Towards the Clinical Management of Cardiac Involvement in Systemic Inflammatory Conditions—a Central Role for CMR

  • Lea Winau
  • Eike Nagel
  • Eva Herrmann
  • Valentina O. PuntmannEmail author
Cardiac Magnetic Resonance (V Puntmann and E Nagel, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Cardiac Magnetic Resonance


Purpose of Review

Anti-inflammatory therapies in systemic inflammatory diseases (SID) improve disease-associated disability and may also reduce cardiovascular events. Further optimization of treatment to directly target the inflammation affecting the cardiovascular system represents a potential goal of contemporary treatment. Yet, lack of non-invasive means to detect cardiovascular involvement and to monitor the response to treatment limit such advancements. This is also reflected in the recent 2017 ESC position paper on clinical management of cardiac involvement in SIDs, whose recommendations continue to rely on insensitive, radiation-heavy and invasive diagnostic methods. Absence of evidence and the context of a life-long chronic disease, necessitating ongoing monitoring and serial assessments, puts such recommendations in question. The growing evidence-base for the performance of cardiovascular magnetic resonance (CMR) in patients with SID, and especially of T1 and T2 mapping, offers a viable pathway towards identification of cardiovascular involvement and may potentially guide cardiovascular-specific therapies.

Recent Findings

In this review, we appraise the current evidence for the role of CMR in management of cardiac involvement patients with SID.


We propose an interdisciplinary framework with a central role for CMR to support the clinical management of cardiac involvement in SID patients.


Cardiovascular magnetic resonance Systemic inflammatory diseases Rheumatoid arthritis Systemic lupus erythematosus Cardiac sarcoidosis Non-ischaemic cardiomyopathy T1 mapping T2 mapping 


Compliance with Ethical Standards

Conflict of Interest

All authors declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.


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

  1. 1.
    Knockaert DC. Cardiac involvement in systemic inflammatory diseases. Eur Heart J. 2007;28(15):1797–804.CrossRefPubMedGoogle Scholar
  2. 2.
    Hamdulay SS, Mason JC. Disease-modifying anti-rheumatic drugs: do they reduce cardiac complications of RA? Heart. 2009;95(18):1471–2.CrossRefPubMedGoogle Scholar
  3. 3.
    Urowitz MB, Gladman DD, Tom BDM, Ibañez D, Farewell VT. Changing patterns in mortality and disease outcomes for patients with systemic lupus erythematosus. J Rheumatol. 2008;35(11):2152–8.CrossRefPubMedGoogle Scholar
  4. 4.
    Douglas KMJ. Excess recurrent cardiac events in rheumatoid arthritis patients with acute coronary syndrome. Ann Rheum Dis. 2006;65(3):348–53.CrossRefPubMedGoogle Scholar
  5. 5.
    Bengtsson C, Ohman ML, Nived O, Dahlqvist SR. Cardiovascular event in systemic lupus erythematosus in northern Sweden: incidence and predictors in a 7-year follow-up study. Lupus. 2012 Mar 16;21(4):452–9.CrossRefPubMedGoogle Scholar
  6. 6.
    • Caforio ALP, Adler Y, Agostini C, Allanore Y, Anastasakis A, Arad M, et al. Diagnosis and management of myocardial involvement in systemic immune-mediated diseases: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Disease. Eur Heart J. 2017;38(35):2649–62. The latest ESC position paper on myocarditis focuses on the role of biopsy in the diagnosis of myocardial inflammation rather than including CMR as a valid method in diagnosis and prognosis. Furthermore, it lacks several recent CMR studies. CrossRefPubMedGoogle Scholar
  7. 7.
    Mavrogeni SI, Kitas GD, Dimitroulas T, Sfikakis PP, Seo P, Gabriel S, et al. Cardiovascular magnetic resonance in rheumatology: current status and recommendations for use. Int J Cardiol. 2016;217(C):135–48.CrossRefPubMedGoogle Scholar
  8. 8.
    Gerster M, Peker E, Nagel E, Puntmann VO. Deciphering cardiac involvement in systemic inflammatory diseases: noninvasive tissue characterisation using cardiac magnetic resonance is key to improved patients’ care. Expert Rev Cardiovasc Ther. 2016;14(11):1283–95.CrossRefPubMedGoogle Scholar
  9. 9.
