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Current Cardiology Reviews

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ISSN (Print): 1573-403X
ISSN (Online): 1875-6557

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Review Article

Combined Brain/Heart Magnetic Resonance Imaging in Systemic Lupus Erythematosus

Author(s): Sophie Mavrogeni*, Loukia Koutsogeorgopoulou, Theodoros Dimitroulas, George Markousis-Mavrogenis, Kyriaki Boki, Gikas Katsifis, Vasiliki Vartela, Cees G. Kallenberg, Genovefa Kolovou and George Kitas

Volume 16, Issue 3, 2020

Page: [178 - 186] Pages: 9

DOI: 10.2174/1573403X15666190801122105

Price: $65

Abstract

Cardiovascular Disease (CVD) in Systemic Lupus Erythematosus (SLE) and Neuropsychiatric SLE (NPSLE) has an estimated prevalence of 50% and 40%, respectively and both constitute major causes of death among SLE patients. In this review, a combined brain/heart Magnetic Resonance Imaging (MRI) for SLE risk stratification has been proposed.

The pathophysiologic background of NPSLE includes microangiopathy, macroscopic infarcts and accelerated atherosclerosis. Classic brain MRI findings demonstrate lesions suggestive of NPSLE in 50% of the NPSLE cases, while advanced MRI indices can detect pre-clinical lesions in the majority of them, but their clinical impact still remains unknown. Cardiac involvement in SLE includes myo-pericarditis, valvular disease/endocarditis, Heart Failure (HF), coronary macro-microvascular disease, vasculitis and pulmonary hypertension. Classic and advanced Cardiovascular Magnetic Resonance (CMR) indices allow function and tissue characterization for early diagnosis and treatment follow-up of CVD in SLE.

Although currently, there are no clinical data supporting the combined use of brain/heart MRI in asymptomatic SLE, it may have a place in cases with clinical suspicion of brain/heart involvement, especially in patients at high risk for CVD/stroke such as SLE with antiphospholipid syndrome (SLE/APS), in whom concurrent cardiac and brain lesions have been identified. Furthermore, it may be of value in SLE with multi-organ involvement, NPSLE with concurrent cardiac involvement, and recent onset of arrhythmia and/or heart failure.

Keywords: Magnetic resonance imaging, systemic lupus erythematosus, brain lesions, cardiovascular disease, neuropsychiatric symptoms, cognitive dysfunction.

