinburgh, Scotland). 2008;27(6):793–9. https://doi.org/10.1016/j.clnu.2008.06.013.

    Article  CAS  Google Scholar 

  26. Farkas J, von Haehling S, Kalantar-Zadeh K, Morley JE, Anker SD, Lainscak M. Cachexia as a major public health problem: frequent, costly, and deadly. J Cachexia Sarcopenia Muscle. 2013;4(3):173–8. https://doi.org/10.1007/s13539-013-0105-y.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Anker SD, Ponikowski P, Varney S, Chua TP, Clark AL, Webb-Peploe KM, et al. Wasting as independent risk factor for mortality in chronic heart failure. Lancet (London, England). 1997;349(9058):1050–3. https://doi.org/10.1016/s0140-6736(96)07015-8.

    Article  CAS  Google Scholar 

  28. Kondrup J, Rasmussen HH, Hamberg O, Stanga Z. Nutritional risk screening (NRS 2002): a new method based on an analysis of controlled clinical trials. Clin Nutr (Edinburgh, Scotland). 2003;22(3):321–36.

    Article  Google Scholar 

  29. Heberton GA, Nassif M, Bierhals A, Novak E, LaRue SJ, Lima B, et al. Usefulness of psoas muscle area determined by computed tomography to predict mortality or prolonged length of hospital stay in patients undergoing left ventricular assist device implantation. Am J Cardiol. 2016;118(9):1363–7. https://doi.org/10.1016/j.amjcard.2016.07.061.

    Article  PubMed  Google Scholar 

  30. Bibas L, Saleh E, Alkharji S, Chetrit J, Mullie L, Cantarovich M, et al. Sarcopenia and mortality after heart transplantation. Can J Cardiol. 2017;33(10):S71–S2. https://doi.org/10.1016/j.cjca.2017.07.145.

    Article  Google Scholar 

  31. Kumar A, Ansari BA, Kim J, Suri A, Gaddam S, Yenigalla S, et al. Axial muscle size as a strong predictor of death in subjects with and without heart failure. J Am Heart Assoc. 2019;8(4):e010554. https://doi.org/10.1161/jaha.118.010554.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Rossignol P, Masson S, Barlera S, Girerd N, Castelnovo A, Zannad F, et al. Loss in body weight is an independent prognostic factor for mortality in chronic heart failure: insights from the GISSI-HF and Val-HeFT trials. Eur J Heart Fail. 2015;17(4):424–33. https://doi.org/10.1002/ejhf.240.

    Article  PubMed  Google Scholar 

  33. Tsuchida K, Fujihara Y, Hiroki J, Hakamata T, Sakai R, Nishida K, et al. Significance of Sarcopenia Evaluation in Acute Decompensated Heart Failure. Skeletal Muscle Mass Index versus Fat-Free Mass Index. Int Heart J. 2018;59(1):143–8. https://doi.org/10.1536/ihj.17-057.

    Article  CAS  PubMed  Google Scholar 

  34. Narumi T, Watanabe T, Kadowaki S, Takahashi T, Yokoyama M, Kinoshita D, et al. Sarcopenia evaluated by fat-free mass index is an important prognostic factor in patients with chronic heart failure. Eur J Int Med. 2015;26(2):118–22. https://doi.org/10.1016/j.ejim.2015.01.008.

    Article  Google Scholar 

  35. Melenovsky V, Kotrc M, Borlaug BA, Marek T, Kovar J, Malek I, et al. Relationships between right ventricular function, body composition, and prognosis in advanced heart failure. J Am Coll Cardiol. 2013;62(18):1660–70. https://doi.org/10.1016/j.jacc.2013.06.046.

    Article  PubMed  Google Scholar 

  36. Kuzuya M, Izawa S, Enoki H, Okada K, Iguchi A. Is serum albumin a good marker for malnutrition in the physically impaired elderly? Clin Nutr (Edinburgh, Scotland). 2007;26(1):84–90. https://doi.org/10.1016/j.clnu.2006.07.009.

