Heart Failure Reviews

, Volume 24, Issue 4, pp 489–498 | Cite as

Pathophysiology and imaging of heart failure in women with autoimmune rheumatic diseases

  • Sophie I. MavrogeniEmail author
  • George Markousis-Mavrogenis
  • Loukia Koutsogeorgopoulou
  • Theodoros Dimitroulas
  • Vasiliki Vartela
  • Angelos Rigopoulos
  • Michel Noutsias
  • Genovefa Kolovou


Autoimmune rheumatic diseases (ARDs) affect 8% of the population, and approximately 78% of them are women. Cardiovascular disease (CVD) in ARDs encompasses different pathophysiologic processes, such as endothelial dysfunction, myocardial/vascular inflammation and accelerated atherosclerosis with silent clinical presentation, leading to heart failure (HF), usually with preserved ejection fraction. Echocardiography and cardiovascular magnetic resonance (CMR) are the two most commonly used noninvasive imaging modalities for the evaluation of HF in patients with ARDs. Echocardiography currently represents the main diagnostic tool for cardiac imaging in clinical practice. However, the demand for more efficient and prompt diagnostic and therapeutic approach in this specific population necessitates the implementation of modalities capable of providing a more detailed and quantified information from the point of tissue characterization. Furthermore, echocardiography is an operator and acoustic window depended modality, with relatively low reproducibility and unable to perform tissue characterization. CMR is a noninvasive modality without radiation that can give reproducible and operator-independent information about both myocardial function and tissue characterization. By providing quantification of oedema, stress perfusion defects and fibrosis, CMR can diagnose myocardial inflammation, micro–macro-vascular myocardial ischemia and replacement or diffuse fibrosis, respectively. Tissue characterization allows for moving beyond the cardiac function to the assessment of intra- and inter-cellular alterations and promotes the development of personalized cardiac and anti-rheumatic treatment in ARDs with HF. ARDs are mainly female diseases. Cardiac involvement leading in HF is not unusual in ARDs and remains the main cause of death. Noninvasive, nonradiating imaging modalities such as echocardiography and CMR represent the main diagnostic tools. Specifically, echocardiography represents the first diagnostic approach; however, it is CMR that gives information about the pathophysiologic background behind HF in ARDs.


Heart failure Echocardiography Cardiovascular magnetic resonance Nuclear imaging Cardiovascular computed tomography Myocardial perfusion–fibrosis Coronary artery disease Vasculitis Rheumatic cardiovascular disease Myocarditis 



  1. 1.
    Yancy CW, Jessup M, Bozkurt B, Butler J, Casey DE Jr, Drazner MH, Fonarow GC, Geraci SA, Horwich T, Januzzi JL, Johnson MR, Kasper EK, Levy WC, Masoudi FA, McBride PE, McMurray JJV, Mitchell JE, Peterson PN, Riegel B, Sam F, Stevenson LW, Tang WHW, Tsai EJ, Wilkoff BL (2013) 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Circulation. 128:1810–1815Google Scholar
  2. 2.
    Loehr LR, Rosamond WD, Chang PP, Folsom AR, Chambless LE (2008) Heart failure incidence and survival (from the Atherosclerosis Risk in Communities study). Am J Cardiol 101:1016–1022Google Scholar
  3. 3.
    Petrie M, Dawson N, Murdoch D, Davie A, McMurray J (1999) Failure of women’s hearts. Circulation. 99:2334–2341Google Scholar
  4. 4.
    Rumsfeld J, Masoudi F (2004) Sex differences: implications for heart failure care. Eur Heart J 25:101–103Google Scholar
  5. 5.
    Elster SK, Braunwald E, Wood HF (1956) A study of C-reactive protein in the serum of patients with congestive heart failure. Am Heart J 51:533–541Google Scholar
  6. 6.
    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 103:2055–2059Google Scholar
  7. 7.
    Levine B, Kalman J, Mayer L, Fillit HM, Packer M (1990) Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. N Engl J Med 323:236–241Google Scholar
  8. 8.
    DuBrock HM, AbouEzzeddine OF, Redfield MM (2018) High-sensitivity C-reactive protein in heart failure with preserved ejection fraction. PLoS One 13(8):e0201836Google Scholar
  9. 9.