Graphical Abstract

[1]
Doria A, Iaccarino L, Ghirardello A, et al. Long-term prognosis and causes of death in systemic lupus erythematosus. Am J Med 2006; 119(8): 700-6.
[http://dx.doi.org/10.1016/j.amjmed.2005.11.034] [PMID: 16887417]
[2]
Cervera R, Abarca-Costalago M, Abramovicz D, et al. Systemic lupus erythematosus in Europe at the change of the millennium: lessons from the “Euro-Lupus Project”. Autoimmun Rev 2006; 5(3): 180-6.
[http://dx.doi.org/10.1016/j.autrev.2005.06.004] [PMID: 16483917]
[3]
Bertsias GK, Ioannidis JP, Aringer M, et al. EULAR recommendations for the management of systemic lupus erythematosus with neuropsychiatric manifestations: Report of a task force of the EULAR standing committee for clinical affairs. Ann Rheum Dis 2010; 69(12): 2074-82.
[http://dx.doi.org/10.1136/ard.2010.130476] [PMID: 20724309]
[4]
Luyendijk J, Steens SC, Ouwendijk WJ. Neuroimaging evidence of white matter inflammation in newly diagnosed systemic lupus erythematosus. Arthritis Rheum 2011; 63(3): 722-32.
[5]
Ramage AE, Fox PT, Brey RL. Neuroimaging evidence of white matter inflammation in newly diagnosed systemic lupus erythematosus. Arthritis Rheum 2011; 63(10): 3048-57.
[6]
Bortoluzzi A, Scire C, Bombardieri S. Development and validation of a new algorithm for attribution of neuropsychiatric events in systemic lupus erythematosus. Arthritis Rheum 2015; 54(5): 891-8.
[7]
The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 1999; 42(4): 599-608.
[http://dx.doi.org/10.1002/1529-0131(199904)42:4<599:AID-ANR2>3.0.CO;2-F] [PMID: 10211873]
[8]
Netto TM, Zimmermann N, Rueda-Lopes F. Neuropsychiatric lupus: Classification criteria in neuroimaging studies. Can J Neurol Sci 2013; 40(3): 284-91.
[9]
Ellis SG, Verity MA. Central nervous system involvement in systemic lupus erythematosus: A review of neuropathologic findings in 57 cases, 1955--1977. Semin Arthritis Rheum 1979; 8(3): 212-21.
[http://dx.doi.org/10.1016/S0049-0172(79)80009-8] [PMID: 424765]
[10]
Sibbitt WL Jr, Brooks WM, Kornfeld M, Hart BL, Bankhurst AD, Roldan CA. Magnetic resonance imaging and brain histopathology in neuropsychiatric systemic lupus erythematosus. Semin Arthritis Rheum 2010; 40(1): 32-52.
[http://dx.doi.org/10.1016/j.semarthrit.2009.08.005] [PMID: 19880162]
[11]
Sarbu MI, Salman-Monte TC, Muñoz PR, Lisbona MP, Bernabé MA, Carbonell J. Differences between clinical and laboratory findings in patients with recent diagnosis of SLE according to the positivity of anti-dsDNA by the Crithidia luciliae method. Lupus 2015; 24(11): 1198-203.
[http://dx.doi.org/10.1177/0961203315573852] [PMID: 25716418]
[12]
Fanouriakis A, Boumpas DT, Bertsias GK. Pathogenesis and treatment of CNS lupus. Curr Opin Rheumatol 2013; 25(5): 577-83.
[http://dx.doi.org/10.1097/BOR.0b013e328363eaf1] [PMID: 23836074]
[13]
Conti F, Alessandri C, Bompane D, et al. Autoantibody profile in systemic lupus erythematosus with psychiatric manifestations: A role for anti-endothelial-cell antibodies. Arthritis Res Ther 2004; 6(4): R366-72.
[http://dx.doi.org/10.1186/ar1198] [PMID: 15225372]
[14]
Omdal R, Brokstad K, Waterloo K, Koldingsnes W, Jonsson R, Mellgren SI. Neuropsychiatric disturbances in SLE are associated with antibodies against NMDA receptors. Eur J Neurol 2005; 12(5): 392-8.