    Article  CAS  Google Scholar 

  37. Bharadwaj S, Ginoya S, Tandon P, Gohel TD, Guirguis J, Vallabh H, et al. Malnutrition: laboratory markers vs nutritional assessment. Gastroenterol Rep (Oxf). 2016;4(4):272–80. https://doi.org/10.1093/gastro/gow013.

    Article  Google Scholar 

  38. Lourenço P, Silva S, Friões F, Alvelos M, Amorim M, Couto M, et al. Low prealbumin is strongly associated with adverse outcome in heart failure. Heart. 2014;100(22):1780–5. https://doi.org/10.1136/heartjnl-2014-305747.

    Article  CAS  PubMed  Google Scholar 

  39. von Haehling S, Ebner N, Evertz R, Ponikowski P, Anker SD. Iron deficiency in heart failure: an overview. JACC Heart failure. 2019;7(1):36–46. https://doi.org/10.1016/j.jchf.2018.07.015.

    Article  Google Scholar 

  40. Cappellini MD, Comin-Colet J, de Francisco A, Dignass A, Doehner W, Lam CS, et al. Iron deficiency across chronic inflammatory conditions: international expert opinion on definition, diagnosis, and management. Am J Hematol. 2017;92(10):1068–78. https://doi.org/10.1002/ajh.24820.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Boulton FE. The myoglobin content of human skeletal muscle. Br J Haematol. 1973;25(2):281.

    CAS  PubMed  Google Scholar 

  42. Stugiewicz M, Tkaczyszyn M, Kasztura M, Banasiak W, Ponikowski P, Jankowska EA. The influence of iron deficiency on the functioning of skeletal muscles: experimental evidence and clinical implications. Eur J Heart Fail. 2016;18(7):762–73. https://doi.org/10.1002/ejhf.467.

    Article  PubMed  Google Scholar 

  43. Martens P, Nijst P, Verbrugge FH, Smeets K, Dupont M, Mullens W. Impact of iron deficiency on exercise capacity and outcome in heart failure with reduced, mid-range and preserved ejection fraction. Acta Cardiol. 2018;73(2):115–23. https://doi.org/10.1080/00015385.2017.1351239.

    Article  PubMed  Google Scholar 

  44. Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, et al. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2011;96(7):1911–30. https://doi.org/10.1210/jc.2011-0385.

    Article  CAS  PubMed  Google Scholar 

  45. Witte KK, Byrom R, Gierula J, Paton MF, Jamil HA, Lowry JE, et al. Effects of vitamin D on cardiac function in patients with chronic HF: the VINDICATE study. J Am Coll Cardiol. 2016;67(22):2593–603. https://doi.org/10.1016/j.jacc.2016.03.508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Sanders KM, Scott D, Ebeling PR. Vitamin D deficiency and its role in muscle-bone interactions in the elderly. Curr Osteoporos Rep. 2014;12(1):74–81. https://doi.org/10.1007/s11914-014-0193-4.

    Article  PubMed  Google Scholar 

  47. Visser M, Deeg DJ, Lips P. Low vitamin D and high parathyroid hormone levels as determinants of loss of muscle strength and muscle mass (sarcopenia): the longitudinal aging study Amsterdam. J Clin Endocrinol Metab. 2003;88(12):5766–72. https://doi.org/10.1210/jc.2003-030604.

    Article  CAS  PubMed  Google Scholar 

  48. Wicherts IS, van Schoor NM, Boeke AJ, Visser M, Deeg DJ, Smit J, et al. Vitamin D status predicts physical performance and its decline in older persons. J Clin Endocrinol Metab. 2007;92(6):2058–65. https://doi.org/10.1210/jc.2006-1525.

    Article  CAS  PubMed  Google Scholar 

  49. Costanzo S, De Curtis A, Di Castelnuovo A, Persichillo M, Bonaccio M, Pounis G, et al. Serum vitamin D deficiency and risk of hospitalization for heart failure: prospective results from the Moli-sani study. Nutr Metab Cardiovasc Dis : NMCD. 2018;28(3):298–307. https://doi.org/10.1016/j.numecd.2017.11.008.