    Mavrogeni SI, Kitas GD, Dimitroulas T, Sfikakis PP, Seo P, Gabriel S, Patel AR, Gargani L, Bombardieri S, Matucci-Cerinic M, Lombardi M, Pepe A, Aletras AH, Kolovou G, Miszalski T, van Riel P, Semb A, Gonzalez-Gay MA, Dessein P, Karpouzas G, Puntmann V, Nagel E, Bratis K, Karabela G, Stavropoulos E, Katsifis G, Koutsogeorgopoulou L, van Rossum A, Rademakers F, Pohost G, Lima JA (2016) Cardiovascular magnetic resonance in rheumatology: current status and recommendations for use. Int J Cardiol 217:135–148Google Scholar
  10. 10.
    Zandman-Goddard G, Peeva E, Shoenfeld Y (2007) Gender and autoimmunity. Autoimmun Rev 6:366–372Google Scholar
  11. 11.
    Fairweather D, Frisancho-Kiss S, Rose NR (2008) Sex differences in autoimmune disease from a pathologic perspective. Am J Pathol 173:600–609Google Scholar
  12. 12.
    Mavrogeni S, Dimitroulas T, Gabriel S, Sfikakis PP, Pohost GM, Kitas GD (2014) Why currently used diagnostic techniques for heart failure in rheumatoid arthritis are not enough: the challenge of cardiovascular magnetic resonance imaging. Rev Cardiovasc Med 15(4):320–331Google Scholar
  13. 13.
    Nurmohamed MT, Heslinga M, Kitas GD (2015) Cardiovascular comorbidity in rheumatic diseases. Nat Rev Rheumatol 11(12):693–704Google Scholar
  14. 14.
    Gasparyan AY, Ayvazyan L, Cocco G, Kitas GD (2012) Adverse cardiovascular effects of antirheumatic drugs: implications for clinical practice and research. Curr Pharm Des 18(11):1543–1555Google Scholar
  15. 15.
    Myasoedova E, Crowson CS, Turesson C, Gabriel SE, Matteson EL (2011) Incidence of extraarticular rheumatoid arthritis in Olmsted County, Minnesota, in 1995–2007 versus 1985–1994: a population-based study. J Rheumatol 38:983–989Google Scholar
  16. 16.
    Ramagopalan SV, Goldacre R, Skingsley A, Conlon C, Goldacre MJ (2013) Associations between selected immune-mediated diseases and tuberculosis: record-linkage studies. BMC Med 11:97Google Scholar
  17. 17.
    Steen VD, Oddis CV, Conte CG, Janoski J, Casterline GZ, Medsger TA Jr (1997) Incidence of systemic sclerosis in Allegheny County, Pennsylvania. A twenty-year study of hospital-diagnosed cases, 1963–1982. Arthritis Rheum 40(3):441–445Google Scholar
  18. 18.
    Gaubitz M (2006) Epidemiology of connective tissue disorders. Rheumatology 45:iii3–iii4Google Scholar
  19. 19.
    Carlos de Souza FE, Levy-Neto M, Katsuyuki Shinjo S (2011) Prevalence of clinical and laboratory manifestations and comorbidities in polymyositis according to gender. Rev Bras Reumatol 51(5)Google Scholar
  20. 20.
    Lim AY, Lee GY, Jang SY, Gwag HB, Choi SH, Jeon ES, Cha HS, Sung K, Kim YW, Kim SM, Choe YH, Kim DK (2015) Gender differences in clinical and angiographic findings of patients with Takayasu arteritis. Clin Exp Rheumatol 33(2 Suppl 89):S-132–S-137Google Scholar
  21. 21.
    Chang RK (2002) Epidemiologic characteristics of children hospitalized for Kawasaki disease in California. Pediatr Infect Dis J 21(12):1150–1155Google Scholar
  22. 22.
    Nicola PJ, Maradit-Kremers H, Roger VL, Jacobsen SJ, Crowson CS, Ballman KV et al (2005) The risk of congestive heart failure in rheumatoid arthritis: a population-based study over 46 years. Arthritis Rheum 52:412–420Google Scholar
  23. 23.
    Schoenfeld SR, Kasturi S, Costenbader KH (2013) The epidemiology of atherosclerotic cardiovascular disease among patients with SLE: a systematic review. Semin Arthritis Rheum 43:77–95Google Scholar
  24. 24.
