Clinical Reviews in Allergy & Immunology

, Volume 52, Issue 3, pp 323–332 | Cite as

Cardiac Impairment in Rheumatoid Arthritis and Influence of Anti-TNFα Treatment

Article
First Online:

Abstract

There is evidence that rheumatoid arthritis (RA) is associated with higher overall and cardiovascular (CV) morbidity and mortality as compared with general population. Increased prevalence of traditional risk factors and chronic inflammation, that has been recognized as independent CV risk factor, may play an important role in atherosclerosis and subsequently ischemic heart disease development. However, myocardial dysfunction as a result of chronic inflammation and secondarily myocardial fibrosis markedly participates on heart failure development. Proinflammatory cytokines, such as C-reactive protein, tumor necrosis factor alpha (TNFα), interleukins 1 and 6, that are markedly increased in RA, play a role in the acceleration of atherosclerosis as well as myocardial fibrosis development. Several studies documented that increased CV risk was associated with seropositivity, disease activity score, citrullination, and duration of RA. Early detection of heart dysfunction is based on echocardiographic detection of diastolic dysfunction resulting from myocardial inflammation and fibrosis. Some studies showed also higher prevalence of left ventricular systolic dysfunction and increased prevalence of cardiac arrhythmias as compared to non-RA population. There are still controversies on the impact of NT-proBNP in predicting cardiac impairment in RA patients. Some authors consider it to be a sensitive noninvasive predictor of subclinical CV disease in these patients and also a predictor of all-cause mortality independently on traditional CV risk factors. However, the correlation with parameters of cardiac function was confirmed only in a few studies. The impact of biological treatment on progression of atherosclerosis and heart failure is still controversial and seems to be not harmful in young patients with normal left ventricular function. The effect of biologics, especially anti-TNFα drugs, is probably related to the cardiac function before treatment. Larger prospective clinical, echocardiographic, and magnetic resonance studies are needed.

Keywords

Rheumatoid arthritis Atherosclerosis Heart failure Anti-TNFα treatment NT-proBNP 
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Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Alamanos Y, Drosos AA (2005) Epidemiology of adult rheumatoid arthritis. Autoimmun Rev 4(3):130–136CrossRefPubMedGoogle Scholar
  2. 2.
    Norton S, Sacker A, Dixey J, Done J, Williams P, Young A (2013) Early rheumatoid arthritis study. Trajectories of functional limitation in early rheumatoid arthritis and their association with mortality. Rheumatology (Oxford) 52(11):2016–2024CrossRefGoogle Scholar
  3. 3.
    Schuett KA, Lehrke M, Marx N, Burgmaier M (2015) High risk cardiovascular patients: clinical features, comorbidities and interconnecting mechanisms. Front Immunol 6:1–9CrossRefGoogle Scholar
  4. 4.
    Young A, Koduri G, Batley M, Kulinskaya E, Gough A, Norton S et al (2007) Mortality in rheumatoid arthritis. Increased in the early course of disease, in ischaemic heart disease and in pulmonary fibrosis. Rheumatol (Oxford) 46(2):350–357CrossRefGoogle Scholar
  5. 5.
    Wallberg-Johnsson S, Ohman ML, Dahlqvist SR (1997) Cardiovascular morbidity and mortality in patients with seropositive rheumatoid arthritis in northern Sweden. J Rheumatol 24:445–451Google Scholar
  6. 6.
    Ajeganova S, Humphreys JH, Verheul MK, van Steenbergen HW, van Nies JA, Hafstrom I et al. (2016) Anticitrullinated protein antibodies and rheumatoid factor are associated with increased mortality but different cause of death in patients with rheumatoid arthritis: a longitudinal study in three European cohort. Ann Rheum Dis. doi:  10.1136/annrheumdis-2015-208579.
  7. 7.
