About this Journal Submit a Manuscript Table of Contents
ISRN Hematology
Volume 2012 (2012), Article ID 246915, 9 pages
http://dx.doi.org/10.5402/2012/246915
Review Article

Anemia in Heart Failure Patients

Department of Hematology, University Hospital of Heraklion, P.O. Box 1352, 71110 Heraklion, Crete, Greece

Received 30 December 2011; Accepted 18 January 2012

Academic Editors: D. Del Principe, J. Johnston, and F. W. Quelle

Copyright © 2012 Michael G. Alexandrakis and George Tsirakis. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. M. Miniño, M. P. Heron, S. L. Murphy, and K. D. Kochanek, “Deaths: final data for 2004,” National Vital Statistics Reports, vol. 55, no. 19, pp. 1–119, 2007. View at Scopus
  2. C. D. Mathers, A. D. Lopez, and C. J. L. Murray, “The burden of disease and mortality by condition: data, methods, and results for 2001,” in Global Burden of Disease and Risk Factors, A. D. Lopez, C. D. Mathers, M. Ezzati, D. T. Jamison, and C. J. L. Murray, Eds., pp. 45–240, The World Bank and Oxford University Press, Washington, DC, USA, 2006.
  3. J. B. O'Connell and M. R. Bristow, “Economic impact of heart failure in the United States: time for a different approach,” Journal of Heart and Lung Transplantation, vol. 13, no. 4, pp. S107–S112, 1994. View at Scopus
  4. M. Packer, “The neurohormonal hypothesis: a theory to explain the mechanism of disease progression in heart failure,” Journal of the American College of Cardiology, vol. 20, no. 1, pp. 248–254, 1992. View at Scopus
  5. F. Triposkiadis, G. Karayannis, G. Giamouzis, J. Skoularigis, G. Louridas, and J. Butler, “The sympathetic nervous system in heart failure. physiology, pathophysiology, and clinical implications,” Journal of the American College of Cardiology, vol. 54, no. 19, pp. 1747–1762, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. D. S. Silverberg, D. Wexler, M. Blum, and A. Iaina, “The cardio renal anemia syndrome: correcting anemia in patients with resistant congestive heart failure can improve both cardiac and renal function and reduce hospitalizations,” Clinical Nephrology, vol. 60, no. 1, supplement 1, pp. S93–S102, 2003. View at Scopus
  7. S. Neubauer, “The failing heart - An engine out of fuel,” New England Journal of Medicine, vol. 356, no. 11, pp. 1140–1151, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. B. Blanc, C. A. Finch, L. Hallberg, et al., “Nutritional anemias,” World Health Organization Technical Report Series 405, 1968.
  9. E. Beutler and J. Waalen, “The definition of anemia: what is the lower limit of normal of the blood hemoglobin concentration?” Blood, vol. 107, no. 5, pp. 1747–1750, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. H. F. Groenveld, J. L. Januzzi, K. Damman et al., “Anemia and Mortality in Heart Failure Patients. A Systematic Review and Meta-Analysis,” Journal of the American College of Cardiology, vol. 52, no. 10, pp. 818–827, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. K. F. Adams, I. L. Piña, J. K. Ghali et al., “Prospective evaluation of the association between hemoglobin concentration and quality of life in patients with heart failure,” American Heart Journal, vol. 158, no. 6, pp. 965–971, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. Y. D. Tang and S. D. Katz, “Anemia in chronic heart failure: prevalence, etiology, clinical correlates, and treatment options,” Circulation, vol. 113, no. 20, pp. 2454–2461, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. T. B. Horwich, G. C. Fonarow, M. A. Hamilton, W. R. MacLellan, and J. Borenstein, “Anemia is associated with worse symptoms, greater impairment in functional capacity and a significant increase in mortality in patients with advanced heart failure,” Journal of the American College of Cardiology, vol. 39, no. 11, pp. 1780–1786, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. T. H. Le Jemtel and S. Arain, “Mediators of anemia in chronic heart failure,” Heart Failure Clinics, vol. 6, no. 3, pp. 289–293, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. G. L. Smith, J. H. Lichtman, M. B. Bracken et al., “Renal impairment and outcomes in heart failure. systematic review and meta-analysis,” Journal of the American College of Cardiology, vol. 47, no. 10, pp. 1987–1996, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. H. L. Hillege, A. R. J. Girbes, P. J. De Kam et al., “Renal function, neurohormonal activation, and survival in patients with chronic heart failure,” Circulation, vol. 102, no. 2, pp. 203–210, 2000. View at Scopus
