Cardiovascular magnetic resonance in systemic sclerosis: “Pearls and pitfalls”

Seminars in Arthritis and Rheumatism

Volumn 47, Issue 1, 2017, Pages 79-85

  Mavrogeni, Sophie I ^a   Schwitter, Juerg ^b   Gargani, Luna ^c   Pepe, Alessia ^d   Monti, Lorenzo ^e   Allanore, Yannick ^f   Matucci Cerinic, Marco ^g,h  

^a ONASSIS CARDIAC SURGERY CENTER   (Greece)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c INSTITUTE OF CLINICAL PHYSIOLOGY   (Italy)

^d FONDAZIONE TOSCANA GABRIELE MONASTERIO   (Italy)

^e HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^f Institut Cochin   (France)

^g UNIVERSITY OF FLORENCE   (Italy)

^h AOUC   (Italy)

Author keywords

Cardiac catheterization; Cardiovascular magnetic resonance imaging; ECG; Echocardiography; Systemic sclerosis

Indexed keywords

GADOLINIUM;

ANEURYSM CLIP; ARTIFACT; ARTIFICIAL HEART PACEMAKER; CARDIOVASCULAR DISEASE; CARDIOVASCULAR MAGNETIC RESONANCE; CARDIOVASCULAR SYSTEM EXAMINATION; CONTRAST ENHANCEMENT; DIAGNOSTIC ACCURACY; DIAGNOSTIC ERROR; DIAGNOSTIC IMAGING; GOLD STANDARD; HEART EJECTION FRACTION; HEART MUSCLE FIBROSIS; HEART VENTRICLE VOLUME; HUMAN; HYPERTENSION; IMAGE ANALYSIS; IMPLANTABLE CARDIOVERTER DEFIBRILLATOR; KIDNEY FUNCTION; MYOCARDITIS; PRIORITY JOURNAL; PULMONARY HYPERTENSION; REPRODUCIBILITY; REVIEW; SENSITIVITY AND SPECIFICITY; SYSTEMIC SCLEROSIS; VALVULAR HEART DISEASE; CARDIAC MUSCLE; COMPLICATION; FEMALE; FIBROSIS; HEART VOLUME; MALE; MORTALITY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY;

CARDIAC VOLUME; CARDIOVASCULAR DISEASES; FEMALE; FIBROSIS; HUMANS; HYPERTENSION, PULMONARY; MAGNETIC RESONANCE IMAGING; MALE; MYOCARDIUM; SCLERODERMA, SYSTEMIC;

EID: 85019583015     PISSN: 00490172     EISSN: 1532866X     Source Type: Journal    
DOI: 10.1016/j.semarthrit.2017.03.020     Document Type: Review

References (83)