    Crepaldi G, Scire CA, Carrara G, Sakellariou G, Caporali R, Hmamouchi I et al (2016) Cardiovascular comorbidities relate more than others with disease activity in rheumatoid arthritis. PLoS One 11(1):e0146991. doi: 10.1371/journal.pone.0146991 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Innala L, Sjoberg C, Moller B, Ljung L, Smedby T, Sodergren A et al (2016) Co-morbidity in patients with early rheumatoid arthritis-inflammation matters. Arthritis Res Ther 18(1):33. doi: 10.1186/s13075-016-0928-y CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Maradit-Kremers H, Nicola PJ, Crowson CS, Ballman KV, Gabriel SE (2004) Prognostic importance of low body mass index in relation to cardiovascular mortality in rheumatoid arthritis. Arthritis Rheumatism 50:3450–3456CrossRefGoogle Scholar
  10. 10.
    Maradit-Kremers H, Crowson CS, Nicola PJ, Ballman KV, Roger VL, Jacobsen SJ, Gabriel SE (2005) Increased unrecognized coronary heart disease and sudden death in rheumatoid arthritis. Arthritis Rheum 52:402–410CrossRefPubMedGoogle Scholar
  11. 11.
    Kobayashi H, Giles JT, Polak JF, Blumenthal RS, Leffell MS, Szklo M et al (2010) Increased prevalence of carotid artery atherosclerosis in rheumatoid arthritis is artery specific. J Rheumatol 37:730–739CrossRefPubMedGoogle Scholar
  12. 12.
    Giles JT, Fernandes V, Lima JAC, Bathon JM (2005) Myocardial dysfunction in rheumatoid arthritis: epidemiology and pathogenesis. Arthritis Res Ther 7:195–207CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Ntusi NA, Piechnik SK, Francis JM, Ferreira VM, Matthews PM, Robson MD et al (2015) Diffuse myocardial fibrosis and inflammation in rheumatoid arthritis: insights from CMR T1 mapping. JACC Cardiovasc Imaging 8(5):526–536CrossRefPubMedGoogle Scholar
  14. 14.
    Rodriguez-Rodriguez L, Lopez-Mejias R, Fernandez-Gutierez B, Balsa A, Gonzales-Gay MA, Martin J (2015) Rheumatoid arthritis: genetic variants as biomarkers of cardiovascular disease. Curr Pharm Des 21(2):182–201CrossRefPubMedGoogle Scholar
  15. 15.
    Kumar N, Marshall NJ, Hammal DM, Pearce MS, Parker L, Furniss SS et al (2007) Causes of death in patients with rheumatoid arthritis: comparison with siblings and matched osteoarthritis controls. J Rheumatol 34:1695–1698PubMedGoogle Scholar
  16. 16.
    Wolfe F, Michaud K (2004) Heart failure in rheumatoid arthritis: rates, predictors and the effects of anti tumor necrosis factor therapy. Am J Med 116:305–311CrossRefPubMedGoogle Scholar
  17. 17.
    McCoy SS, Crowson CS, Maradit-Kremers H, Therneau TM, Roger V, Matteson EL, Gabriel SE (2013) Long-term outcomes and treatment after myocardial infarction in patients with rheumatoid arthritis. J Rheumatol 40(5):605–610. doi: 10.3899/jrheum.120941 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Rostom S, Mengat M, Lahlou R, Hari A, Bahim R, Hassouni NH (2013) Metabolic syndrome in rheumatoid arthritis: case control study. BMC Musculosceletal Dis 14:147CrossRefGoogle Scholar
  19. 19.
    Parra-Salcedo F, Contreras-Yáñez I, Elías-López D, Aguilar-Salinas CA, Pascual-Ramos V (2015) Prevalence, incidence and characteristics of the metabolic syndrome (MetS) in a cohort of Mexican Mestizo early rheumatoid arthritis patients treated with conventional disease modifying anti-rheumatic drugs: the complex relationship between MetS and disease activity. Arthritis Res Ther 17:34. doi: 10.1186/s13075-015-0549-x CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Lee SH, Choi H, Cho BL, An AR, Seo YG, Jin HS et al (2016) Relationship between metabolic syndrome and rheumatoid arthritis. Korean J Fam Med 37(1):44–50. doi: 10.4082/kjfm.2016.37.1.44 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Zhang J, Fu L, Shi J, Chen X, Li Y, Ma B, Zhang Y (2013) The risk of metabolic syndrome in patients with rheumatoid arthritis: a meta-analysis of observational studies. PLoS One 8(10):e78151. doi: 10.1371/journal.pone.0078151 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Jiang P, Li H, Li X (2015) Diabetes mellitus risk factors in rheumatoid arthritis: a systematic review and meta-analysis. Clin Exp Rheumatol 33:115–121PubMedGoogle Scholar
  23. 23.