    Mavrogeni S, Karabela G, Koutsogeorgopoulou L, Stavropoulos E, Katsifis G, Plastiras SC, Kitas GD, Panopoulos S, Pentazos G, Tzatzaki E, Markousis-Mavrogenis G, Kolovou G, Sfikakis PP (2016) Pseudo-infarction pattern in diffuse systemic sclerosis. Evaluation using cardiovascular magnetic resonance. Int J Cardiol 214:465–468Google Scholar
  25. 25.
    Mavrogeni S, Sfikakis PP, Dimitroulas T, Kolovou G, Kitas GD (2014) Cardiac and muscular involvement in idiopathic inflammatory myopathies: noninvasive diagnostic assessment and the role of cardiovascular and skeletal magnetic resonance imaging. Inflamm Allergy Drug Targets 13(3):206–216Google Scholar
  26. 26.
    Mavrogeni S, Sfikakis PP, Dimitroulas T, Koutsogeorgopoulou L, Karabela G, Katsifis G, Stavropoulos E, Gialafos E, Spiliotis G, Kolovou G, Kitas GD (2015) Imaging patterns of cardiovascular involvement in mixed connective tissue disease evaluated by cardiovascular magnetic resonance. Inflamm Allergy Drug Targets. 14(2):111–116Google Scholar
  27. 27.
    Mavrogeni S, Markousis-Mavrogenis G, Kolovou G (2014) Cardiovascular magnetic resonance for evaluation of heart involvement in ANCA-associated vasculitis. A luxury or a valuable diagnostic tool? Inflamm Allergy Drug Targets. 13:305–311Google Scholar
  28. 28.
    Biskup M, Biskup W, Majdan M, Targońska-Stępniak B (2018) Cardiovascular system changes in rheumatoid arthritis patients with continued low disease activity. Rheumatol Int 38(7):1207–1215Google Scholar
  29. 29.
    Wislowska M, Dereń D, Kochmański M, Sypuła S, Rozbicka J (2009) Systolic and diastolic heart function in SLE patients. Rheumatol Int 29:1469–1476Google Scholar
  30. 30.
    Tennøe AH, Murbræch K, Andreassen JC, Fretheim H, Garen T, Gude E, Andreassen A, Aakhus S, Molberg Ø, Hoffmann-Vold AM (2018) Left ventricular diastolic dysfunction predicts mortality in patients with systemic sclerosis. J Am Coll Cardiol 72(15):1804–1813Google Scholar
  31. 31.
    Yndestad A, Damås JK, Øie E, Ueland T, Gullestad L, Aukrust P (2007) Role of inflammation in the progression of heart failure. Curr Cardiol Rep 9:236–241Google Scholar
  32. 32.
    Mavrogeni S, Karabela G, Stavropoulos E, Gialafos E, Sfendouraki E, Kyrou L, Kolovou G (2013) Imaging patterns of heart failure in rheumatoid arthritis evaluated by cardiovascular magnetic resonance. Int J Cardiol 168(4):4333–4335Google Scholar
  33. 33.
    Mavrogeni S, Bratis K, Sfendouraki E, Papadopoulou E, Kolovou G (2013) Myopericarditis, as the first sign of rheumatoid arthritis relapse, evaluated by cardiac magnetic resonance. Inflamm Allergy Drug Targets 12(3):206–211Google Scholar
  34. 34.
    Chung CP, Giles JT, Petri M, Szklo M, Post W, Blumenthal RS, Gelber AC, Ouyang P, Jenny NS, Bathon JM (2012) Prevalence of traditional modifiable cardiovascular risk factors in patients with rheumatoid arthritis: comparison with control subjects from the multi-ethnic study of atherosclerosis. Semin Arthritis Rheum 41(4):535–544Google Scholar
  35. 35.
    Sherer Y, Shoenfeld Y (2006) Mechanisms of disease: atherosclerosis in autoimmune diseases. Nat Clin Pract Rheumatol 2(2):99–106Google Scholar
  36. 36.
    Solomon DH, Karlson EW, Rimm EB, Cannuscio CC, Mandl LA, Manson JE, Stampfer MJ et al (2003) Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation 107(9):1303–1307Google Scholar
  37. 37.
    Mavrogeni S, Karabela G, Stavropoulos E, Plastiras S, Spiliotis G, Gialafos E, Kolovou G, Sfikakis PP, Kitas GD (2014) Heart failure imaging patterns in systemic lupus erythematosus. Evaluation using cardiovascular magnetic resonance. Int J Cardiol 176(2):559–561Google Scholar
  38. 38.