1. Steen, V.D., Medsger, T.A. Jr, Severe organ involvement in systemic sclerosis with diffuse scleroderma. Arthritis Rheum 43 (2000), 2437–2444.
2. Ferri, C., Valentini, G., Cozzi, F., Sebastiani, M., Michelassi, C., La Montagna, G., et al. Systemic sclerosis: demographic, clinical, and serologic features and survival in 1,012 Italian patients. Medicine 81 (2002), 139–153.
3. Follansbee, W.P., Curtiss, E.I., Medsger, T.A. Jr, Steen, V.D., Uretsky, B.F., Owens, G.R., et al. Physiologic abnormalities of cardiac function in progressive systemic sclerosis with diffuse scleroderma. N Engl J Med 310 (1984), 142–148.
4. Kahan, A., Devaux, J.Y., Amor, B., Menkès, C.J., Weber, S., Nitenberg, A., et al. Nifedipine and thallium-201 myocardial perfusion in progressive systemic sclerosis. N Engl J Med 314 (1986), 1397–1402.
5. Candell-Riera, J., Armadans-GilL, Simeon, C.P., Castell-Conesa, J., Fonollosa-Pla, V., García-del-Castillo, H., et al. Comprehensive noninvasive assessment of cardiac involvement in limited systemic sclerosis. Arthritis Rheum 39 (1996), 1138–1145.
6. Kahan, A., Allanore, Y., Primary myocardial involvement in systemic sclerosis. Rheumatology 45:Suppl. 4 (2006), iv14–iv17.
7. Rodríguez-Reyna, T.S., Morelos-Guzman, M., Hernández-Reyes, P., Montero-Duarte, K., Martínez-Reyes, C., Reyes-Utrera, C., et al. Assessment of myocardial fibrosis and microvascular damage in systemic sclerosis by magnetic resonance imaging and coronary angiotomography. Rheumatology (Oxford) 54 (2015), 647–654.
8. Steen, V., The heart in systemic sclerosis. Curr Rheumatol Rep 6 (2004), 137–140.
9. Ioannidis, J.P., Vlachoyiannopoulos, P.G., Haidich, A.B., Medsger, T.A. Jr, Lucas, M., Michet, C.J., et al. Mortality in systemic sclerosis: an international meta-analysis of individual patient data. Am J Med 118 (2005), 2–10.
10. Steen, V.D., Medsger, T.A., Changes in causes of death in systemic sclerosis, 1972–2002. Ann Rheum Dis 66 (2007), 940–944.
11. Allanore, Y., Meune, C., Kahan, A., Systemic sclerosis and cardiac dysfunction: evolving concepts and diagnostic methodologies. Curr Opin Rheumatol 20 (2008), 697–702.
12. 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 68 (2009), 1878–1884.
13. Mavrogeni, S.I., Bratis, K., Karabela, G., Spiliotis, G., Wijk, Kv, Hautemann, D., et al. Cardiovascular magnetic resonance imaging clarifies cardiac pathophysiology in early, asymptomatic diffuse systemic sclerosis. Inflamm Allergy Drug Targets 14 (2015), 29–36.
14. Mavrogeni, S., Karabela, G., Koutsogeorgopoulou, L., Stavropoulos, E., Katsifis, G., Plastiras, S.C., et al. Pseudo-infarction pattern in diffuse systemic sclerosis. Evaluation using cardiovascular magnetic resonance. Int J Cardiol 214 (2016), 465–468.
15. Follansbee, W.P., Zerbe, T.R., Medsger, T.A. Jr, Cardiac and skeletal muscle disease in systemic sclerosis (scleroderma): a high risk association. Am Heart J 125 (1993), 194–203.
16. Hegedus, I., Czirjak, L., Left ventricular wall motion abnormalities in 80 patients with systemic sclerosis. Clin Rheumatol 14 (1995), 161–164.
17. Valentini, G., Vitale, D.F., Giunta, A., Maione, S., Gerundo, G., Arnese, M., et al. Diastolic abnormalities in systemic sclerosis: evidence for associated defective cardiac functional reserve. Ann Rheum Dis 55 (1996), 455–460.
18. Maron, B.A., Independence day: separating right ventricular function from pulmonary arterial hypertension in systemic sclerosis. Circulation 133:24 (2016), 2345–2347.
19. Valenzuela, A., Nandagopal, S., Steen, V.D., Chung, L., Monitoring and diagnostic approaches for pulmonary arterial hypertension in patients with systemic sclerosis. Rheum Dis Clin North Am 41 (2015), 489–506.