    Isted A, Grigoratos C, Bratis K, Carr-White G, Nagel E, Puntmann VO. Native T1 in deciphering the reversible myocardial inflammation in cardiac sarcoidosis with anti-inflammatory treatment. Int J Cardiol. 2016;203:459–62.CrossRefPubMedGoogle Scholar
  10. 10.
    Mavrogeni S, Karabela G, Stavropoulos E, Plastiras S, Spiliotis G, Gialafos E, et al. Heart failure imaging patterns in systemic lupus erythematosus. Evaluation using cardiovascular magnetic resonance. Int J Cardiol. 2014;176(2):559–61.CrossRefPubMedGoogle Scholar
  11. 11.
    Maradit-Kremers H, Crowson CS, Nicola PJ, Ballman KV, Roger VRL, Jacobsen SJ, et al. Increased unrecognized coronary heart disease and sudden deaths in rheumatoid arthritis: a population-based cohort study. Arthritis Rheum. 2005;52(2):402–11.CrossRefPubMedGoogle Scholar
  12. 12.
    Nicola PJ, Maradit-Kremers H, Roger VRL, Jacobsen SJ, Crowson CS, Ballman KV, et al. The risk of congestive heart failure in rheumatoid arthritis: a population-based study over 46 years. Arthritis Rheum. 2005;52(2):412–20.CrossRefPubMedGoogle Scholar
  13. 13.
    Palmieri V, Migliaresi P, Orefice M, Lupo T, Di Minno MND, Valentini G, et al. High prevalence of subclinical cardiovascular abnormalities in patients with systemic lupus erythematosus in spite of a very low clinical damage index. Nutr Metab Cardiovasc Dis. 2009;19(4):234–40.CrossRefPubMedGoogle Scholar
  14. 14.
    Manzi S, Meilahn EN, Rairie JE, Conte CG, Medsger TA, Jansen-McWilliams L, et al. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham Study. Am J Epidemiol. 1997;145(5):408–15.CrossRefPubMedGoogle Scholar
  15. 15.
    Hinojar R, Foote L, Sangle S, Marber M, Mayr M, Carr-White G, et al. Native T1 and T2 mapping by CMR in lupus myocarditis: disease recognition and response to treatment. Int J Cardiol. 2016;222:717–26.CrossRefPubMedGoogle Scholar
  16. 16.
    Zhang Y, Corona-Villalobos CP, Kiani AN, Eng J, Kamel IR, Zimmerman SL, et al. Myocardial T2 mapping by cardiovascular magnetic resonance reveals subclinical myocardial inflammation in patients with systemic lupus erythematosus. Int J Cardiovasc Imaging. 2014;31(2):389–97.CrossRefPubMedGoogle Scholar
  17. 17.
    Puntmann VO, D’Cruz D, Smith Z, Pastor A, Choong P, Voigt T, et al. Native myocardial T1 mapping by cardiovascular magnetic resonance imaging in subclinical cardiomyopathy in patients with systemic lupus erythematosus. Circulation: Cardiovascular Imaging. 2013;6(2):295–301.Google Scholar
  18. 18.
    Ntusi NAB, Piechnik SK, Francis JM, Ferreira VM, Matthews PM, Robson MD, et al. Diffuse myocardial fibrosis and inflammation in rheumatoid arthritis. J Am Coll Cardiol Img. 2015;8(5):526–36.CrossRefGoogle Scholar
  19. 19.
    Mavrogeni S, Spargias C, Bratis C, Kolovou G, Markussis V, Papadopoulou E, et al. Myocarditis as a precipitating factor for heart failure: evaluation and 1-year follow-up using cardiovascular magnetic resonance and endomyocardial biopsy. Eur J Heart Fail. 2011;13(8):830–7.CrossRefPubMedGoogle Scholar
  20. 20.
    Patel MR, Cawley PJ, Heitner JF, Klem I, Parker MA, Jaroudi WA, et al. Detection of myocardial damage in patients with sarcoidosis. Circulation. 2009;120(20):1969–77.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Greulich S, Deluigi CC, Gloekler S, Wahl A, Zürn C, Kramer U, et al. CMR imaging predicts death and other adverse events in suspected cardiac sarcoidosis. J Am Coll Cardiol Img. 2013;6(4):501–11.CrossRefGoogle Scholar
  22. 22.