    Lu MC, Yan ST, Yin WY, Koo M, Lai NS (2014) Risk of rheumatoid arthritis in patients with type 2 diabetes: a nationwide population-based case-control study. PLoS One 9(7):e101528. doi: 10.1371/journal.pone.0101528 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Ursini F, Russo E, D’Angelo S, Arturi F, Hribal ML, D’Antona L et al (2016) Prevalence of undiagnosed diabetes in rheumatoid arthritis: an OGTT study. Medicine (Baltimore) 95(7):e2552. doi: 10.1097/MD.0000000000002552 CrossRefGoogle Scholar
  25. 25.
    Baghdadi LR, Woodman RJ, Shanahan EM, Mangoni AA (2015) The impact of traditional cardiovascular risk factors on cardiovascular outcomes in patients with rheumatoid arthritis: a systematic review and meta-analysis. PLoS One 10(2):e0117952. doi: 10.1371/journal.pone.0117952 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Gabriel SE, Crowson CS, O’Fallon WM (1999) Comorbidity in arthritis. J Rheumatol 26:2475–2479PubMedGoogle Scholar
  27. 27.
    Dessein PH, Stanwix AE, Joffe BI (2002) Cardiovascular risk in rheumatoid arthritis versus osteoarthritis: acute phase response related decreased insulin sensitivity and high-density lipoprotein cholesterol as well as clustering of metabolic syndrome features in rheumatoid arthritis. Arthritis Res 4(5):R5CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Solomon DH, Karlson EW, Rimm EB, Cannuscio CC, Mandl LA, Manson JE et al (2003) Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation 107(9):1303–1309CrossRefPubMedGoogle Scholar
  29. 29.
    Yang X, Gao F, Liu Y (2015) Association of homocysteine with immunological-inflammatory and metabolic laboratory markers and factors in relation to hyperhomocysteinaemia in rheumatoid arthritis. Clin Exp Rheumatol 33(6):900–903PubMedGoogle Scholar
  30. 30.
    Hamamoto K, Yamada S, Yasumoto M, Yoda M, Yoda K, Tsuda A et al (2016) Association of nocturnal hypertension with disease activity in rheumatoid arthritis. Am J Hypertens 29(3):340–347. doi: 10.1093/ajh/hpv119 PubMedGoogle Scholar
  31. 31.
    Zhao Q, Hong D, Zhang Y, Sang Y, Yang Z, Zhang X (2015) Association between anti-TNF therapy for rheumatoid arthritis and hypertension: a meta-analysis of randomized controlled trials. Medicine (Baltimore) 94(14):e731. doi: 10.1097/MD.0000000000000731 CrossRefGoogle Scholar
  32. 32.
    Jonsson SW, Backman C, Johnson O, Karp K, Lundstrom E, Sundqvist KG, Dahlqvist SR (2011) Increased prevalence of atherosclerosis in patients with medium term rheumatoid arthritis. J Rheumatol 28:2597–2602Google Scholar
  33. 33.
    Sakai R, Hirano F, Kihara M, Yokoyama W, Yamazaki H, Harada S et al (2015) High prevalence of cardiovascular comorbidities in patients with rheumatoid arthritis from a population-based cross-sectional study of a Japanese health insurance database. Mod Rheumatol 14:1–7Google Scholar
  34. 34.
    Myasoedova E, Gabriel SE, Green AB, Matteson EL, Crowson CS (2013) Impact of statin use on lipid levels in statin-naive patients with rheumatoid arthritis versus non-rheumatoid arthritis subjects: results from a population-based study. Arthritis Care Res (Hoboken) 65(10):1592–1599Google Scholar
  35. 35.