[http://dx.doi.org/10.1111/j.1468-1331.2004.00976.x] [PMID: 15804272]
[15]
Ballocca F, D’Ascenzo F, Moretti C, et al. Predictors of cardiovascular events in patients with systemic lupus erythematosus (SLE): A systematic review and meta-analysis. Eur J Prev Cardiol 2015; 22(11): 1435-41.
[PMID: 25139772]
[16]
Bernatsky S, Boivin JF, Joseph L, et al. Mortality in systemic lupus erythematosus. Arthritis Rheum 2006; 54(8): 2550-7.
[http://dx.doi.org/10.1002/art.21955] [PMID: 16868977]
[17]
Gustafsson J, Gunnarsson I, Börjesson O, et al. Predictors of the first cardiovascular event in patients with systemic lupus erythematosus - a prospective cohort study. Arthritis Res Ther 2009; 11(6): R186.
[http://dx.doi.org/10.1186/ar2878] [PMID: 20003285]
[18]
Rosner S, Ginzler EM, Diamond HS, et al. A multicenter study of outcome in systemic lupus erythematosus. II. Causes of death. Arthritis Rheum 1982; 25(6): 612-7.
[http://dx.doi.org/10.1002/art.1780250602] [PMID: 7046757]
[19]
Petri M, Spence D, Bone LR, Hochberg MC. Coronary artery disease risk factors in the Johns Hopkins Lupus Cohort: Prevalence, recognition by patients, and preventive practices. Medicine (Baltimore) 1992; 71(5): 291-302.
[http://dx.doi.org/10.1097/00005792-199209000-00004] [PMID: 1522805]
[20]
Esdaile JM, Abrahamowicz M, Grodzicky T, et al. Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 2001; 44(10): 2331-7.
[http://dx.doi.org/10.1002/1529-0131(200110)44:10<2331:AID-ART395>3.0.CO;2-I] [PMID: 11665973]
[21]
Rahman P, Urowitz MB, Gladman DD, Bruce IN, Genest J Jr. Contribution of traditional risk factors to coronary artery disease in patients with systemic lupus erythematosus. J Rheumatol 1999; 26(11): 2363-8.
[PMID: 10555892]
[22]
Toloza SMA, Uribe AG, McGwin G Jr, et al. Systemic lupus erythematosus in a multiethnic US cohort (LUMINA). XXIII. Baseline predictors of vascular events. Arthritis Rheum 2004; 50(12): 3947-57.
[http://dx.doi.org/10.1002/art.20622] [PMID: 15593203]
[23]
Pons-Estel GJ, González LA, Zhang J, et al. Predictors of cardiovascular damage in patients with systemic lupus erythematosus: Data from LUMINA (LXVIII), a multiethnic US cohort. Rheumatology (Oxford) 2009; 48(7): 817-22.
[http://dx.doi.org/10.1093/rheumatology/kep102] [PMID: 19454606]
[24]
Borchers AT, Keen CL, Shoenfeld Y, Gershwin ME. Surviving the butterfly and the wolf: Mortality trends in systemic lupus erythematosus. Autoimmun Rev 2004; 3(6): 423-53.
[http://dx.doi.org/10.1016/j.autrev.2004.04.002] [PMID: 15351310]
[25]
Kasitanon N, Magder LS, Petri M. Predictors of survival in systemic lupus erythematosus. Medicine (Baltimore) 2006; 85(3): 147-56.
[http://dx.doi.org/10.1097/01.md.0000224709.70133.f7] [PMID: 16721257]
[26]
Urowitz MB, Gladman DD, Tom BD, Ibañez D, Farewell VT. Changing patterns in mortality and disease outcomes for patients with systemic lupus erythematosus. J Rheumatol 2008; 35(11): 2152-8.
[http://dx.doi.org/10.3899/jrheum.080214] [PMID: 18793004]
[27]
Ocampo-Piraquive V, Nieto-Aristizábal I, Cañas CA, Tobón GJ. Mortality in systemic lupus erythematosus: Causes, predictors and interventions. Expert Rev Clin Immunol 2018; 14(12): 1043-53.
[http://dx.doi.org/10.1080/1744666X.2018.1538789] [PMID: 30338717]
[28]
Anderson E, Nietert PJ, Kamen DL, Gilkeson GS. Ethnic disparities among patients with systemic lupus erythematosus in South Carolina. J Rheumatol 2008; 35(5): 819-25.