    Article  CAS  PubMed  Google Scholar 

  50. Heywood JT, Fonarow GC, Costanzo MR, Mathur VS, Wigneswaran JR, Wynne J. High prevalence of renal dysfunction and its impact on outcome in 118,465 patients hospitalized with acute decompensated heart failure: a report from the ADHERE database. J Card Fail. 2007;13(6):422–30. https://doi.org/10.1016/j.cardfail.2007.03.011.

    Article  PubMed  Google Scholar 

  51. Tuegel C, Bansal N. Heart failure in patients with kidney disease. Heart. 2017;103(23):1848–53. https://doi.org/10.1136/heartjnl-2016-310794.

    Article  CAS  PubMed  Google Scholar 

  52. Shlipak MG, Stehman-Breen C, Fried LF, Song X, Siscovick D, Fried LP, et al. The presence of frailty in elderly persons with chronic renal insufficiency. Am J Kidney Dis : the official journal of the National Kidney Foundation. 2004;43(5):861–7.

    Article  Google Scholar 

  53. Maurer MS, Horn E, Reyentovich A, Dickson VV, Pinney S, Goldwater D, et al. Can a left ventricular assist device in individuals with advanced systolic heart failure improve or reverse frailty? J Am Geriatr Soc. 2017;65(11):2383–90. https://doi.org/10.1111/jgs.15124.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Jenkins R, Mandarano L, Gugathas S, Kaski JC, Anderson L, Banerjee D. Impaired renal function affects clinical outcomes and management of patients with heart failure. ESC heart failure. 2017;4(4):576–84. https://doi.org/10.1002/ehf2.12185.

    Article  PubMed  PubMed Central  Google Scholar 

  55. KDOQI. Clinical practice guidelines and clinical practice recommendations for Anemia in chronic kidney disease. Am J Kidney Dis : the official journal of the National Kidney Foundation. 2006;47(5 Suppl 3):S11–145. https://doi.org/10.1053/j.ajkd.2006.03.010.

    Article  Google Scholar 

  56. Zhou Y, Hellberg M, Svensson P, Hoglund P, Clyne N. Sarcopenia and relationships between muscle mass, measured glomerular filtration rate and physical function in patients with chronic kidney disease stages 3-5. Nephrol Dialysis Transplant : official publication of the European Dialysis and Transplant Association - European Renal Association. 2018;33(2):342–8. https://doi.org/10.1093/ndt/gfw466.

    Article  CAS  Google Scholar 

  57. Pereira RA, Cordeiro AC, Avesani CM, Carrero JJ, Lindholm B, Amparo FC, et al. Sarcopenia in chronic kidney disease on conservative therapy: prevalence and association with mortality. Nephrol Dialysis Transplant : official publication of the European Dialysis and Transplant Association - European Renal Association. 2015;30(10):1718–25. https://doi.org/10.1093/ndt/gfv133.

    Article  CAS  Google Scholar 

  58. Anker SD, Ponikowski PP, Clark AL, Leyva F, Rauchhaus M, Kemp M, et al. Cytokines and neurohormones relating to body composition alterations in the wasting syndrome of chronic heart failure. Eur Heart J. 1999;20(9):683–93. https://doi.org/10.1053/euhj.1998.1446.

    Article  CAS  PubMed  Google Scholar 

  59. Cesari M, Penninx BW, Pahor M, Lauretani F, Corsi AM, Rhys Williams G, et al. Inflammatory markers and physical performance in older persons: the InCHIANTI study. J Gerontol A Biol Sci Med Sci. 2004;59(3):242–8. https://doi.org/10.1093/gerona/59.3.m242.