    Provan SA, Semb AG, Hisdal J, Stranden E, Aqewall S, Dagfinud H et al (2011) Remission is the goal for cardiovascular risk management in patients with rheumatoid arthritis: a cross-sectional comparative study. Ann Rheum Dis 70:812–817CrossRefPubMedGoogle Scholar
  36. 36.
    Hurt-Camejo E, Paredes S, Masana L, Camejo G, Sartipy P, Rosengren B et al (2001) Elevated levels of small, low-density lipoprotein with high affinity for arterial matrix components in patients with rheumatoid arthritis: possible contribution of phospholipase A2 to this atherogenic profile. Arthritis Rheum 44:2761–2767CrossRefPubMedGoogle Scholar
  37. 37.
    Chavan VU, Ramavataram D, Patel PA, Rupani MP (2015) Evaluation of serum magnesium, lipid profile and various biochemical parameters as risk factors of cardiovascular diseases in patients with rheumatoid arthritis. J Clin Diagn Res 9(4):BC01–BC05PubMedPubMedCentralGoogle Scholar
  38. 38.
    Liao KP, Liu J, Lu B, Solomon DH, Kim SC (2015) Association between lipid levels and major adverse cardiovascular events in rheumatoid arthritis compared to non-rheumatoid arthritis patients. Arthritis Rheumatol 67(8):2004–2010CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Södergren A, Karp K, Bengtsson C, Möller B, Rantapää-Dahlqvist S, Wållberg-Jonsson S (2015) The extent of subclinical atherosclerosis is partially predicted by the inflammatory load: a prospective study over 5 years in patients with rheumatoid arthritis and matched controls. J Rheumatol 42(6):935–942CrossRefPubMedGoogle Scholar
  40. 40.
    Ahmed A, Hollan I, Curran SA, Kitson SM, Riggio MP, Mikkelsen K et al. (2016) Rheumatoid arthritis patients have a pro-atherogenic cytokine microenvironment in the aortic adventitia. Arthritis Rheumatol. doi:  10.1002/art.39574
  41. 41.
    del Rincón I, Polak JF, O’Leary DH, Battafarano DF, Erikson JM, Restrepo JF et al (2015) Systemic inflammation and cardiovascular risk factors predict rapid progression of atherosclerosis in rheumatoid arthritis. Ann Rheum Dis 74(6):1118–1123CrossRefPubMedGoogle Scholar
  42. 42.
    Kuo D, Crowson CS, Gabriel SE, Matteson EL (2014) Hyperuricemia and incident cardiovascular disease and noncardiac vascular events in patients with rheumatoid arthritis. Int J Rheumatol 2014:523897. doi: 10.1155/2014/523897 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Maijer KI, Neumann E, Müller-Lander U, Drop DACAD, Ramwadhdoeve TH, Choi IYK et al (2015) Serum Vaspin levels are associated with the development of clinically manifest arthritis in autoantibody-positive individuals. PLoS One 10(12):e0144932CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Nicola PJ, Crowson CS, Maradit-Kremers H, Ballman KV, Roger VL, Jacobsen SJ, Gabriel SE (2006) Contribution of congestive heart failure and ischemic heart disease to excess mortality in rheumatoid arthritis. Arthritis Rheum 54(1):60–67CrossRefPubMedGoogle Scholar
  45. 45.
    Nicola PJ, Maradit-Kremers H, Roger VL, Jacobsen SJ, Crowson CS, Ballman KV, Gabriel SE (2005) The risk of congestive heart failure in rheumatoid arthritis: a population-based study over 46 years. Arthritis Rheum 52(2):412–420CrossRefPubMedGoogle Scholar
  46. 46.
    Schau T, Gottwald M, Arbach O, Seifert M, Schopp M, Neuss M et al (2015) Increased prevalence of diastolic heart failure in patients with rheumatoid arthritis correlates with active disease, but not with treatment type. J Rheumatol 42:2029–2037CrossRefPubMedGoogle Scholar
  47. 47.