  17. A. S. Go, J. Yang, L. M. Ackerson et al., “Hemoglobin level, chronic kidney disease, and the risks of death and hospitalization in adults with chronic heart failure—the anemia in chronic heart failure: Outcomes and Resource Utilization (ANCHOR) study,” Circulation, vol. 113, no. 23, pp. 2713–2723, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. J. B. Young, W. T. Abraham, N. M. Albert et al., “Relation of low hemoglobin and anemia to morbidity and mortality in patients hospitalized with heart failure (Insight from the OPTIMIZE-HF Registry),” American Journal of Cardiology, vol. 101, no. 2, pp. 223–230, 2008. View at Publisher · View at Google Scholar · View at PubMed
  19. J. C. Luthi, W. D. Flanders, M. Burnier, B. Burnand, and W. M. McClellan, “Anemia and chronic kidney disease are associated with poor outcomes in heart failure patients,” BMC Nephrology, vol. 7, article no. 3, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. D. S. Silverberg, D. Wexler, A. Iaina, and D. Schwartz, “The correction of anemia in patients with the combination of chronic kidney disease and congestive heart failure may prevent progression of both conditions,” Clinical and Experimental Nephrology, vol. 13, no. 2, pp. 101–106, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. W. H. W. Tang, W. Tong, A. Jain, G. S. Francis, C. M. Harris, and J. B. Young, “Evaluation and long-term prognosis of new-onset, transient, and persistent anemia in ambulatory patients with chronic heart failure,” Journal of the American College of Cardiology, vol. 51, no. 5, pp. 569–576, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. I. S. Anand, M. A. Kuskowski, T. S. Rector et al., “Anemia and change in hemoglobin over time related to mortality and morbidity in patients with chronic heart failure: results from Val-HeFT,” Circulation, vol. 112, no. 8, pp. 1121–1127, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. A. Sandhu, S. Soman, M. Hudson, and A. Besarab, “Managing anemia in patients with chronic heart failure: what do we know?” Vascular Health and Risk Management, vol. 6, no. 1, pp. 237–252, 2010.
  24. I. S. Anand, “Pathophysiology of anemia in heart failure,” Heart Failure Clinics, vol. 6, no. 3, pp. 279–288, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. E. O'Meara, T. Clayton, M. B. McEntegart et al., “Clinical correlates and consequences of anemia in a broad spectrum of patients with heart failure—results of the candesartan in heart failure: assessment of reduction in mortality and morbidity (CHARM) program,” Circulation, vol. 113, no. 7, pp. 986–994, 2006. View at Publisher · View at Google Scholar · View at PubMed
  26. S. Philipp, H. Ollmann, T. Schink, R. Dietz, F. Luft, and R. Willenbrock, “The impact of anaemia and kidney function in congestive heart failure and preserved systolic function,” Nephrology Dialysis Transplantation, vol. 20, no. 5, pp. 915–919, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. L. P. McMahon, K. Mason, S. L. Skinner, C. M. Burge, L. E. Grigg, and G. J. Becker, “Effects of haemoglobin normalization on quality of life and cardiovascular parameters in end-stage renal failure,” Nephrology Dialysis Transplantation, vol. 15, no. 9, pp. 1425–1430, 2000. View at Scopus
  28. B. D. Westenbrink, F. W. Visser, A. A. Voors et al., “Anaemia in chronic heart failure is not only related to impaired renal perfusion and blunted erythropoietin production, but to fluid retention as well,” European Heart Journal, vol. 28, no. 2, pp. 166–171, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. E. M. Tong and A. R. Nissenson, “Erythropoietin and anemia,” Seminars in Nephrology, vol. 21, no. 2, pp. 190–203, 2001. View at Scopus
  30. N. D. Vaziri, “Erythropoietin and transferrin metabolism in nephrotic syndrome,” American Journal of Kidney Diseases, vol. 38, no. 1, pp. 1–8, 2001. View at Scopus
  31. M. Mrug, T. Stopka, B. A. Julian, J. F. Prchal, and J. T. Prchal, “Angiotensin II stimulates proliferation of normal early erythroid progenitors,” Journal of Clinical Investigation, vol. 100, no. 9, pp. 2310–2314, 1997. View at Scopus
  32. I. S. Anand, “Anemia and Chronic Heart Failure. Implications and Treatment Options,” Journal of the American College of Cardiology, vol. 52, no. 7, pp. 501–511, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. K. E. Bernstein, H. D. Xiao, K. Frenzel et al., “Six truisms concerning ACE and the renin-angiotensin system educed from the genetic analysis of mice,” Circulation Research, vol. 96, no. 11, pp. 1135–1144, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. D. S. Silverberg, D. Wexler, A. Iaina, and D. Schwartz, “Correction of iron deficiency in the cardiorenal syndrome,” International Journal of Nephrology, vol. 2011, Article ID 365301, 8 pages, 2011. View at Publisher · View at Google Scholar · View at PubMed