    Article  PubMed  Google Scholar 

  60. Bian AL, Hu HY, Rong YD, Wang J, Wang JX, Zhou XZ. A study on relationship between elderly sarcopenia and inflammatory factors IL-6 and TNF-alpha. Eur J Med Res. 2017;22(1):25. https://doi.org/10.1186/s40001-017-0266-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Yoshihisa A, Kanno Y, Watanabe S, Yokokawa T, Abe S, Miyata M, et al. Impact of nutritional indices on mortality in patients with heart failure. Open heart. 2018;5(1):e000730. https://doi.org/10.1136/openhrt-2017-000730.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Castellano G, Affuso F, Conza PD, Fazio S. The GH/IGF-1 Axis and heart failure. Curr Cardiol Rev. 2009;5(3):203–15. https://doi.org/10.2174/157340309788970306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Anker SD, Volterrani M, Pflaum CD, Strasburger CJ, Osterziel KJ, Doehner W, et al. Acquired growth hormone resistance in patients with chronic heart failure: implications for therapy with growth hormone. J Am Coll Cardiol. 2001;38(2):443–52.

    Article  CAS  PubMed  Google Scholar 

  64. Cittadini A, Saldamarco L, Marra AM, Arcopinto M, Carlomagno G, Imbriaco M, et al. Growth hormone deficiency in patients with chronic heart failure and beneficial effects of its correction. J Clin Endocrinol Metab. 2009;94(9):3329–36. https://doi.org/10.1210/jc.2009-0533.

    Article  CAS  PubMed  Google Scholar 

  65. Bhandari SS, Narayan H, Jones DJ, Suzuki T, Struck J, Bergmann A, et al. Plasma growth hormone is a strong predictor of risk at 1 year in acute heart failure. Eur J Heart Fail. 2016;18(3):281–9. https://doi.org/10.1002/ejhf.459.

    Article  CAS  PubMed  Google Scholar 

  66. Hassfeld S, Eichhorn C, Stehr K, Naegele H, Geier C, Steeg M, et al. Insulin-like growth factor-binding proteins 2 and 3 are independent predictors of a poor prognosis in patients with dilated cardiomyopathy. Heart. 2007;93(3):359–60. https://doi.org/10.1136/hrt.2006.090092.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Liu H, Bravata DM, Olkin I, Nayak S, Roberts B, Garber AM, et al. Systematic review: the safety and efficacy of growth hormone in the healthy elderly. Ann Intern Med. 2007;146(2):104–15.

    Article  PubMed  Google Scholar 

  68. Buvat J, Maggi M, Guay A, Torres LO. Testosterone deficiency in men: systematic review and standard operating procedures for diagnosis and treatment. J Sex Med. 2013;10(1):245–84. https://doi.org/10.1111/j.1743-6109.2012.02783.x.

    Article  CAS  PubMed  Google Scholar 

  69. Kalicinska E, Wojtas K, Majda J, Doehner W, von Haehling S, Banasiak W, et al. Anabolic deficiencies in men with systolic heart failure: do co-morbidities and therapies really contribute significantly? Aging Male : the official journal of the International Society for the Study of the Aging Male. 2013;16(3):123–31. https://doi.org/10.3109/13685538.2013.807427.

    Article  CAS  Google Scholar 

  70. Wu HY, Wang XF, Wang JH, Li JY. Testosterone level and mortality in elderly men with systolic chronic heart failure. Asian J Androl. 2011;13(5):759–63. https://doi.org/10.1038/aja.2011.26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Jankowska EA, Filippatos G, Ponikowska B, Borodulin-Nadzieja L, Anker SD, Banasiak W, et al. Reduction in circulating testosterone relates to exercise capacity in men with chronic heart failure. J Card Fail. 2009;15(5):442–50. https://doi.org/10.1016/j.cardfail.2008.12.011.

    Article  CAS  PubMed  Google Scholar 

  72. Jankowska EA, Biel B, Ponikowska B, Borodulin-Nadzieja L, Petruk-Kowalczyk J, Banasiak W, et al. 679 Reduction in serum testosterone deteriorates exercise capacity in men in the course of chronic heart failure. Eur J Heart Fail Suppl. 2007;6(S1):148. https://doi.org/10.1016/S1567-4215(07)60413-5.

    Article  Google Scholar 

  73. Jankowska EA, Biel B, Majda J, Szklarska A, Lopuszanska M, Medras M, et al. Anabolic deficiency in men with chronic heart failure: prevalence and detrimental impact on survival. Circulation. 2006;114(17):1829–37. https://doi.org/10.1161/circulationaha.106.649426.