[PMID: 18381790]
[29]
Mikdashi J, Nived O. Measuring disease activity in adults with systemic lupus erythematosus: The challenges of administrative burden and responsiveness to patient concerns in clinical research. Arthritis Res Ther 2015; 17(1): 183.
[http://dx.doi.org/10.1186/s13075-015-0702-6] [PMID: 26189728]
[30]
Roldan CA, Gelgand EA, Qualls CR, Sibbitt WL Jr. Valvular heart disease is associated with nonfocal neuropsychiatric systemic lupus erythematosus. J Clin Rheumatol 2006; 12(1): 3-10.
[http://dx.doi.org/10.1097/01.rhu.0000200378.42836.7f] [PMID: 16484873]
[31]
Mavrogeni S, Kitas GD, Lamb HJ, et al. Combined brain and heart magnetic resonance imaging in systemic vasculitides: Fiction or real need? Clin Exp Rheumatol 2018; 36(2): 152-9.
[32]
Sibbitt WL Jr, Sibbitt RR, Griffey RH, Eckel C, Bankhurst AD. Magnetic resonance and computed tomographic imaging in the evaluation of acute neuropsychiatric disease in systemic lupus erythematosus. Ann Rheum Dis 1989; 48(12): 1014-22.
[http://dx.doi.org/10.1136/ard.48.12.1014] [PMID: 2619353]
[33]
Zardi EM, Taccone A, Marigliano B, Margiotta DP, Afeltra A. Neuropsychiatric systemic lupus erythematosus: Tools for the diagnosis. Autoimmun Rev 2014; 13(8): 831-9.
[http://dx.doi.org/10.1016/j.autrev.2014.04.002] [PMID: 24704869]
[34]
Castellino G, Govoni M, Giacuzzo S, Trotta F. Optimizing clinical monitoring of central nervous system involvement in SLE. Autoimmun Rev 2008; 7(4): 297-304.
[http://dx.doi.org/10.1016/j.autrev.2007.11.022] [PMID: 18295733]
[35]
Csépány T, Bereczki D, Kollár J, Sikula J, Kiss E, Csiba L. MRI findings in central nervous system systemic lupus erythematosus are associated with immunoserological parameters and hypertension. J Neurol 2003; 250(11): 1348-54.
[http://dx.doi.org/10.1007/s00415-003-0223-0] [PMID: 14648152]
[36]
Toledano P, Sarbu N, Espinosa G, Bargalló N, Cervera R. Neuropsychiatric systemic lupus erythematosus: Magnetic resonance imaging findings and correlation with clinical and immunological features. Autoimmun Rev 2013; 12(12): 1166-70.
[http://dx.doi.org/10.1016/j.autrev.2013.07.004] [PMID: 23851139]
[37]
Mikdashi J, Handwerger B. Predictors of neuropsychiatric damage in systemic lupus erythematosus: Data from the Maryland lupus cohort. Rheumatology (Oxford) 2004; 43(12): 1555-60.
[http://dx.doi.org/10.1093/rheumatology/keh384] [PMID: 15342927]
[38]
Wardlaw JM, Smith EE, Biessels GJ, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 2013; 12(8): 822-38.
[http://dx.doi.org/10.1016/S1474-4422(13)70124-8] [PMID: 23867200]
[39]
Wahlund LO, Barkhof F, Fazekas F, et al. A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke 2001; 32(6): 1318-22.
[http://dx.doi.org/10.1161/01.STR.32.6.1318] [PMID: 11387493]
[40]
Rovaris M, Inglese M, Viti B, et al. The contribution of fast-FLAIR MRI for lesion detection in the brain of patients with systemic autoimmune diseases. J Neurol 2000; 247(1): 29-33.
[http://dx.doi.org/10.1007/s004150050006] [PMID: 10701894]
[41]
Sanna G, Piga M, Terryberry JW, et al. Central nervous system involvement in systemic lupus erythematosus: Cerebral imaging and serological profile in patients with and without overt neuropsychiatric manifestations. Lupus 2000; 9(8): 573-83.