    • Puntmann VO, Isted A, Hinojar R, Foote L, Carr-White G, Nagel E. T1 and T2 mapping in recognition of early cardiac involvement in systemic sarcoidosis. Radiology. 2017;162732. T1 mapping detects early stages of myocardial involvement in systemic sarcoidosis and is overall a reliable marker for inflammatory reversibility upon usage of CMR imaging-based treatment . Google Scholar
  23. 23.
    Puntmann VO, Bigalke B, Nagel E. Characterization of the inflammatory phenotype in atherosclerosis may contribute to the development of new therapeutic and preventative interventions. Trends in Cardiovascular Medicine. 2010;20(5):176–81.CrossRefPubMedGoogle Scholar
  24. 24.
    Varma N, Hinojar R, D’Cruz D, Arroyo Ucar E, Indermuehle A, Peel S, et al. Coronary vessel wall contrast enhancement imaging as a potential direct marker of coronary involvement. J Am Coll Cardiol Img. 2014;7(8):762–70.CrossRefGoogle Scholar
  25. 25.
    Raman SV, Aneja A, Aneja A, Jarjour WN, Jarjour WN. CMR in inflammatory vasculitis. J Cardiovasc Magn Reson [Internet]. 2012;14(1):82. Scholar
  26. 26.
    Keenan NG, Mason JC, Maceira A, Assomull R, O’Hanlon R, Chan C, et al. Integrated cardiac and vascular assessment in Takayasu arteritis by cardiovascular magnetic resonance. Arthritis Rheum. 2009;60(11):3501–9.CrossRefPubMedGoogle Scholar
  27. 27.
    Ntusi NA, Piechnik SK, Francis JM, Ferreira VM, Rai AB, Matthews PM, et al. Subclinical myocardial inflammation and diffuse fibrosis are common in systemic sclerosis—a clinical study using myocardial T1-mapping and extracellular volume quantification. J Cardiovasc Magn Reson. 2014;16(1):21.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Barison A, Gargani L, De Marchi D, Aquaro GD, Guiducci S, Picano E, et al. Early myocardial and skeletal muscle interstitial remodelling in systemic sclerosis: insights from extracellular volume quantification using cardiovascular magnetic resonance. Eur Heart J - Cardiovasc Imaging. 2015;16(1):74–80.CrossRefPubMedGoogle Scholar
  29. 29.
    Ishimori ML, Martin R, Berman DS, Goykhman P, Shaw LJ, Shufelt C, et al. Myocardial ischemia in the absence of obstructive coronary artery disease in systemic lupus erythematosus. J Am Coll Cardiol Img. 2011;4(1):27–33.CrossRefGoogle Scholar
  30. 30.
    Di Cesare E, Battisti S, Di Sibio A, Cipriani P, Giacomelli R, Liakouli V, et al. Early assessment of sub-clinical cardiac involvement in systemic sclerosis (SSc) using delayed enhancement cardiac magnetic resonance (CE-MRI). Eur J Radiol. 2013;82(6):e268–73.CrossRefPubMedGoogle Scholar
  31. 31.
    Marmursztejn J, Guillevin L, Trebossen R, Cohen P, Guilpain P, Pagnoux C, et al. Churg-Strauss syndrome cardiac involvement evaluated by cardiac magnetic resonance imaging and positron-emission tomography: a prospective study on 20 patients. Rheumatology (Oxford). 2013;52(4):642–50.CrossRefGoogle Scholar
  32. 32.
    Appenzeller S, Pineau C, Clarke A. Acute lupus myocarditis: clinical features and outcome. Lupus. 2011;20(9):981–8.CrossRefPubMedGoogle Scholar
  33. 33.
    Ishimori ML, Agarwal M, Ng RK, Nugent LD, Wallace DJ, Siegel RJ, et al. Lupus cardiomyopathy: a reversible form of left ventricular dysfunction. Arthritis Res Ther. 2012;14(Suppl 3):A61.CrossRefPubMedCentralGoogle Scholar
  34. 34.
    Bruce IN. “Not only...but also”: factors that contribute to accelerated atherosclerosis and premature coronary heart disease in systemic lupus erythematosus. Rheumatology. 2005;44(12):1492–502.CrossRefPubMedGoogle Scholar
  35. 35.