    Mavrogeni S, Sfikakis PP, Gialafos E, Bratis K, Karabela G, Stavropoulos E, Spiliotis G, Sfendouraki E, Panopoulos S, Bournia V, Kolovou G, Kitas GD (2014) Cardiac tissue characterization and the diagnostic value of cardiovascular magnetic resonance in systemic connective tissue diseases. Arthritis Care Res (Hoboken) 66:104–112Google Scholar
  39. 39.
    Poudel DR, Derk CT (2018) Mortality and survival in systemic sclerosis: a review of recent literature. Curr Opin Rheumatol 30(6):588–593Google Scholar
  40. 40.
    Poudel DR, Jayakumar D, Danve A, Sehra ST, Derk CT (2018) Determinants of mortality in systemic sclerosis: a focused review. Rheumatol Int 38(10):1847–1858Google Scholar
  41. 41.
    Elhai M, Meune C, Boubaya M, Avouac J, Hachulla E, Balbir-Gurman A, Riemekasten G, Airò P, Joven B, Vettori S, Cozzi F, Ullman S, Czirják L, Tikly M, Müller-Ladner U, Caramaschi P, Distler O, Iannone F, Ananieva LP, Hesselstrand R, Becvar R, Gabrielli A, Damjanov N, Salvador MJ, Riccieri V, Mihai C, Szücs G, Walker UA, Hunzelmann N, Martinovic D, Smith V, Müller CS, Montecucco CM, OprisD IF, Vlachoyiannopoulos PG, Stamenkovic B, Rosato E, Heitmann S, JHW D, Zenone T, Seidel M, Vacca A, Langhe E, Novak S, Cutolo M, Mouthon L, Henes J, Chizzolini C, CAV M, Solanki K, Rednic S, Stamp L, Anic B, Santamaria VO, De Santis M, Yavuz S, Sifuentes-Giraldo WA, Chatelus E, Stork J, Laar JV, Loyo E, García de la Peña Lefebvre P, Eyerich K, Cosentino V, Alegre-Sancho JJ, Kowal-Bielecka O, Rey G, Matucci-Cerinic M, Allanore Y, EUSTAR group (2017) Mapping and predicting mortality from systemic sclerosis. Ann Rheum Dis 76(11):1897–1905Google Scholar
  42. 42.
    Arias-Nuñez MC, Llorca J, Vazquez-Rodriguez TR, Gomez-Acebo I, Miranda-Filloy JA, Martin J, Gonzalez-Juanatey C, Gonzalez-Gay MA (2008) Systemic sclerosis in northwestern Spain: a 19-year epidemiologic study. Medicine (Baltimore) 87:272–280Google Scholar
  43. 43.
    Mok MY, Lau CS (2010) The burden and measurement of cardiovascular disease in SSc. Nat Rev Rheumatol 6:430–434Google Scholar
  44. 44.
    Dimitroulas T, Giannakoulas G, Karvounis H, Garyfallos A, Settas L, Kitas GD (2014) Micro- and macrovascular treatment targets in scleroderma heart disease. Curr Pharm Des 20(4):536–544Google Scholar
  45. 45.
    Pêgo GM, Ramalho AR, Costa S, Silva F, Donato P, Franco F (2017) Autoimmune myocarditis in systemic sclerosis: an unusual form of scleroderma heart disease presentation. ESC Heart Fail 4(3):365–370Google Scholar
  46. 46.
    Mavrogeni S, Markousis-Mavrogenis G, Kolovou G (2011) Diffuse, subendocardial vasculitis identified by cardiovascular magnetic resonance. Use of images to learn pathophysiology. J Vasc 2(2):106Google Scholar
  47. 47.
    Mavrogeni S, Douskou M, Manoussakis MN (2011) Contrast-enhanced CMR imaging reveals myocardial involvement in idiopathic inflammatory myopathy without cardiac manifestations. JACC Cardiovasc Imaging 4(12):1324–1325Google Scholar
  48. 48.
    Huber AT, Bravetti M, Lamy J, Bacoyannis T, Roux C, de Cesare A, Rigolet A, Benveniste O, Allenbach Y, Kerneis M, Cluzel P, Kachenoura N, Redheuil A (2018) Non-invasive differentiation of idiopathic inflammatory myopathy with cardiac involvement from acute viral myocarditis using cardiovascular magnetic resonance imaging T1 and T2 mapping. J Cardiovasc Magn Reson 20(1):11Google Scholar
  49. 49.