  35. D. O. Okonko, A. K.J. Mandal, C. G. Missouris, and P. A. Poole-Wilson, “Disordered iron homeostasis in chronic heart failure: prevalence, predictors, and relation to anemia, exercise capacity, and survival,” Journal of the American College of Cardiology, vol. 58, no. 12, pp. 1241–1251, 2011. View at Publisher · View at Google Scholar · View at PubMed
  36. S. Stancu, A. Stanciu, A. Zugravu et al., “Bone marrow iron, iron indices, and the response to intravenous iron in patients with non-dialysis-dependent CKD,” American Journal of Kidney Diseases, vol. 55, no. 4, pp. 639–647, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. G. Weiss and L. T. Goodnough, “Anemia of chronic disease,” New England Journal of Medicine, vol. 352, no. 10, pp. 1011–1023, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. M. Testa, M. Yeh, P. Lee et al., “Circulating levels of cytokines and their endogenous modulators in patients with mild to severe congestive heart failure due to coronary artery disease or hypertension,” Journal of the American College of Cardiology, vol. 28, no. 4, pp. 964–971, 1996. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Comnick and A. Ishani, “Renal biomarkers of kidney injury in cardiorenal syndrome,” Current Heart Failure Reports, vol. 8, no. 2, pp. 99–105, 2011. View at Publisher · View at Google Scholar · View at PubMed
  40. G. Dallalio, E. Law, and R. T. Means, “Hepcidin inhibits in vitro erythroid colony formation at reduced erythropoietin concentrations,” Blood, vol. 107, no. 7, pp. 2702–2704, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. G. J. Anderson and C. D. Vulpe, “Mammalian iron transport.,” Cellular and Molecular Life Sciences, vol. 66, no. 20, pp. 3241–3261, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. C. Camaschella and A. Pagani, “Iron and erythropoiesis: a dual relationship,” International Journal of Hematology, vol. 93, no. 1, pp. 21–26, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. Y. Naito, T. Tsujino, M. Matsumoto, T. Sakoda, M. Ohyanagi, and T. Masuyama, “Adaptive response of the heart to long-term anemia induced by iron deficiency,” American Journal of Physiology, Heart and Circulatory Physiology, vol. 296, no. 3, pp. H585–H593, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. F. Dong, X. Zhang, B. Culver, H. G. Chew, R. O. Kelley, and J. Ren, “Dietary iron deficiency induces ventricular dilation, mitochondrial ultrastructural aberrations and cytochrome c release: involvement of nitric oxide synthase and protein tyrosine nitration,” Clinical Science, vol. 109, no. 3, pp. 277–286, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  45. G. Weiss, E. Meusburger, G. Radacher, K. Garimorth, U. Neyer, and G. Mayer, “Effect of iron treatment on circulating cytokine levels in ESRD patients receiving recombinant human erythropoietin,” Kidney International, vol. 64, no. 2, pp. 572–578, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. E. Nagababu, S. Gulyani, C. J. Earley, R. Cutler, M. Mattson, and J. Rifkind, “Iron-deficiency anaemia enhances red blood cell oxidative stress,” Free Radical Research, vol. 42, no. 9, pp. 824–829, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. D. Imberti, M. Giorgi Pierfranceschi, M. Falciani, and D. Prisco, “Venous thromboembolism prevention in patients with heart failure: an often neglected issue,” Pathophysiology of Haemostasis and Thrombosis, vol. 36, no. 2, pp. 69–74, 2008. View at Publisher · View at Google Scholar · View at PubMed
  48. I. Kuku, E. Kaya, S. Yologlu, R. Gokdeniz, and A. Baydin, “Platelet counts in adults with iron deficiency anemia,” Platelets, vol. 20, no. 6, pp. 401–405, 2009. View at Scopus
  49. E. Streja, C. P. Kovesdy, S. Greenland et al., “Erythropoietin, iron depletion, and relative thrombocytosis: a possible explanation for hemoglobin-survival paradox in hemodialysis,” American Journal of Kidney Diseases, vol. 52, no. 4, pp. 727–736, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. N. V. Dahl, D. H. Henry, and D. W. Coyne, “Thrombosis with erythropoietic stimulating agents - Does iron-deficient erythropoiesis play a role?” Seminars in Dialysis, vol. 21, no. 3, pp. 210–211, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. Y. Beguin, M. Loo, S. R'Zik et al., “Effect of recombinant human erythropoietin on platelets in patients with anemia of renal failure: correlation of platelet count with erythropoietic activity and iron parameters,” European Journal of Haematology, vol. 53, no. 5, pp. 265–270, 1994. View at Scopus
  52. D. O. Okonko, S. B. Marley, S. D. Anker, P. A. Poole-Wilson, and M. Y. Gordon, “Erythropoietin resistance contributes to anaemia in chronic heart failure and relates to aberrant JAK-STAT signal transduction,” International Journal of Cardiology. In press.