    Ishimori ML, Agarwal M, Beigel R, Ng RK, Firooz N, Weisman MH, et al. Systemic lupus erythematosus cardiomyopathy—a case series demonstrating a reversible form of left ventricular dysfunction. Echocardiography. 2013;31(5):563–8.CrossRefGoogle Scholar
  36. 36.
    Puntmann VO, Carr-White G, Jabbour A, Yu C-Y, Gebker R, Kelle S, et al. T1-mapping and outcome in nonischemic cardiomyopathy. J Am Coll Cardiol Img. 2016;9(1):40–50.CrossRefGoogle Scholar
  37. 37.
    Dabir D, Child N, Kalra A, Rogers T, Gebker R, Jabbour A, et al. Reference values for healthy human myocardium using a T1 mapping methodology: results from the international T1 multicenter cardiovascular magnetic resonance study. J Cardiovasc Magn Reson. 2014;16(1):34.CrossRefGoogle Scholar
  38. 38.
    Hinojar R, Foote L, Cummins C, Higgins DM, Nagel E, Puntmann V. Standardised postprocessing of native T2 in detection and discrimination of myocarditis—comparison with native T1 mapping. J Cardiovasc Magn Reson. 2016;18(Suppl 1):O14.CrossRefPubMedCentralGoogle Scholar
  39. 39.
    Marinescu MA, Löffler AI, Ouellette M, Smith L, Kramer CM, Bourque JM. Coronary microvascular dysfunction, microvascular angina, and treatment strategies. JCMG. 2015;8(2):210–20.Google Scholar
  40. 40.
    Nagel E. Taking the last hurdles: magnetic resonance myocardial perfusion imaging. JACC Cardiovasc Imaging. 2009;2(4):434–6.CrossRefPubMedGoogle Scholar
  41. 41.
    Recio-Mayoral A, Mason JC, Kaski JC, Rubens MB, Harari OA, Camici PG. Chronic inflammation and coronary microvascular dysfunction in patients without risk factors for coronary artery disease. Eur Heart J. 2009;30(15):1837–43.CrossRefPubMedGoogle Scholar
  42. 42.
    Fichtlscherer S, Rossig L, Breuer S, Vasa M, Dimmeler S, Zeiher AM. Tumor necrosis factor antagonism with etanercept improves systemic endothelial vasoreactivity in patients with advanced heart failure. Circulation. 2001;104(25):3023–5.CrossRefPubMedGoogle Scholar
  43. 43.
    Ishimori ML, Anderson L, Weisman MH, Mehta PK, Bairey Merz CN, Wallace DJ. Microvascular angina: an underappreciated cause of SLE chest pain. J Rheumatol. 2013;40(5):746–7.CrossRefPubMedGoogle Scholar
  44. 44.
    Pasceri V, Yeh ETH. A tale of two diseases : atherosclerosis and rheumatoid arthritis. Circulation. 1999;100(21):2124–6.CrossRefPubMedGoogle Scholar
  45. 45.
    Symmons DPM, Gabriel SE. Epidemiology of CVD in rheumatic disease, with a focus on RA and SLE. Nat Rev Rheumatol. 2011;7(7):399–408.CrossRefPubMedGoogle Scholar
  46. 46.
    Puntmann VO, Taylor PC, Barr A, Schnackenburg B, Jahnke C, Paetsch I. Towards understanding the phenotypes of myocardial involvement in the presence of self-limiting and sustained systemic inflammation: a magnetic resonance imaging study. Rheumatology. 2010 Feb 11;49(3):528–35.CrossRefPubMedGoogle Scholar
  47. 47.
    Puntmann VO, Peker E, Chandrashekhar Y, Nagel E. T1 mapping in characterizing myocardial disease. Circ Res. 2016;119(2):277–99.CrossRefPubMedGoogle Scholar
  48. 48.
    Zawadowski G, Klarich K, Moder K, Edwards W, Cooper L. A contemporary case series of lupus myocarditis. Lupus. 2012;21(13):1378–84.CrossRefPubMedGoogle Scholar
  49. 49.
    Bohnen S, Radunski UK, Lund GK, Kandolf R, Stehning C, Schnackenburg B, et al. Performance of T1 and T2 mapping cardiovascular magnetic resonance to detect active myocarditis in patients with recent-onset heart failure. Circulation: Cardiovascular Imaging. 2015;8(6):e003073.Google Scholar
  50. 50.