    Article  CAS  PubMed  Google Scholar 

  74. Loncar G, Springer J, Anker M, Doehner W, Lainscak M. Cardiac cachexia: hic et nunc. J Cachexia Sarcopenia Muscle. 2016;7(3):246–60. https://doi.org/10.1002/jcsm.12118.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Serra-Prat M, Palomera E, Roca M, Puig-Domingo M. Long-term effect of ghrelin on nutritional status and functional capacity in the elderly: a population-based cohort study. Clin Endocrinol. 2010;73(1):41–7. https://doi.org/10.1111/j.1365-2265.2009.03730.x.

    Article  CAS  Google Scholar 

  76. Nagaya N, Uematsu M, Kojima M, Date Y, Nakazato M, Okumura H, et al. Elevated circulating level of ghrelin in cachexia associated with chronic heart failure: relationships between ghrelin and anabolic/catabolic factors. Circulation. 2001;104(17):2034–8.

    Article  CAS  PubMed  Google Scholar 

  77. Steinbeck L, Ebner N, Valentova M, Bekfani T, Elsner S, Dahinden P, et al. Detection of muscle wasting in patients with chronic heart failure using C-terminal agrin fragment: results from the studies investigating co-morbidities aggravating heart failure (SICA-HF). Eur J Heart Fail. 2015;17(12):1283–93. https://doi.org/10.1002/ejhf.400.

    Article  CAS  PubMed  Google Scholar 

  78. Araujo JP, Lourenco P, Rocha-Goncalves F, Ferreira A, Bettencourt P. Adiponectin is increased in cardiac cachexia irrespective of body mass index. Eur J Heart Fail. 2009;11(6):567–72. https://doi.org/10.1093/eurjhf/hfp046.

    Article  CAS  PubMed  Google Scholar 

  79. Szabo T, Scherbakov N, Sandek A, Kung T, von Haehling S, Lainscak M, et al. Plasma adiponectin in heart failure with and without cachexia: catabolic signal linking catabolism, symptomatic status, and prognosis. Nutr Metab Cardiovasc Dis : NMCD. 2014;24(1):50–6. https://doi.org/10.1016/j.numecd.2013.04.015.

    Article  CAS  PubMed  Google Scholar 

  80. Breitbart A, Auger-Messier M, Molkentin JD, Heineke J. Myostatin from the heart: local and systemic actions in cardiac failure and muscle wasting. Am J Physiol Heart Circ Physiol. 2011;300(6):H1973–H82. https://doi.org/10.1152/ajpheart.00200.2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Lenk K, Schur R, Linke A, Erbs S, Matsumoto Y, Adams V, et al. Impact of exercise training on myostatin expression in the myocardium and skeletal muscle in a chronic heart failure model. Eur J Heart Fail. 2009;11(4):342–8. https://doi.org/10.1093/eurjhf/hfp020.

    Article  CAS  PubMed  Google Scholar 

  82. • Vest AR, Chan M, Deswal A, Givertz MM, Lekavich C, Lennie T, et al. Nutrition, Obesity, and Cachexia in Patients With Heart Failure: A Consensus Statement from the Heart Failure Society of America Scientific Statements Committee. J Card Fail. 2019;25(5):380–400. https://doi.org/10.1016/j.cardfail.2019.03.007 This article suggests an approach to the assessment of HF patients (both inpatients and outpatients) with malnutrition in combination with either cachexia and obesity and a management strategy for each cohort.

    Article  PubMed  Google Scholar 

  83. Rozentryt P, von Haehling S, Lainscak M, Nowak JU, Kalantar-Zadeh K, Polonski L, et al. The effects of a high-caloric protein-rich oral nutritional supplement in patients with chronic heart failure and cachexia on quality of life, body composition, and inflammation markers: a randomized, double-blind pilot study. J Cachexia Sarcopenia Muscle. 2010;1(1):35–42. https://doi.org/10.1007/s13539-010-0008-0.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Aquilani R, Viglio S, Iadarola P, Opasich C, Testa A, Dioguardi FS, et al. Oral amino acid supplements improve exercise capacities in elderly patients with chronic heart failure. Am J Cardiol. 2008;101(11a):104e–10e. https://doi.org/10.1016/j.amjcard.2008.03.008.