20. Diethelm, L., Dery, R., Lipton, M.J., Higgins, C.B., Atrial-level shunts: sensitivity and specificity of MR in diagnosis. Radiology. 162 (1987), 181–186.
21. Mavrogeni, S.I., Markussis, Vyron, Kaklamanis, L., Tsiapras, D., Paraskevaidis, I., Karavolias, G., et al. A comparison of magnetic resonance imaging and cardiac biopsy in the evaluation of heart iron overload in patients with [beta]-thalassemia major. Eur J Haematol 75 (2005), 241–247.
22. Higgins, C.B., Byrd, B.F., Stark, D., Lim, T.H., Kircher, B., Pflugfelder, P., et al. Diagnostic accuracy and estimation of the severity of valvular regurgitation from the signal void on cine magnetic resonance imaging. Am Heart J 118 (1989), 760–767.
23. Masui, T., Finck, S., Higgins, C.B., Constrictive pericarditis and restrictive cardiomyopathy: evaluation with MR imaging. Radiology. 182 (1992), 369–373.
24. Nienaber, C.A., von Kodolitsch, Y., Nicholas, V., Siglow, V., Piepho, A., Brockhoff, C., et al. The diagnosis of thoracic aortic dissection by noninvasive imaging procedures. N Engl J Med 328 (1993), 1–9.
25. Kim, W.Y., Danias, P.G., Stuber, M., Flamm, S.D., Plein, S., Nagel, E., et al. Coronary magnetic resonance angiography for the detection of coronary stenosis. N Engl J Med 345 (2001), 1863–1869.
26. Manning, W.J., Li, W., Edelman, R.R., A preliminary report comparing magnetic resonance coronary angiography with conventional angiography. N Engl J Med 328 (1993), 828–832.
27. Post, J.C., van Rossum, A.C., Bronzwaer, J.G., de Cock, C.C., Hofman, M.B., Valk, J., et al. Magnetic resonance angiography of anomalous coronary arteries: a new gold standard for delineating the proximal course?. Circulation 92 (1995), 3163–3171.
28. Mavrogeni, S., Papadopoulos, G., Douskou, M., Kaklis, S., Seimenis, I., Baras, I., et al. Magnetic resonance angiography is equivalent to x-ray coronary angiography for the evaluation of the coronary arteries in Kawasaki disease. J Am Coll Cardiol 43 (2004), 649–652.
29. Mavrogeni, S., Papadopoulos, G., Douskou, M., Kaklis, S., Seimenis, I., Varlamis, G., et al. Magnetic resonance angiography, function and viability evaluation in patients with Kawasaki disease. J Cardiovasc Magn Reson 8 (2006), 493–498.
30. Mavrogeni, S., Manoussakis, M.N., Karagiorga, T.C., Douskou, M., Panagiotakos, D., Bournia, V., et al. Detection of coronary artery lesions and myocardial necrosis by magnetic resonance in systemic necrotizing vasculitides. Arthritis Rheum. 61 (2009), 1121–1129.
31. Kwong, R.Y., Chan, A.K., Brown, K.A., Chan, C.W., Reynolds, H.G., Tsang, S., et al. Impact of unrecognized myocardial scar detected by cardiac magnetic resonance imaging on event-free survival in patients presenting with signs or symptoms of coronary artery disease. Circulation 113 (2006), 2733–2743.
32. Friedrich, M.G., Sechtem, U., Schulz-Menger, J., Holmvang, G., Alakija, P., Cooper, L.T., et al. Cardiovascular magnetic resonance in myocarditis: a JACC White Paper. J Am Coll Cardiol 53 (2009), 1475–1487.
33. Schwitter, J., Wacker, C.M., van Rossum, A.C., 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 29 (2008), 480–489.
34. Schalla, S., Nagel, E., Lehmkuhl, H., Klein, C., Bornstedt, A., Schnackenburg, B., et al. Comparison of magnetic resonance real-time imaging of LV function with conventional magnetic resonance imaging and echocardiography. Am J Cardiol 87 (2001), 95–99.
35. Bottini, P.B., Carr, A.A., Prisant, M., et al. Magnetic resonance imaging compared to echo/phy to assess LV MASS in the hypertensive patient. Am J Hypertension 8 (1995), 221–826.