  53. D. O. Okonko, S. B. Marley, S. D. Anker, P. A. Poole-Wilson, and M. Y. Gordon, “Suppression of erythropoiesis in patients with chronic heart failure and anaemia of unknown origin: evidence of an immune basis,” International Journal of Cardiology. In press.
  54. U. Förstermann and T. Münzel, “Endothelial nitric oxide synthase in vascular disease: from marvel to menace,” Circulation, vol. 113, no. 13, pp. 1708–1714, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. A. Bøyum, H. B. Fjerdingstad, V. A. Tennfjord, H. B. Benestad, and D. Løvhaug, “Specific antibodies to mouse Sca-1- (Ly-6A/E) or Thy-1-positive haematopoietic progenitor cells induce formation of nitric oxide which inhibits subsequent colony formation,” European Journal of Haematology, vol. 73, no. 6, pp. 427–430, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. J. P. Maciejewski, C. Selleri, T. Sato et al., “Nitric oxide suppression of human hematopoiesis in vitro. Contribution to inhibitory action of interferon-γ and tumor necrosis factor-α,” Journal of Clinical Investigation, vol. 96, no. 2, pp. 1085–1092, 1995. View at Scopus
  57. P. O. Iversen, K. B. Andersson, A. V. Finsen et al., “Separate mechanisms cause anemia in ischemic vs. nonischemic murine heart failure,” American Journal of Physiology, Regulatory Integrative and Comparative Physiology, vol. 298, no. 3, pp. R808–R814, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. A. Zittermann, A. Jungvogel, S. Prokop et al., “Vitamin D deficiency is an independent predictor of anemia in end-stage heart failure,” Clinical Research in Cardiology, vol. 100, no. 9, pp. 781–788, 2011. View at Publisher · View at Google Scholar · View at PubMed
  59. D. Kansagara, E. Dyer, H. Englander, M. Freeman, and D. Kagen, Treatment of Anemia in Patients with Heart Disease: A Systematic Review, Department of Veterans Affairs, Washington, DC, USA, 2011.
  60. D. S. Silverberg, D. Wexler, M. Blum et al., “The use of subcutaneous erythropoietin and intravenous iron for the treatment of the anemia of severe, resistant congestive heart failure improves cardiac and renal function and functional cardiac class, and markedly reduces hospitalizations,” Journal of the American College of Cardiology, vol. 35, no. 7, pp. 1737–1744, 2000. View at Publisher · View at Google Scholar · View at Scopus
  61. D. S. Silverberg, A. Iaina, D. Wexler, and M. Blum, “The pathological consequences of anaemia,” Clinical and Laboratory Haematology, vol. 23, no. 1, pp. 1–6, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Zilberman, D. S. Silverberg, I. Bits et al., “Improvement of anemia with erythropoietin and intravenous iron reduces sleep-related breathing disorders and improves daytime sleepiness in anemic patients with congestive heart failure,” American Heart Journal, vol. 154, no. 5, pp. 870–876, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. D. S. Silverberg, D. Wexler, M. Blum et al., “Effects of treatment with epoetin beta on outcomes in patients with anaemia and chronic heart failure,” Kidney and Blood Pressure Research, vol. 28, no. 1, pp. 41–47, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. J. M. O. Arnold, J. G. Howlett, P. Dorian et al., “Canadian Cardiovascular Society Consensus Conference recommendations on heart failure update 2007: prevention, management during intercurrent illness or acute decompensation, and use of biomarkers,” Canadian Journal of Cardiology, vol. 23, no. 1, pp. 21–45, 2007. View at Scopus
  65. S. V. Rao, J. G. Jollis, R. A. Harrington et al., “Relationship of blood transfusion and clinical outcomes in patients with acute coronary syndromes,” Journal of the American Medical Association, vol. 292, no. 13, pp. 1555–1562, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  66. J. E. Toblli, A. Lombraña, P. Duarte, and F. Di Gennaro, “Intravenous iron reduces nt-pro-brain natriuretic peptide in anemic patients with chronic heart failure and renal insufficiency,” Journal of the American College of Cardiology, vol. 50, no. 17, pp. 1657–1665, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  67. S. D. Anker, J. C. Colet, G. Filippatos et al., “Rationale and design of Ferinject assessment in patients with IRon deficiency and chronic Heart Failure (FAIR-HF) study: a randomized, placebo-controlled study of intravenous iron supplementation in patients with and without anaemia,” European Journal of Heart Failure, vol. 11, no. 11, pp. 1084–1091, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  68. R. Gaber, N. A. Kotb, M. Ghazy, H. M. Nagy, M. Salama, and A. Elhendy, “Tissue doppler and strain rate imaging detect improvement of myocardial function in iron deficient patients with congestive heart failure after iron replacement therapy,” Echocardiography, vol. 29, no. 1, pp. 13–18, 2012.