    Article  CAS  PubMed  Google Scholar 

  85. Forbes SC, Little JP, Candow DG. Exercise and nutritional interventions for improving aging muscle health. Endocrine. 2012;42(1):29–38. https://doi.org/10.1007/s12020-012-9676-1.

    Article  CAS  PubMed  Google Scholar 

  86. Gould DW, Lahart I, Carmichael AR, Koutedakis Y, Metsios GS. Cancer cachexia prevention via physical exercise: molecular mechanisms. J Cachexia Sarcopenia Muscle. 2013;4(2):111–24. https://doi.org/10.1007/s13539-012-0096-0.

    Article  PubMed  Google Scholar 

  87. Lenk K, Erbs S, Hollriegel R, Beck E, Linke A, Gielen S, et al. Exercise training leads to a reduction of elevated myostatin levels in patients with chronic heart failure. Eur J Prev Cardiol. 2012;19(3):404–11. https://doi.org/10.1177/1741826711402735.

    Article  PubMed  Google Scholar 

  88. Clark AL, Coats AJS, Krum H, Katus HA, Mohacsi P, Salekin D, et al. Effect of beta-adrenergic blockade with carvedilol on cachexia in severe chronic heart failure: results from the COPERNICUS trial. J Cachexia Sarcopenia Muscle. 2017;8(4):549–56. https://doi.org/10.1002/jcsm.12191.

    Article  PubMed  PubMed Central  Google Scholar 

  89. Anker SD, Negassa A, Coats AJ, Afzal R, Poole-Wilson PA, Cohn JN, et al. Prognostic importance of weight loss in chronic heart failure and the effect of treatment with angiotensin-converting-enzyme inhibitors: an observational study. Lancet (London, England). 2003;361(9363):1077–83. https://doi.org/10.1016/s0140-6736(03)12892-9.

    Article  CAS  Google Scholar 

  90. Khawaja T, Chokshi A, Ji R, Kato TS, Xu K, Zizola C, et al. Ventricular assist device implantation improves skeletal muscle function, oxidative capacity, and growth hormone/insulin-like growth factor-1 axis signaling in patients with advanced heart failure. J Cachexia Sarcopenia Muscle. 2014;5(4):297–305. https://doi.org/10.1007/s13539-014-0155-9.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Anker SD, Comin Colet J, Filippatos G, Willenheimer R, Dickstein K, Drexler H, et al. Ferric carboxymaltose in patients with heart failure and iron deficiency. N Engl J Med. 2009;361(25):2436–48. https://doi.org/10.1056/NEJMoa0908355.

    Article  CAS  PubMed  Google Scholar 

  92. Bauer JM, Verlaan S, Bautmans I, Brandt K, Donini LM, Maggio M, et al. Effects of a vitamin D and leucine-enriched whey protein nutritional supplement on measures of sarcopenia in older adults, the PROVIDE study: a randomized, double-blind, placebo-controlled trial. J Am Med Dir Assoc. 2015;16(9):740–7. https://doi.org/10.1016/j.jamda.2015.05.021.

    Article  PubMed  Google Scholar 

  93. Chung ES, Packer M, Lo KH, Fasanmade AA, Willerson JT. Randomized, double-blind, placebo-controlled, pilot trial of infliximab, a chimeric monoclonal antibody to tumor necrosis factor-alpha, in patients with moderate-to-severe heart failure: results of the anti-TNF therapy against congestive heart failure (ATTACH) trial. Circulation. 2003;107(25):3133–40. https://doi.org/10.1161/01.Cir.0000077913.60364.D2.