36. Jeuthe, S., Wassilew, K., O H-Ici, D., da Silva, T.F., Münch, F., Berger, F., et al. Myocardial T1 maps reflect histological findings in acute and chronic stages of myocarditis in a rat model. J Cardiovasc Magn Reson, 18, 2016, 19.
37. Pieroni, M., De Santis, M., Zizzo, G., Bosello, S., Smaldone, C., Campioni, M., et al. Recognizing and treating myocarditis in recent-onset systemic sclerosis heart disease: potential utility of immunosuppressive therapy in cardiac damage progression. Semin Arthritis Rheum 43 (2014), 526–535.
38. Ntusi, N.A., Piechnik, S.K., Francis, J.M., Ferreira, V.M., Rai, A.B., Matthews, P.M., 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, 16, 2014, 21.
39. Chopra, H., Arangalage, D., Bouleti, C., Zarka, S., Fayard, F., Chillon, S., et al. Prognostic value of the infarct- and non-infarct like patterns and cardiovascular magnetic resonance parameters on long-term outcome of patients after acute myocarditis. Int J Cardiol 212 (2016), 63–69.
40. Pöyhönen, P., Holmström, M., Kivistö S., Hänninen, H., Late gadolinium enhancement on CMR and sustained ventricular tachycardia predict severe cardiac inflammation. Acta Cardiol 69 (2014), 637–647.
41. Sandmeier, B., Jäger, V.K., Nagy, G., Carreira, P.E., Tzankov, A., Widuchowska, M., et al. Autopsy versus clinical findings in patients with systemic sclerosis in a case series from patients of the EUSTAR database. Clin Exp Rheumatol 33:4 Suppl. 91 (2015), S75–S79.
42. Mavrogeni, S.I., Kitas, G.D., Dimitroulas, T., Sfikakis, P.P., Seo, P., Gabriel, S., et al. Cardiovascular magnetic resonance in rheumatology: current status and recommendations for use. Int J Cardiol 217 (2016), 135–148.
43. Barison, A., Gargani, L., De Marchi, D., Aquaro, G.D., Guiducci, S., Picano, E., et al. Early myocardial and skeletal muscle interstitial remodelling in systemic sclerosis: insights from ex tracellular volume quantification using cardiovascular magnetic resonance. Eur Heart J Cardiovasc Imaging 16 (2015), 74–80.
44. Khouzam, R.N., D'Cruz, I.A., Arroyo, M., Minderman, D., Systemic scleroderma with moderate to severe mitral regurgitation: unusual three-dimensional echocardiographic features. Can J Cardiol, 24, 2008, 152.
45. Ferrari, G., Pratali, S., Pucci, A., Bortolotti, U., Aortic valve replacement in systemic sclerosis. J Cardiovasc Med (Hagerstown) 16:Suppl. 1 (2015), S60–S61.
46. Penmetcha, M., Rosenbush, S.W., Harris, C.A., Cardiac valvular disease in scleroderma and systemic lupus erythematosus/scleroderma overlap associated with antiphospholipid antibodies. J Rheumatol. 23 (1996), 2171–2174.
47. Mukerjee, D. St, George, D., Coleiro, B., Knight, C., Denton, C.P., Davar, J., et al. Prevalence and outcome in systemic sclerosis associated pulmonary arterial hypertension: application of a registry approach. Ann Rheum Dis 62 (2003), 1088–1093.
48. Vonk Noordegraaf, A., Naeije, R., Right ventricular function in scleroderma-related pulmonary hypertension. Rheumatology (Oxford) 47:Suppl. 5 (2008), v42–v43.
49. Hassoun, P.M., The right ventricle in scleroderma (2013 Grover Conference Series). Pulm Circ 5 (2015), 3–14.
50. Benza, R., Biederman, R., Murali, S., Gupta, H., Role of cardiac magnetic resonance imaging in the management of patients with pulmonary arterial hypertension. J Am Coll Cardiol 52 (2008), 1683–1692.
51. Peacock, A.J., Vonk Noordegraaf, A., Cardiac magnetic resonance imaging in pulmonary arterial hypertension. Eur Respir Rev 22 (2013), 526–534.