    Sharp GC, Irvin WS, Tan EM, Gould RG, Holman HR (1972) Mixed connective tissue disease: an apparently distinct rheumatic disease syndrome associated with a specific antibody to an extractable nuclear antigen (ENA). Am J Med 52:148–159Google Scholar
  50. 50.
    Sharp GC (1987) Diagnostic criteria for classification of MCTD. In: Kasukawa R, Sharp GC (eds) Mixed connective tissue diseases and anti-nuclear antibodies. Elsevier, Amsterdam, pp 23–32Google Scholar
  51. 51.
    Kasukawa R, Too T, Miyawaki S et al (1987) Preliminary diagnostic criteria for classification of mixed connective tissue disease. In: Kasukawa R, Sharp GC (eds) Mixed connective tissue diseases and anti-nuclear antibodies. Elsevier, Amsterdam, pp 41–47Google Scholar
  52. 52.
    Alarcon-Segovia D, Villareal M (1987) Classification and diagnostic criteria for mixed connective tissue disease. In: Kasukawa R, Sharp GC (eds) Mixed connective tissue diseases and anti-nuclear antibodies. Elsevier, Amsterdam, pp 33–40Google Scholar
  53. 53.
    Cappelli S, Bellando Randone S, Martinović D, Tamas MM, Pasalić K, Allanore Y, Mosca M, Talarico R, Opris D, Kiss CG, Tausche AK, Cardarelli S, Riccieri V, Koneva O, Cuomo G, Becker MO, Sulli A, Guiducci S, Radić M, Bombardieri S, Aringer M, Cozzi F, Valesini G, Ananyeva L, Valentini G, Riemekasten G, Cutolo M, Ionescu R, Czirják L, Damjanov N, Rednic S, Matucci Cerinic M (2012) “To be or not to be,” ten years after: evidence for mixed connective tissue disease as a distinct entity. Semin Arthritis Rheum 41:589–598Google Scholar
  54. 54.
    Habets WJ, de Rooij DJ, Salden MH et al (1983) Antibodies against distinct nuclear matrix proteins are characteristic for mixed connective tissue disease. Clin Exp Immunol 54:265–276Google Scholar
  55. 55.
    Mosca M (2014) Mixed connective tissue diseases: new aspects of clinical picture, prognosis and pathogenesis. Isr Med Assoc J 16(11):725–726Google Scholar
  56. 56.
    Nimelstein SH, Brody ST, McShane D, Holman HR (1980) Mixed connective tissue disease: a subsequent evaluation of the original 25 patients. Medicine 59:239–248Google Scholar
  57. 57.
    Burdt MA, Hoffman RW, Deutscher SL, Wang GS, Johnson JC, Sharp GC (1999) Long-term outcome in mixed connective tissue disease. Arthritis Rheum 42:899–909Google Scholar
  58. 58.
    Hajas A, Szodoray P, Nakken B, Gaal J, Zöld E, Laczik R, Demeter N, Nagy G, Szekanecz Z, Zeher M, Szegedi G, Bodolay E (2013) Clinical course prognosis, and causes of death in mixed connective tissue diseases. J Rheumatol 40:1134–1142Google Scholar
  59. 59.
    Tani C, Carli L, Vagnani S, Talarico R, Baldini C, Mosca M, Bombardieri S (2014) The diagnosis and classification of mixed connective tissue disease. J Autoimmun 48-49:46–49Google Scholar
  60. 60.
    Jennette JC, Falk RJ, Bacon PA, Basu N, Cid MC, Ferrario F, Flores-Suarez LF, Gross WL, Guillevin L, Hagen EC, Hoffman GS, Jayne DR, Kallenberg CG, Lamprecht P, Langford CA, Luqmani RA, Mahr AD, Matteson EL, Merkel PA, Ozen S, Pusey CD, Rasmussen N, Rees AJ, Scott DG, Specks U, Stone JH, Takahashi K, Watts RA (2013) 2012 revised International Chapel Hill Consensus Conference Nomenclature of Vasculitides. Arthritis Rheum 65(1):1–11Google Scholar
  61. 61.