[http://dx.doi.org/10.1191/096120300678828695] [PMID: 11035431]
[42]
Jennings JE, Sundgren PC, Attwood J, McCune J, Maly P. Value of MRI of the brain in patients with systemic lupus erythematosus and neurologic disturbance. Neuroradiology 2004; 46(1): 15-21.
[http://dx.doi.org/10.1007/s00234-003-1049-2] [PMID: 14648006]
[43]
Appenzeller S, Pike GB, Clarke AE. Magnetic resonance imaging in the evaluation of central nervous system manifestations in systemic lupus erythematosus. Clin Rev Allergy Immunol 2008; 34(3): 361-6.
[http://dx.doi.org/10.1007/s12016-007-8060-z] [PMID: 18084729]
[44]
Katsumata Y, Harigai M, Kawaguchi Y, et al. Diagnostic reliability of magnetic resonance imaging for central nervous system syndromes in systemic lupus erythematosus: A prospective cohort study. BMC Musculoskelet Disord 2010; 11: 13.
[http://dx.doi.org/10.1186/1471-2474-11-13] [PMID: 20096132]
[45]
Appenzeller S, Vasconcelos Faria A, Li LM, Costallat LT, Cendes F. Quantitative magnetic resonance imaging analyses and clinical significance of hyperintense white matter lesions in systemic lupus erythematosus patients. Ann Neurol 2008; 64(6): 635-43.
[http://dx.doi.org/10.1002/ana.21483] [PMID: 19107986]
[46]
Castellino G, Padovan M, Bortoluzzi A, et al. Single photon emission computed tomography and magnetic resonance imaging evaluation in SLE patients with and without neuropsychiatric involvement. Rheumatology (Oxford) 2008; 47(3): 319-23.
[http://dx.doi.org/10.1093/rheumatology/kem354] [PMID: 18218648]
[47]
Ainiala H, Dastidar P, Loukkola J, et al. Cerebral MRI abnormalities and their association with neuropsychiatric manifestations in SLE: A population-based study. Scand J Rheumatol 2005; 34(5): 376-82.
[http://dx.doi.org/10.1080/03009740510026643] [PMID: 16234185]
[48]
Benedict RH, Shucard JL, Zivadinov R, Shucard DW. Neuropsychological impairment in systemic lupus erythematosus: A comparison with multiple sclerosis. Neuropsychol Rev 2008; 18(2): 149-66.
[http://dx.doi.org/10.1007/s11065-008-9061-2] [PMID: 18521755]
[49]
Petri M, Naqibuddin M, Carson KA, et al. Brain magnetic resonance imaging in newly diagnosed systemic lupus erythematosus. J Rheumatol 2008; 35(12): 2348-54.
[http://dx.doi.org/10.3899/jrheum.071010] [PMID: 18793003]
[50]
Doubal FN, Dennis MS, Wardlaw JM. Characteristics of patients with minor ischaemic strokes and negative MRI: A cross-sectional study. J Neurol Neurosurg Psychiatry 2011; 82(5): 540-2.
[http://dx.doi.org/10.1136/jnnp.2009.190298] [PMID: 20584742]
[51]
Sarbu N, Bargalló N, Cervera R. Advanced and conventional magnetic resonance imaging in neuropsychiatric lupus. F1000 Res 2015; 4: 162.
[52]
Karassa FB, Ioannidis JP, Boki KA, et al. Predictors of clinical outcome and radiologic progression in patients with neuropsychiatric manifestations of systemic lupus erythematosus. Am J Med 2000; 109(8): 628-34.
[http://dx.doi.org/10.1016/S0002-9343(00)00603-3] [PMID: 11099682]
[53]
Xu J, Cheng Y, Chai P, et al. White-matter volume reduction and the protective effect of immunosuppressive therapy in systemic lupus erythematosus patients with normal appearance by conventional magnetic resonance imaging. J Rheumatol 2010; 37(5): 974-86.
[http://dx.doi.org/10.3899/jrheum.090967] [PMID: 20231206]
[54]