52. Freed, B.H., GombergMaitland, M., Chandra, S., MorAvi, V., Rich, S., Archer, S.L., et al. Late gadolinium enhancement cardiovascular magnetic resonance predicts clinical worsening in patients with pulmonary hypertension. J Cardiovasc Magn Reson, 14, 2012, 11.
53. Kanski, M., Arheden, H., Wuttge, D.M., Bozovic, G., Hesselstrand, R., Ugander, M., Pulmonary blood volume indexed to lung volume is reduced in newly diagnosed systemic sclerosis compared to normals—a prospective clinical cardiovascular magnetic resonance study addressing pulmonary vascular changes. J Cardiovasc Magn Reson, 15, 2013, 86.
54. Peacock, A.J., Crawley, S., McLure, L., Blyth, K., Vizza, C.D., Poscia, R., et al. Changes in right ventricular function measured by cardiac magnetic resonance imaging in patients receiving pulmonary arterial hypertension-targeted therapy: the EURO-MR study. Circ Cardiovasc Imaging 7 (2014), 107–114.
55. Swift, A.J., Rajaram, S., Condliffe, R., Capener, D., Hurdman, J., Elliot, C.A., et al. Diagnostic accuracy of cardiovascular magnetic resonance imaging of right ventricular morphology and function in the assessment of suspected pulmonary hypertension results from the ASPIRE registry. J Cardiovasc Magn Reson, 14, 2014, 40.
56. Spruijt, O.A., Vissers, L., Bogaard, H.J., Hofman, M.B., Vonk-Noordegraaf, A., Marcus, J.T., Increased native T1-values at the interventricular insertion regions in precapillary pulmonary hypertension. Int J Cardiovasc Imaging 32 (2016), 451–459.
57. Hartnell, G.G., Spence, L., Hughes, L.A., Cohen, M.C., Saouaf, R., Buff, B., Safety of MR imaging in patients who have retained metallic materials after cardiac surgery. AJR Am J Roentgenol 168 (1997), 1157–1159.
58. Friedrich, M.G., Strohm, O., Kivelitz, D., Gross, W., Wagner, A., Schulz-Menger, J., et al. Behaviour of implantable coronary stents during magnetic resonance imaging. Int J Cardiovasc Intervent 2 (1999), 217–222.
59. Luechinger, R., Schwitter, J., Bruder, O., CMR update, 2nd ed., 2012, J. Schwitter, Switzerland, 32–52.
60. Mavrogeni, S.I., Poulos, G., Sfikakis, P.P., Kitas, G.D., Kolovou, G., Theodorakis, G., Is there a place for cardiovascular magnetic resonance conditional devices in systemic inflammatory diseases?. Expert Rev Cardiovasc Ther 14 (2016), 677–682.
61. Schwitter, J., Gold, M.R., Al Fagih, A., Lee, S., Peterson, M., Ciuffo, A., et al. Image quality of cardiac magnetic resonance imaging in patients with an implantable cardioverter defibrillator system designed for the magnetic resonance imaging environment. Circ Cardiovasc Imaging, 9(5), 2016 pii: e004025. http://dx.doi.org/10.1161/CIRCIMAGING.115.004025.
62. Schwitter, J., Kanal, E., Schmitt, M., Anselme, F., Albert, T., Hayes, D.L., et al. Impact of the Advisa MRI™ Pacing System on the diagnostic quality of cardiac MR images and contraction patterns of cardiac muscle during scans: advisa MRI randomized clinical multicenter study results. Heart Rhythm 10 (2013), 864–872.
63. Thomsen, H.S., Morcos, S.K., Torsten, A., Bellin, M.-F., Bertolotto, M., Bongartz, Georg, et al. Nephrogenic systemic fibrosis and gadolinium-based contrastmedia: updated ESUR Contrast Medium Safety Committee guidelines. Eur Radiol 23 (2013), 307–318.
64. Piccini, D., Feng, L., Bonanno, G., Coppo, S., Yerly, J., Lim, R., et al. Four-dimensional respiratory motion-resolved whole-heart coronary MRA. Magn Reson Med, 2016.
65. Monney, P., Piccini, D., Rutz, T., Vincenti, G., Coppo, S., Koestner, S., et al. Single centre experience of the application of self navigated 3D whole heart CMR for the assessment of cardiac anatomy in congenital heart disease. J Cardiovasc Magn Reson, 17, 2015, 55.