    • Hinojar R, Foote L, Arroyo Ucar E, Jackson T, Jabbour A, Yu C-Y, et al. Native T1 in discrimination of acute and convalescent stages in patients with clinical diagnosis of myocarditis. J Am Coll Cardiol Img. 2015;8(1):37–46. This study reveals the difference of acute and chronic disease by CMR imaging. It specially focuses on T1 and T2 mapping as markers of inflammatory activity and disease stages. CrossRefGoogle Scholar
  51. 51.
    Puntmann VO, Voigt T, Chen Z, Mayr M, Karim R, Rhode K, et al. Native T1 mapping in differentiation of normal myocardium from diffuse disease in hypertrophic and dilated cardiomyopathy. J Am Coll Cardiol Img. 2013;6(4):475–84.CrossRefGoogle Scholar
  52. 52.
    Hinojar R, Varma N, Child N, Goodman B, Jabbour A, Yu C-Y, et al. T1 mapping in discrimination of hypertrophic phenotypes: hypertensive heart disease and hypertrophic cardiomyopathyclinical perspective. Circulation: Cardiovascular Imaging. 2015;8(12):e003285.Google Scholar
  53. 53.
    Giri S, Chung Y-C, Merchant A, Mihai G, Rajagopalan S, Raman SV, et al. T2 quantification for improved detection of myocardial edema. J Cardiovasc Magn Reson. 2009;11(1):56.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Lurz P, Luecke C, Eitel I, Föhrenbach F, Frank C, Grothoff M, et al. Comprehensive cardiac magnetic resonance imaging in patients with suspected myocarditis. J Am Coll Cardiol. 2016;67(15):1800–11.CrossRefPubMedGoogle Scholar
  55. 55.
    von Knobelsdorff-Brenkenhoff F, Schüler J, Dogangüzel S, Dieringer MA, Rudolph A, Greiser A, et al. Detection and monitoring of acute myocarditis applying quantitative cardiovascular magnetic resonance. Circulation: Cardiovascular Imaging. 2017;10(2):e005242.Google Scholar
  56. 56.
    Hachulla A-L, Launay D, Gaxotte V, de Groote P, Lamblin N, Devos P, et al. Cardiac magnetic resonance imaging in systemic sclerosis: a cross-sectional observational study of 52 patients. Ann Rheum Dis. 2009;68(12):1878–84.CrossRefPubMedGoogle Scholar
  57. 57.
    Radunski UK, Lund GK, Stehning C, Schnackenburg B, Bohnen S, Adam G, et al. CMR in patients with severe myocarditis. J Am Coll Cardiol Img. 2014;7(7):667–75.CrossRefGoogle Scholar
  58. 58.
    Child N, Suna G, Dabir D, Yap ML, Rogers T, Kathirgamanathan M, et al. Comparison of MOLLI, shMOLLLI, and SASHA in discrimination between health and disease and relationship with histologically derived collagen volume fraction. Eur Heart J Cardiovasc Imaging. 2017.Google Scholar
  59. 59.
    Caforio ALP, Pankuweit S, Arbustini E, Basso C, Gimeno-Blanes J, Felix SB, et al. Current state of knowledge on aetiology, diagnosis, management, and therapy of myocarditis: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J. 2013;34(33):2636–48.CrossRefPubMedGoogle Scholar
  60. 60.
    Authors/Task Force members, Perk J, De Backer G, Gohlke H, Graham I, Verschuren M, et al. European guidelines on cardiovascular disease prevention in clinical practice (version 2012): The Fifth Joint Task Force of the European Society of Cardiology and Other Societies on Cardiovascular Disease Prevention in Clinical Practice (constituted by representatives of nine societies and by invited experts) * Developed with the special contribution of the European Association for Cardiovascular Prevention & Rehabilitation (EACPR). Eur Heart J. 2012;33(13):1635–701.CrossRefGoogle Scholar
  61. 61.
    2013 ESC guidelines on the management of stable coronary artery disease. Eur Heart J. 2013;34(38):2949–3003.Google Scholar
  62. 62.
    Shaw LJ, Olson MB, Kip K, Kelsey SF, Johnson BD, Mark DB, et al. The value of estimated functional capacity in estimating outcome. J Am Coll Cardiol. 2006;47(3):S36–43.CrossRefPubMedGoogle Scholar
  63. 63.