    Mavrogeni S, Markousis-Mavrogenis G, Kolovou G (2014) Cardiovascular magnetic resonance for evaluation of heart involvement in ANCA-associated vasculitis. A luxury or a valuable diagnostic tool? Inflamm Allergy Drug Targets 13:305–311Google Scholar
  62. 62.
    Di Carli MF, Murthy VL (2011) Cardiac PET/CT for the evaluation of known or suspected coronary artery disease. Radiographics. 31(5):1239–1254Google Scholar
  63. 63.
    Mavrogeni S, Markousis-Mavrogenis G, Koutsogeorgopoulou L, Kolovou G (2017) Cardiovascular magnetic resonance imaging: clinical implications in the evaluation of connective tissue diseases. J Inflamm Res 10:55–61Google Scholar
  64. 64.
    Mavrogeni S, Apostolou D, Argyriou P, Velitsista S, Papa L, Efentakis S, Vernardos E, Kanoupaki M, Kanoupakis G, Manginas A (2017) T1 and T2 mapping in cardiology: “mapping the obscure object of desire”. Cardiology. 138(4):207–217Google Scholar
  65. 65.
    Greulich S, Mayr A, Kitterer D, Latus J, Henes J, Vecchio F, Kaesemann P, Patrascu A, Greiser A, Groeninger S, Romeo F, Braun N, Alscher MD, Sechtem U, Mahrholdt H (2017) Advanced myocardial tissue characterisation by a multi-component CMR protocol in patients with rheumatoid arthritis. Eur Radiol 27(11):4639–4649Google Scholar
  66. 66.
    Messroghli DR, Moon JC, Ferreira VM, Grosse-Wortmann L, He T, Kellman P, Mascherbauer J, Nezafat R, Salerno M, Schelbert EB, Taylor AJ, Thompson RB, Ugander M, van Heeswijk RB, Friedrich MG (2018) Correction to: Clinical recommendations for cardiovascular magnetic resonance mapping of T1, T2, T2* and extracellular volume: a consensus statement by the Society for Cardiovascular Magnetic Resonance (SCMR) endorsed by the European Association for Cardiovascular Imaging (EACVI). J Cardiovasc Magn Reson 20(1):9Google Scholar
  67. 67.
    Kobayashi H, Kobayashi Y, Yokoe I, Akashi Y, Takei M, Giles JT (2017) Magnetic resonance imaging-detected myocardial inflammation and fibrosis in rheumatoid arthritis: associations with disease characteristics and N-terminal pro-brain natriuretic peptide levels. Arthritis Care Res 69(9):1304–1311Google Scholar
  68. 68.
    Kobayashi Y, Jon T, Giles JT, Hirano M, Yokoe I, Nakajima Y, Bathon JM, Lima JAC, H. (2010) Assessment of myocardial abnormalities in rheumatoid arthritis using a comprehensive cardiac magnetic resonance approach: a pilot study. Arthritis Res Ther 12(5):R171Google Scholar
  69. 69.
    Ntusi NAB, Piechnik SK, Francis JM, Ferreira VM, Matthews PM, Robson MD, Wordsworth PB, Neubauer S, Karamitsos TD (2015) Diffuse myocardial fibrosis and inflammation in rheumatoid arthritis: insights from CMR T1 mapping. JACC Cardiovasc Imaging 8(5):526–536Google Scholar
  70. 70.
    Bradham W, Ormseth MJ, Elumogo C, Palanisamy S, Liu CY, Lawson MA, Soslow JH, Kawel-Boehm N, Bluemke DA, Stein CM (2018) Absence of fibrosis and inflammation by cardiac magnetic resonance imaging in rheumatoid arthritis patients with low to moderate disease activity. J Rheumatol 45(8):1078–1084Google Scholar
  71. 71.
    Mavrogeni S, Koutsogeorgopoulou L, Markousis-Mavrogenis G, Bounas A, Tektonidou M, Lliossis SC, Daoussis D, Plastiras S, Karabela G, Stavropoulos E, Katsifis G, Vartela V, Kolovou G (2018) Cardiovascular magnetic resonance detects silent heart disease missed by echocardiography in systemic lupus erythematosus. Lupus 27(4):564–571Google Scholar
  72. 72.
    Puntmann VO, D’Cruz D, Smith Z, Pastor A, Choong P, Voigt T, Carr-White G, Sangle S, Schaeffter T, Nagel E (2013) Native myocardial T1mapping by cardiovascular magnetic resonance imaging in subclinical cardiomyopathy in patients with systemic lupus erythematosus. Circ Cardiovasc Imaging 6(2):295–301Google Scholar
  73. 73.