    Guedes C, Bianchi-Fior P, Cormier B, Barthelemy B, Rat AC, Boissier MC (2001) Cardiac manifestation of rheumatoid arthritis: a case-control transesophageal echocardiography study in 30 patients. Arthritis Rheum 45(2):129–135CrossRefPubMedGoogle Scholar
  48. 48.
    Myasoedova E, Crowson CS, Nicola PJ, Maradit-Kremers H, Davis JM 3rd, Roger VL et al (2011) The influence of rheumatoid arthritis disease characteristics on heart failure. J Rheumatol 38(8):1601–1606CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Listing J, Strangfeld A, Kekow J, Schneider M, Kapelle A, Wassenberg S, Zink A (2008) Does tumor necrosis factor-α inhibition promote or prevent heart failure in patients with rheumatoid arthritis? Arthritis Rheum 58:667–677CrossRefPubMedGoogle Scholar
  50. 50.
    Sarzi-Puttini P, Atzueni F, Doria A, Iaccarino L, Turiel M (2005) Tumor necrosis factor-alpha, biologic agents and cardiovascular risk. Lupus 14(9):780–784CrossRefPubMedGoogle Scholar
  51. 51.
    Roldan AC, DeLong C, Qualls CR, Crawford MC (2007) Characterization of valvular heart disease in rheumatoid arthritis by transesophageal echocardiography and clinical correlates. Am J Cardiol 100:496–502CrossRefPubMedGoogle Scholar
  52. 52.
    Giles JT, Fert-Bober J, Park JK, Bingham CO 3rd, Andrade F, Fox-Talbot K et al (2012) Myocardial citrullination in rheumatoid arthritis: a correlative histopathologic study. Arthritis Res Ther 14:R39CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Di Franco M, Paradiso M, Mammarella A, Paoletti V, Labbadia G, Coppotelli L et al (2000) Diastolic function abnormalities in rheumatoid arthritis. Evaluation by echo Doppler transmitral flow and pulmonary venous flow: relation with duration of disease. Ann Rheum Dis 59:227–229CrossRefPubMedGoogle Scholar
  54. 54.
    Liang KP, Myasoedova E, Crowson CS, Davis JM, Roger VL, Karon BL et al (2010) Increased prevalence of diastolic dysfunction in rheumatoid arthritis. Ann Rheum Dis 69(9):1665–1670CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Tomáš L, Lazúrová I, Oetterová M, Pundová L, Petrášová D, Studenčan M (2013) Left ventricular morphology and function in patients with rheumatoid arthritis. Wien Klin Wochenschr 125(9-10):233–238CrossRefPubMedGoogle Scholar
  56. 56.
    Sakthiswary R, Das S (2015) Predictors of diastolic dysfunction in rheumatoid arthritis. Saudi Med J 36(5):525–529CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Bhatia GS, Sosin MD, Patel JV, Grindulis KA, Khattak FH, Huighes EA et al (2006) Left ventricular systolic dysfunction in rheumatoid disease. An unrecognized burden? J Am Coll Cardiol 47:1169–1174CrossRefPubMedGoogle Scholar
  58. 58.
    Cioffi G, Viapiana O, Ognibeni F, Dalbeni A, Gatti D, Adami S et al (2015) Prevalence and factors related to left ventricular systolic dysfunction in asymptomatic patients with rheumatoid arthritis. A prospective tissue Doppler echocardiography study. Herz 40(7):989–996CrossRefPubMedGoogle Scholar
  59. 59.
    Lazzerini PE, Capecchi PL, Acampa M, Galeazzi M, Laghi-Pasini F (2014) Arrhythmic risk in rheumatoid arthritis: the driving role of systemic inflammation. Autoimmun Rev 13(9):936–944CrossRefPubMedGoogle Scholar
  60. 60.