66. Coppo, S., Piccini, D., Bonanno, G., Chaptinel, J., Vincenti, G., Feliciano, H., et al. Free-running 4D whole-heart self-navigated golden angle MRI: initial results. Magn Reson Med 74 (2014), 1306–1316.
67. Kellman, P., Chefd'hotel, C., Lorenz, C.H., Mancini, C., Arai, A.E., McVeigh, E.R., High spatial and temporal resolution cardiac cine MRI from retrospective reconstruction of data acquired in real time using motion correction and resorting. Magn Reson Med 62 (2009), 1557–1564.
68. 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 222 (2016), 717–726.
69. Kiefer B, Grassner J, Hausman R. Image acquisition in a second with half Fourier acquisition single-shot turbo spin-echo. In: Proceedings of society for magnetic resonance; 1994.
70. Atkinson, D.J., Burstein, D., Edelman, R.R., First-pass cardiac perfusion: evaluation with ultrafast MR imaging. Radiology 174:3 Pt 1 (1990), 757–762.
71. Schwitter, J., Arai, A., Imaging: assessment of cardiac ischaemia and viability: role of cardiovascular magnetic resonance. Eur Heart J 32 (2011), 799–809.
72. Plein, S., Kozerke, S., Suerder, D., Luescher, T.F., Greenwood, J.P., Boesiger, P., et al. High spatial resolution myocardial perfusion cardiac magnetic resonance for the detection of coronary artery disease. Eur Heart J 29 (2008), 2148–2155.
73. Simonetti, O.P., Kim, R.J., Fieno, D.S., Hillenbrand, H.B., Wu, E., Bundy, J.M., et al. An improved MR imaging technique for the visualization of myocardial infarction. Radiology 218 (2001), 215–223.
74. Kellman, P., Arai, A.E., McVeigh, E.R., Aletras, A.H., Phase-sensitive inversion recovery for detecting myocardial infarction using gadolinium-delayed hyperenhancement. Magn Reson Med 47 (2002), 372–383.
75. Locca D, Bucciarelli-Ducci C, Lyne J, Chapparo M, Ferrante G, O'Hanlon R, et al. Rapid assessment of myocardial scar and viability in ischemic heart disease: a cardiovascular magnetic resonance study. In: Proceedings of Society for Cardiovascular Magnetic Resonance; 2009. p.154–7.
76. Sechtem, U., Pflugfelder, P.W., Gould, R.G., Cassidy, M.M., Higgins, C.B., Measurement of right and left ventricular volumes in healthy individuals with cine MR imaging. Radiology 163 (1987), 697–702.
77. Plein, S., Bloomer, T.N., Ridgway, J.P., Jones, T.R., Bainbridge, G.J., Sivananthan, M.U., Steady-state free precession magnetic resonance imaging of the heart: comparison with segmented k-space gradient-echo imaging. J Magn Reson Imaging 14 (2001), 230–236, 10.1002/jmri.1178.
78. Barkhausen, J., Ruehm, S.G., Goyen, M., Buck, T., Laub, G., Debatin, J.F., MR evaluation of ventricular function: true fast imaging with steady-state precession versus fast low-angle shot cine MR imaging: feasibility study. Radiology 219 (2001), 264–269.
79. Thiele, H., Nagel, E., Paetsch, I., Schnackenburg, B., Bornstedt, A., Kouwenhoven, M., et al. Functional cardiac MR imaging with steady-state free precession (SSFP) significantly improves endocardial border delineation without contrast agents. J Magn Reson Imaging 14 (2001), 362–367.
80. Vincenti, G., Monney, P., Chaptinel, J., Rutz, T., Coppo, S., Zenge, M.O., et al. Compressed sensing single-breathhold multi-slice magnetic resonance for fast quantification of left ventricular function, volumes, and mass. J Am Coll Cardiol Img 7 (2014), 882–892.
81. Nayler, G.L., Firmin, D.N., Longmore, D.B., Blood flow imaging by cine magnetic resonance. J Comput Assist Tomogr 10 (1986), 715–722.
82. Moran, P.R., A flow velocity zeugmatographic interlace for NMR imaging in humans. Magn Reson Imaging 1 (1982), 197–203.
83. VanDijk, P., Direct cardiac NMR imaging of heart wall and blood flow velocity. J Comput Assist Tomogr 8 (1984), 429–436.