    Bairey Merz CN, Shaw LJ, Reis SE, Bittner V, Kelsey SF, Olson M, et al. Insights from the NHLBI-sponsored Women’s Ischemia Syndrome Evaluation (WISE) Study. J Am Coll Cardiol. 2006;47(3):S21–9.CrossRefPubMedGoogle Scholar
  64. 64.
    Nagel E. Magnetic resonance perfusion measurements for the noninvasive detection of coronary artery disease. Circulation. 2003;108(4):432–7.CrossRefPubMedGoogle Scholar
  65. 65.
    Schwitter J, Wacker CM, van Rossum AC, Lombardi M, Al-Saadi N, Ahlstrom H, et al. MR-IMPACT: comparison of perfusion-cardiac magnetic resonance with single-photon emission computed tomography for the detection of coronary artery disease in a multicentre, multivendor, randomized trial. Eur Heart J. 2008;29(4):480–9.CrossRefPubMedGoogle Scholar
  66. 66.
    Schwitter J, Wacker CM, Wilke N, Al-Saadi N, Sauer E, Huettle K, et al. MR-IMPACT II: Magnetic Resonance Imaging for Myocardial Perfusion Assessment in Coronary artery disease Trial: perfusion-cardiac magnetic resonance vs. single-photon emission computed tomography for the detection of coronary artery disease: a comparative multicentre, multivendor trial. Eur Heart J. 2013;34(10):775–81.CrossRefPubMedGoogle Scholar
  67. 67.
    Greenwood JP, Maredia N, Younger JF, Brown JM, Nixon J, Everett CC, et al. Cardiovascular magnetic resonance and single-photon emission computed tomography for diagnosis of coronary heart disease (CE-MARC): a prospective trial. Lancet. 2012;379(9814):453–60.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Jaarsma C, Leiner T, Bekkers S, Crijns H, Wildberger J, Nagel E, et al. Diagnostic performance of PET, SPECT and CMR perfusion imaging for the detection of significant coronary artery disease—a meta-analysis. J Cardiovasc Magn Reson. 2011;13(Suppl 1):P75.CrossRefPubMedCentralGoogle Scholar
  69. 69.
    Jaarsma C, Leiner T, Bekkers SC, Crijns HJ, Wildberger JE, Nagel E, et al. Diagnostic performance of noninvasive myocardial perfusion imaging using single-photon emission computed tomography, cardiac magnetic resonance, and positron emission tomography imaging for the detection of obstructive coronary artery disease. J Am Coll Cardiol. 2012;59(19):1719–28.CrossRefPubMedGoogle Scholar
  70. 70.
    Kelle S, Roes SD, Klein C, Kokocinski T, de Roos A, Fleck E, et al. Prognostic value of myocardial infarct size and contractile reserve using magnetic resonance imaging. J Am Coll Cardiol. 2009;54(19):1770–7.CrossRefPubMedGoogle Scholar
  71. 71.
    Nagel E, Shaw LJ. The assessment of ischaemic burden: thoughts on definition and quantification. Eur Heart J - Cardiovasc Imaging. 2014;15(6):610–1.CrossRefPubMedGoogle Scholar
  72. 72.
    Shaw LJ, Berman DS, Picard MH, Friedrich MG, Kwong RY, Stone GW, et al. Comparative definitions for moderate-severe ischemia in stress nuclear, echocardiography, and magnetic resonance imaging. J Am Coll Cardiol Img. 2014;7(6):593–604.CrossRefGoogle Scholar
  73. 73.
    Greenwood JP, Motwani M, Maredia N, Brown JM, Everett CC, Nixon J, et al. Comparison of cardiovascular magnetic resonance and single-photon emission computed tomography in women with suspected coronary artery disease from the Clinical Evaluation of Magnetic Resonance Imaging in Coronary Heart Disease (CE-MARC) Trial. Circulation. 2014;129(10):1129–38.CrossRefPubMedGoogle Scholar
  74. 74.
    Arroyo-Espliguero R. Microvascular dysfunction in cardiac syndrome X: the role of inflammation. Can Med Assoc J. 2006;174(13):1833.CrossRefGoogle Scholar
  75. 75.