    Lindhardsen J, Ahlehoff O, Gislason GH, Madsen OR, Olesen JB, Svendsen JH et al (2012) Risk of atrial fibrillation and stroke in rheumatoid arthritis: Danish nationwide cohort study. BMJ 344:e1257CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Solus J, Chung CP, Oeser A, Avalos I, Gebretsadik T, Shintani A et al (2008) Amino-terminal fragment of the prohormone brain-type natriuretic peptide in rheumatoid arthritis. Arthritis Rheum 58:2662–2669CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Yxfeldt A, Wallberg-Jonsson S, Hultdin J, Rantapää-Dahlqvist S (2003) Homocysteine in patients with rheumatoid arthritis in relation to inflammation and B-vitamin treatment. Scand J Rheumatol 32:205–210CrossRefPubMedGoogle Scholar
  63. 63.
    Bozkurt B, Mann DL, Deswal A (2009) Biomarkers of inflammation in heart failure. Heart Fail Rev 15(4):331–341CrossRefGoogle Scholar
  64. 64.
    Rauchhaus M, Doehner W, Francis DP, Davos C, Kemp M, Liebenthal C et al (2000) Plasma cytokine parameters and mortality in patients with chronic heart failure. Circulation 102(25):3060–3067CrossRefPubMedGoogle Scholar
  65. 65.
    Deswal A, Petersen NJ, Feldman AM, Young JB, White BG, Mann DL (2001) Cytokines and cytokine receptors in advanced heart failure: an analysis of the cytokine database from the Vesnarinone trial (VEST). Circulation 103(16):2055–2059CrossRefPubMedGoogle Scholar
  66. 66.
    Bozkurt B, Torre-Amione G, Smith Warren M, Soran OZ, Feldman AM, Mann DL (2001) Results of targeted anti-tumor necrosis factor therapy with etanercept (ENBREL) in patients with advanced heart failure. Am J Assoc 103:1044–1047Google Scholar
  67. 67.
    Chung ES, Packer M, Lo KH, Fasanmade AA, Willerson JT, Anti-TNF Therapy Against Congestive Heart Failure Investigators (2003) 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 107:3133–3140CrossRefPubMedGoogle Scholar
  68. 68.
    Coletta AP, Clark AL, Banarjee P, Cleland JG (2002) Clinical trials update: RENEWAL (RENAISSANCE and RECOVER) and ATTACH. Eur J Heart Fail 4:243–247CrossRefGoogle Scholar
  69. 69.
    Gabriel SE (2008) Tumor necrosis factor inhibition: a part of the Solution or a part of the problem of heart failure in rheumatoid arthritis. Arthritis Rheum 58:637–640CrossRefPubMedGoogle Scholar
  70. 70.
    Khanna D, McMahon M, Furst DE (2004) Anti tumor necrosis factor-α therapy and heart failure. Arthritis Rheum 50:1040–1048CrossRefPubMedGoogle Scholar
  71. 71.
    Kotyla PJ, Owczarek A, Rakoczy J, Lewicki M, Kucharz EJ, Emery P (2012) Infliximab treatment increases left ventricular ejection fraction in patients with rheumatoid arthritis: assessment of heart function by echocardiography, endothelin-1, interleukin 6 and NT-probrain natriuretic peptide. J Rheumatol 39:4701–4706CrossRefGoogle Scholar
  72. 72.
    Tomáš L, Lazúrová I, Pundová L, Oetterová M, Zakuciová M, Petrášová D, Studenčan M (2013) Acute and long-term effect of infliximab on humoral and echocardiographic parameters in patients with chronic inflammatory diseases. Clin Rheumatol 32(1):61–66CrossRefPubMedGoogle Scholar
  73. 73.
    Curtis JR, Kramer JM, Martin C, Saag KG, Patkar N, Shatin D et al (2007) Heart failure among younger rheumatoid arthritis and Crohn’s patients exposed to TNF-α antagonists. Rheumatol 46:1688–1693CrossRefGoogle Scholar
  74. 74.
    Al-Aly Z, Pan H, Zeringue A, Xian H, McDonald JR, El-Achkar TM, Eisen S (2011) Tumor necrosis factor-α blockade, cardiovascular outcomes, and survival in rheumatoid arthritis. Transl Res 157:10–16CrossRefPubMedGoogle Scholar
  75. 75.