    Article  CAS  PubMed  Google Scholar 

  94. Mann DL, McMurray JJ, Packer M, Swedberg K, Borer JS, Colucci WS, et al. Targeted anticytokine therapy in patients with chronic heart failure: results of the randomized Etanercept worldwide evaluation (RENEWAL). Circulation. 2004;109(13):1594–602. https://doi.org/10.1161/01.Cir.0000124490.27666.B2.

    Article  CAS  PubMed  Google Scholar 

  95. Everett Brendan M, Cornel Jan H, Lainscak M, Anker Stefan D, Abbate A, Thuren T, et al. Anti-inflammatory therapy with Canakinumab for the prevention of hospitalization for heart failure. Circulation. 2019;139(10):1289–99. https://doi.org/10.1161/CIRCULATIONAHA.118.038010.

    Article  CAS  PubMed  Google Scholar 

  96. Caminiti G, Volterrani M, Iellamo F, Marazzi G, Massaro R, Miceli M, et al. Effect of long-acting testosterone treatment on functional exercise capacity, skeletal muscle performance, insulin resistance, and baroreflex sensitivity in elderly patients with chronic heart failure a double-blind, placebo-controlled, randomized study. J Am Coll Cardiol. 2009;54(10):919–27. https://doi.org/10.1016/j.jacc.2009.04.078.

    Article  CAS  PubMed  Google Scholar 

  97. Iellamo F, Volterrani M, Caminiti G, Karam R, Massaro R, Fini M, et al. Testosterone therapy in women with chronic heart failure: a pilot double-blind, randomized, placebo-controlled study. J Am Coll Cardiol. 2010;56(16):1310–6. https://doi.org/10.1016/j.jacc.2010.03.090.

    Article  CAS  PubMed  Google Scholar 

  98. Stout M, Tew GA, Doll H, Zwierska I, Woodroofe N, Channer KS, et al. Testosterone therapy during exercise rehabilitation in male patients with chronic heart failure who have low testosterone status: a double-blind randomized controlled feasibility study. Am Heart J. 2012;164(6):893–901. https://doi.org/10.1016/j.ahj.2012.09.016.

    Article  CAS  PubMed  Google Scholar 

  99. Dobs AS, Boccia RV, Croot CC, Gabrail NY, Dalton JT, Hancock ML, et al. Effects of enobosarm on muscle wasting and physical function in patients with cancer: a double-blind, randomised controlled phase 2 trial. Lancet Oncol. 2013;14(4):335–45. https://doi.org/10.1016/s1470-2045(13)70055-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Nagaya N, Moriya J, Yasumura Y, Uematsu M, Ono F, Shimizu W, et al. Effects of ghrelin administration on left ventricular function, exercise capacity, and muscle wasting in patients with chronic heart failure. Circulation. 2004;110(24):3674–9. https://doi.org/10.1161/01.Cir.0000149746.62908.Bb.

    Article  CAS  PubMed  Google Scholar 

  101. Katakami N, Uchino J, Yokoyama T, Naito T, Kondo M, Yamada K, et al. Anamorelin (ONO-7643) for the treatment of patients with non-small cell lung cancer and cachexia: results from a randomized, double-blind, placebo-controlled, multicenter study of Japanese patients (ONO-7643-04). Cancer. 2018;124(3):606–16. https://doi.org/10.1002/cncr.31128.

    Article  CAS  PubMed  Google Scholar 

  102. Ebner N, von Haehling S. Unlocking the wasting enigma: highlights from the 8th Cachexia conference. J Cachexia Sarcopenia Muscle. 2016;7(1):90–4. https://doi.org/10.1002/jcsm.12106.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Polkey MI, Praestgaard J, Berwick A, Franssen FME, Singh D, Steiner MC, et al. Activin type II receptor blockade for treatment of muscle depletion in chronic obstructive pulmonary disease. A randomized trial. Am J Respir Crit Care Med. 2019;199(3):313–20. https://doi.org/10.1164/rccm.201802-0286OC.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Murphy, L., Gray, A. & Joyce, E. Anabolism to Catabolism: Serologic Clues to Nutritional Status in Heart Failure. Curr Heart Fail Rep 16, 189–200 (2019). https://doi.org/10.1007/s11897-019-00437-y

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