  69. J. González-Costello and J. Comín-Colet, “Iron deficiency and anaemia in heart failure: understanding the FAIR-HF trial,” European Journal of Heart Failure, vol. 12, no. 11, pp. 1159–1162, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  70. S. D. Anker, J. C. Colet, G. Filippatos et al., “Ferric carboxymaltose in patients with heart failure and iron deficiency,” New England Journal of Medicine, vol. 361, no. 25, pp. 2436–2448, 2009. View at Publisher · View at Google Scholar · View at PubMed
  71. D. O. Okonko, A. Grzeslo, T. Witkowski et al., “Effect of intravenous iron sucrose on exercise tolerance in anemic and nonanemic patients with symptomatic chronic heart failure and iron deficiency. FERRIC-HF: a randomized, controlled, observer-blinded trial,” Journal of the American College of Cardiology, vol. 51, no. 2, pp. 103–112, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  72. A. P. Bolger, F. R. Bartlett, H. S. Penston et al., “Intravenous iron alone for the treatment of anemia in patients with chronic heart failure,” Journal of the American College of Cardiology, vol. 48, no. 6, pp. 1225–1227, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  73. R. I. Usmanov, E. B. Zueva, D. S. Silverberg, and M. Shaked, “Intravenous iron without erythropoietin for the treatment of iron deficiency anemia in patients with moderate to severe congestive heart failure and chronic kidney insufficiency,” Journal of Nephrology, vol. 21, no. 2, pp. 236–242, 2008. View at Scopus
  74. S. G. Drakos, M. I. Anastasiou-nana, K. G. Malliaras, and J. N. Nanas, “Anemia in chronic heart failure,” Congestive Heart Failure, vol. 15, no. 2, pp. 87–92, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  75. A. Palazzuoli, D. Silverberg, F. Iovine et al., “Erythropoietin improves anemia exercise tolerance and renal function and reduces B-type natriuretic peptide and hospitalization in patients with heart failure and anemia,” American Heart Journal, vol. 152, no. 6, pp. 1096–e9, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  76. A. Palazzuoli, D. S. Silverberg, F. Iovine et al., “Effects of β-erythropoietin treatment on left ventricular remodeling, systolic function, and B-type natriuretic peptide levels in patients with the cardiorenal anemia syndrome,” American Heart Journal, vol. 154, no. 4, pp. 645–e9, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  77. B. P. Geisler, “Treating anemia in heart failure patients: a review of erythropoiesis- stimulating agents,” Expert Opinion on Biological Therapy, vol. 10, no. 8, pp. 1209–1216, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  78. C. J. Parsa, A. Matsumoto, J. Kim et al., “A novel protective effect of erythropoietin in the infarcted heart,” Journal of Clinical Investigation, vol. 112, no. 7, pp. 999–1007, 2003. View at Publisher · View at Google Scholar · View at Scopus
  79. D. Hefer, T. Yi, D. E. Selby et al., “Erythropoietin induces positive inotropic and lusitropic effects in murine and human myocardium,” Journal of Molecular and Cellular Cardiology, vol. 52, no. 1, pp. 256–263, 2012. View at Publisher · View at Google Scholar · View at PubMed
  80. D. S. Silverberg, “The role of erythropoiesis stimulating agents and intravenous (IV) iron in the cardio renal anemia syndrome,” Heart Failure Reviews, vol. 16, no. 6, pp. 609–614, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  81. J. S. Marques, “Perspectives for the treatment of anemia in heart failure: is there a role for vasopressin antagonists?” Congestive Heart Failure, vol. 18, no. 1, pp. 1–3, 2012.