    Hinojar R, Foote L, Sangle S, Marber M, Mayr M, Carr-White G, D’Cruz D, Nagel E, Puntmann VO (2016) Native T1 and T2 mapping by CMR in lupus myocarditis: disease recognition and response to treatment. Int J Cardiol 222:717–726Google Scholar
  74. 74.
    Zhang Y, Corona-Villalobos CP, Kiani AN, Eng J, Kamel IR, Zimmerman SL, Petri M (2015) Myocardial T2 mapping by cardiovascular magnetic resonance reveals subclinical myocardial inflammation in patients with systemic lupus erythematosus. Int J Cardiovasc Imaging 31(2):389–397Google Scholar
  75. 75.
    Mavrogeni SI, Schwitter J, Gargani L, Pepe A, Monti L, Allanore Y, Matucci-Cerinic M (2017) Cardiovascular magnetic resonance in systemic sclerosis: “pearls and pitfalls”. Semin Arthritis Rheum 47(1):79–85Google Scholar
  76. 76.
    Mavrogeni S, Sfikakis PP, Dimitroulas T, Koutsogeorgopoulou L, Karabela G, Katsifis G, Stavropoulos E, Gialafos E, Spiliotis G, Kolovou G, Kitas GD (2015) Imaging patterns of cardiovascular involvement in mixed connective tissue disease evaluated by cardiovascular magnetic resonance. Inflamm Allergy Drug Targets 14(2):111–116Google Scholar
  77. 77.
    Mavrogeni S, Bratis K, Koutsogeorgopoulou L, Karabela G, Savropoulos E, Katsifis G, Raftakis J, Markousis-Mavrogenis G, Kolovou G (2017) Myocardial perfusion in peripheral Raynaud’s phenomenon. Evaluation using stress cardiovascular magnetic resonance. Int J Cardiol 228:444–448Google Scholar
  78. 78.
    Mavrogeni S, Dimitroulas T, Chatziioannou SN, Kitas G (2013) The role of multimodality imaging in the evaluation of Takayasu arteritis. Semin Arthritis Rheum 42(4):401–412Google Scholar
  79. 79.
    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 (2017) T1 and T2 mapping for evaluation of myocardial involvement in patients with ANCA-associated vasculitides. J Cardiovasc Magn Reson 19(1):6Google Scholar
  80. 80.
    Noutsias M, Seeberg B, Schultheiss HP, Kühl U (1999) Expression of cell adhesion molecules in dilated cardiomyopathy: evidence for endothelial activation in inflammatory cardiomyopathy. Circulation 99(16):2124–2131Google Scholar
  81. 81.
    Gutberlet M, Spors B, Thoma T, Bertram H, Denecke T, Felix R, Noutsias M, Schultheiss HP, Kühl U (2008) Suspected chronic myocarditis at cardiac MR: diagnostic accuracy and association with immunohistologically detected inflammation and viral persistence. Radiology 246(2):401–409Google Scholar
  82. 82.
    Mavrogeni SI, Sfikakis PP, Dimitroulas T, Koutsogeorgopoulou L, Katsifis G, Markousis-Mavrogenis G, Kolovou G, Kitas GD (2018) Can cardiovascular magnetic resonance prompt early cardiovascular/rheumatic treatment in autoimmune rheumatic diseases? Current practice and future perspectives. Rheumatol Int 38:949–958Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Sophie I. Mavrogeni
    • 1
    Email author
  • George Markousis-Mavrogenis
    • 1
  • Loukia Koutsogeorgopoulou
    • 2
  • Theodoros Dimitroulas
    • 3
  • Vasiliki Vartela
    • 1
  • Angelos Rigopoulos
    • 4
  • Michel Noutsias
    • 4
  • Genovefa Kolovou
    • 1
  1. 1.Onassis Cardiac Surgery CenterAthensGreece
  2. 2.Deparment PathophysiologyLaikon HospitalAthensGreece
  3. 3.Deparment of RheumatologyAristotle University of ThessalonikiThessalonikiGreece
  4. 4.Mid-German Heart Center, Department of Internal Medicine III (KIM-III), Division of Cardiology, Angiology and Intensive Medical Care, University Hospital HalleMartin-Luther-University Halle-WittenbergHalle (Saale)Germany

Personalised recommendations