    Mehta PK, Goykhman P, Thomson LEJ, Shufelt C, Wei J, Yang Y, et al. Ranolazine improves angina in women with evidence of myocardial ischemia but no obstructive coronary artery disease. J Am Coll Cardiol Img. 2011;4(5):514–22.CrossRefGoogle Scholar
  76. 76.
    Puntmann VO, D’Cruz D, Taylor PC, Hussain T, Indermuhle A, Butzbach B, et al. Contrast enhancement imaging in coronary arteries in SLE. J Am Coll Cardiol Img. 2012;5(9):962–4.CrossRefGoogle Scholar
  77. 77.
    Faccini A, Kaski JC, Camici PG. Coronary microvascular dysfunction in chronic inflammatory rheumatoid diseases. Eur Heart J. 2016;37(23):1799–806.CrossRefPubMedGoogle Scholar
  78. 78.
    Ntusi NA, Piechnik SK, Francis JM, Ferreira VM, Matthews PM, Robson MD, et al. Diffuse myocardial fibrosis is associated with impaired myocardial strain and disease activity in rheumatoid arthritis: a cardiovascular magnetic resonance study. J Cardiovasc Magn Reson. 2014;16(Suppl 1):P292.CrossRefPubMedCentralGoogle Scholar
  79. 79.
    • Puntmann VO, Arroyo Ucar E, Hinojar Baydes R, Ngah NB, Kuo YS, Dabir D, et al. Aortic stiffness and interstitial myocardial fibrosis by native T1 are independently associated with left ventricular remodeling in patients with dilated cardiomyopathy. Hypertension. 2014;64(4):762–8. T1 mapping is remarkably increased in patients with dilated cardiomyopathy describing interstitial myocardial fibrosis. It is also related to aortic stiffness shown by a strikingly higher pulse wave velocity. CrossRefPubMedGoogle Scholar
  80. 80.
    Gulati A, Jabbour A, Ismail TF, Guha K, Khwaja J, Raza S, et al. Association of fibrosis with mortality and sudden cardiac death in patients with nonischemic dilated cardiomyopathy. JAMA. 2013;309(9):896–908.CrossRefPubMedGoogle Scholar
  81. 81.
    Mavrogeni S, Sfikakis PP, Gialafos E, Bratis K, Karabela G, Stavropoulos E, et al. Cardiac tissue characterization and the diagnostic value of cardiovascular magnetic resonance in systemic connective tissue diseases. Arthritis Care Res. 2013;66(1):104–12.CrossRefGoogle Scholar
  82. 82.
    Mavrogeni SI, Kitas GD, Dimitroulas T, Sfikakis PP, Seo P, Gabriel S, et al. Cardiovascular magnetic resonance in rheumatology: current status and recommendations for use. Int J Cardiol. 2016;217:135–48.CrossRefPubMedGoogle Scholar
  83. 83.
    O’Neill SG, Woldman S, Bailliard F, Norman W, McEwan J, Isenberg DA, et al. Cardiac magnetic resonance imaging in patients with systemic lupus erythematosus. Ann Rheum Dis. 2009;68(9):1478–81.CrossRefPubMedGoogle Scholar
  84. 84.
    Eyler AE, Ahmad FA, Jahangir E. Magnetic resonance imaging of the cardiac manifestations of Churg-Strauss. JRSM Open. SAGE PublicationsSage UK: London, England; 2014;5(4):2054270414525370.Google Scholar
  85. 85.
    Mavrogeni S, Karabela G, Gialafos E, Stavropoulos E, Spiliotis G, Katsifis G, et al. Cardiac involvement in ANCA (+) and ANCA (-) Churg-Strauss syndrome evaluated by cardiovascular magnetic resonance. Inflamm Allergy Drug Targets. 2013;12(5):322–7.CrossRefPubMedGoogle Scholar
  86. 86.
    van Leuven SI, Franssen R, Kastelein JJ, Levi M, Stroes ESG, Tak PP. Systemic inflammation as a risk factor for atherothrombosis. Rheumatology. 2008;47(1):3–7.CrossRefPubMedGoogle Scholar
  87. 87.
    Ridker PM, Everett BM, Thuren T, MacFadyen JG, Chang WH, Ballantyne C, et al. Antiinflammatory therapy with canakinumab for atherosclerotic disease. N Engl J Med. 2017;377(12):1119–31.CrossRefPubMedGoogle Scholar
  88. 88.