    Santos RC, Figueiredo VN, Martinz LC, Haro Moraes C, Quinaglia T, Boer-Martins L et al (2012) Infliximab reduces cardiac output in rheumatoid arthritis patients without heart failure. Rev Assoc Med Bras 58:698–702CrossRefPubMedGoogle Scholar
  76. 76.
    Peters MJ, Welsh P, McInnes IB, Wolbink G, Dijkmans BA, Sattar N, Nurmohamed MT (2010) Tumour necrosis factor alpha blockade reduces circulating N-terminal pro-brain natriuretic peptide levels in patients with active rheumatoid arthritis: results from a prospective cohort study. Ann Rheum Dis 69(7):1281–1285CrossRefPubMedGoogle Scholar
  77. 77.
    Setoguchi S, Schneeweiss S, Avorn J, Katz JN, Weinblatt M, Levin R et al (2008) Tumor necrosis factor-α antagonist use and heart failure in elderly patients with rheumatoid arthritis. Am Heart J 156:336–341CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Solomon DH, Rassen JA, Kuriva B, Chen L, Harrold LR, Graham DJ et al (2013) Heart failure risk among patients with rheumatoid arthritis starting a TNF antagonist. Ann Rheum Dis 72:1813–1818CrossRefPubMedGoogle Scholar
  79. 79.
    Singh JA, Wells GA, Christensen R, Tanjong Ghogomu E, Maxwell L, Macdonald JK et al (2011) Adverse effects of biologics: a network meta-analysis and Cochrane overview. Cochrane Database Syst Rev 16(2):CD008794Google Scholar
  80. 80.
    Suzuki A, Tamamura T, Okai T (2014) Five-year administration of tocilizumab to a patient with rheumatoid arthritis complicated by severe chronic heart failure. Jpn J Clin Immunol 37(6):488–492CrossRefGoogle Scholar
  81. 81.
    Kobayashi Y, Kobayashi H, Giles JT, Hirano M, Nakajima Y, Takei M (2015) Association of tocilizumab with changes in measures of regional left ventricular function in rheumatoid arthritis, as assessed by cardiac magnetic resonance imaging. Int J Rheum Dis. doi:  10.1111/1756-185X.12632
  82. 82.
    Ikonomidis I, Lekakis JP, Nikolaou M, Paraskevaidis I, Andreadou I, Kaplanoglou T et al (2008) Inhibition of interleukin-1 by anakinra improves vascular and left ventricular function in patients with rheumatoid arthritis. Circulation 117:2662–2669CrossRefPubMedGoogle Scholar
  83. 83.
    Ikonomidis I, Tzortzis S, Lekakis J, Paraskevaidis I, Andreadou I, Nikolaou M et al (2009) Lowering interleukin-1 activity with anakinra improves myocardial deformation in rheumatoid arthritis. Heart 95:1502–1507CrossRefPubMedGoogle Scholar
  84. 84.
    Ikonomidis I, Tzortzis S, Andreadou I, Paraskevaidis I, Katseli C, Katsimbri P et al (2014) Increased benefit of Interleukin -1 inhibition on vascular function, myocardial deformation and twisting in patients with coronary artery disease and coexisting rheumatoid arthritis. Circ Cardiovasc Imaging 7:619–628CrossRefPubMedGoogle Scholar
  85. 85.
    Fleischamnn RM, Schechtman J, Bennett R, Handel ML, Burmester GR, Tesser J et al (2003) Anakinra, a recombinant human interleukin-1 receptor antagonist, (r-metHuIL-1ra) in patients with rheumatoid arthritis. Arthritis Rheumatism 48:927–934CrossRefGoogle Scholar
  86. 86.
    Abbate A, Van Tassel BW, Biondi-Zoccai G, Kontos MC, Grizzard JD, Spilmann DW et al (2013) Effects of Interleukin-1 blockade with anakinra on adverse cardiac remodeling and heart failure after acute myocardial infarction (from the Virginia commonwealth University-Anakinra remodeling Trial (2)(VCU-ART2) pilot study). J Cardiol 111:1394–1400CrossRefGoogle Scholar

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© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.1st Department od Internal Medicine, Faculty of MedicinePavol Jozef Šafárik University in KošiceKošiceSlovakia

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