    Ridker PM. From C-reactive protein to Interleukin-6 to Interleukin-1: moving upstream to identify novel targets for Atheroprotection. Circ Res. 2016;118(1):145–56.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    McInnes IB, Thompson L, Giles JT, Bathon JM, Salmon JE, Beaulieu AD, et al. Effect of interleukin-6 receptor blockade on surrogates of vascular risk in rheumatoid arthritis: MEASURE, a randomised, placebo-controlled study. Ann Rheum Dis. 2015;74(4):694–702.CrossRefPubMedGoogle Scholar
  90. 90.
    Hurlimann D. Anti-tumor necrosis factor-alpha treatment improves endothelial function in patients with rheumatoid arthritis. Circulation. 2002;106(17):2184–7.CrossRefPubMedGoogle Scholar
  91. 91.
    Maki-Petaja KM, Elkhawad M, Cheriyan J, Joshi FR, Ostor AJK, Hall FC, et al. Anti-tumor necrosis factor- therapy reduces aortic inflammation and stiffness in patients with rheumatoid arthritis. Circulation. 2012;126(21):2473–80.CrossRefPubMedGoogle Scholar
  92. 92.
    Maki-Petaja KM. Rheumatoid arthritis is associated with increased aortic pulse-wave velocity, which is reduced by anti-tumor necrosis factor- therapy. Circulation. 2006;114(11):1185–92.CrossRefPubMedGoogle Scholar
  93. 93.
    Ferreira VM, Piechnik SK, Dall’Armellina E, Karamitsos TD, Francis JM, Choudhury RP, et al. Non-contrast T1-mapping detects acute myocardial edema with high diagnostic accuracy: a comparison to T2-weighted cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2012;14(1):42.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Greulich S1, Kitterer D1, Latus J1, Aguor E1, Steubing H1, Kaesemann P1, Patrascu A1, Greiser A1, Groeninger S1, Mayr A1, Braun N1, Alscher MD1, Sechtem U1, Mahrholdt H2. Comprehensive Cardiovascular Magnetic Resonance Assessment in Patients With Sarcoidosis and Preserved Left Ventricular Ejection Fraction. Circ Cardiovasc Imaging. 2016;9(11). pii: e005022Google Scholar
  95. 95.
    Hromádka M1, Seidlerová J2, Suchý D3, Rajdl D4, Lhotský J1, Ludvík J5, Rokyta R1, BaxaJ5. Myocardial fibrosis detected by magnetic resonance in systemic sclerosis patients -Relationship with biochemical and echocardiography parameters. Int J Cardiol. 2017;249:448-453.
  96. 96.
    Wu R1, An DA1, Hu J2, Jiang M3, Guo Q4, Xu JR1, Wu LM1. The apparent diffusioncoefficient is strongly correlated with extracellular volume, a measure of myocardial fibrosis,and subclinical cardiomyopathy in patients with systemic lupus erythematosus. Acta Radiol. 2018;59(3):287-295.
  97. 97.
    Holmström M, Koivuniemi R, Korpi K, Kaasalainen T, Laine M, Kuuliala, Leirisalo-Repo M,Kupari M, Kivistö S. Cardiac magnetic resonance imaging reveals frequent myocardialinvolvement and dysfunction in active rheumatoid arthritis. Clin Exp Rheumatol 2016;34(3):416-23Google Scholar
  98. 98.
    Greulich S, Mayr A, Kitterer D, Latus J, Henes J, Steubing H, Kaesemann P, Patrascu A,Greiser A, Groeninger S, Braun N, Alscher MD, Sechtem U, Mahrholdt H. T1 and T2 mappingfor evaluation of myocardial involvement in patients with ANCA-associated vasculitides. JCardiovasc Magn Reson. 2017;19(1):6Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Lea Winau
    • 1
  • Eike Nagel
    • 1
    • 2
  • Eva Herrmann
    • 3
  • Valentina O. Puntmann
    • 1
    • 2
    Email author
  1. 1.Institute for Experimental and Translational Cardiovascular Imaging, DZHK Centre for Cardiovascular ImagingGoethe University Hospital FrankfurtFrankfurt am MainGermany
  2. 2.Department of CardiologyGoethe University Hospital FrankfurtFrankfurt am MainGermany
  3. 3.DZHK Institute of Biostatistics and Mathematical Modelling at Goethe University FrankfurtFrankfurt am MainGermany

Personalised recommendations