Zivadinov R, Havrdová E, Bergsland N, et al. Thalamic atrophy is associated with development of clinically definite multiple sclerosis. Radiology 2013; 268(3): 831-41.
[http://dx.doi.org/10.1148/radiol.13122424] [PMID: 23613615]
[55]
Appenzeller S, Carnevalle AD, Li LM, Costallat LT, Cendes F. Hippocampal atrophy in systemic lupus erythematosus. Ann Rheum Dis 2006; 65(12): 1585-9.
[http://dx.doi.org/10.1136/ard.2005.049486] [PMID: 16439436]
[56]
Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G. Diffusion tensor MR imaging of the human brain. Radiology 1996; 201(3): 637-48.
[http://dx.doi.org/10.1148/radiology.201.3.8939209] [PMID: 8939209]
[57]
Le Bihan D. Looking into the functional architecture of the brain with diffusion MRI. Nat Rev Neurosci 2003; 4(6): 469-80.
[http://dx.doi.org/10.1038/nrn1119] [PMID: 12778119]
[58]
Schmidt-Wilcke T, Cagnoli P, Wang P, et al. Diminished white matter integrity in patients with systemic lupus erythematosus. Neuroimage Clin 2014; 5: 291-7.
[http://dx.doi.org/10.1016/j.nicl.2014.07.001] [PMID: 25161895]
[59]
Kozora E, Filley CM. Cognitive dysfunction and white matter abnormalities in systemic lupus erythematosus. J Int Neuropsychol Soc 2011; 17(3): 385-92.
[http://dx.doi.org/10.1017/S1355617711000191] [PMID: 21338548]
[60]
Zhang L, Harrison M, Heier LA, et al. Diffusion changes in patients with systemic lupus erythematosus. Magn Reson Imaging 2007; 25(3): 399-405.
[http://dx.doi.org/10.1016/j.mri.2006.09.037] [PMID: 17371731]
[61]
Lee SP, Wu CS, Hsieh LC, Cheung WK, Chou MC. Efficacy of magnetic resonance diffusion tensor imaging and three-dimensional fiber tractography in the detection of clinical manifestations of central nervous system lupus. Magn Reson Imaging 2014; 32(5): 598-603.
[http://dx.doi.org/10.1016/j.mri.2014.02.005] [PMID: 24629511]
[62]
Jones JT, DiFrancesco M, Zaal AI, et al. Childhood-onset lupus with clinical neurocognitive dysfunction shows lower streamline density and pairwise connectivity on diffusion tensor imaging. Lupus 2015; 24(10): 1081-6.
[http://dx.doi.org/10.1177/0961203315572718] [PMID: 25701565]
[63]
Bosma GP, Rood MJ, Huizinga TW, de Jong BA, Bollen EL, van Buchem MA. Detection of cerebral involvement in patients with active neuropsychiatric systemic lupus erythematosus by the use of volumetric magnetization transfer imaging. Arthritis Rheum 2000; 43(11): 2428-36.
[http://dx.doi.org/10.1002/1529-0131(200011)43:11<2428:AID-ANR9>3.0.CO;2-H] [PMID: 11083265]
[64]
Cagnoli P, Harris RE, Frechtling D, et al. Reduced Insular Glutamine and N-acetylaspartate in systemic lupus erythematosus: A single-voxel (1)H-MR spectroscopy study. Acad Radiol 2013; 20(10): 1286-96.
[http://dx.doi.org/10.1016/j.acra.2013.07.011] [PMID: 24029061]
[65]
Guillen-Del Castillo A, Alonso J, Martínez-Valle F, et al. Increased myo-inositol in parietal white and gray matter as a biomarker of poor prognosis in neuropsychiatric lupus: A case report. Lupus 2014; 23(10): 1073-8.
[http://dx.doi.org/10.1177/0961203314534303] [PMID: 25118052]
[66]
Sarbu N, López-Rueda A, Chirife O, Capurro S. CT-perfusion time-maps likely disclose the earliest imaging signs of posterior reversible encephalopathy syndrome (PRES). J Neuroradiol 2014; 41(2): 147-9.
[http://dx.doi.org/10.1016/j.neurad.2013.08.003] [PMID: 24075649]
[67]
Emmer BJ, van Osch MJ, Wu O, et al. Perfusion MRI in neuro-psychiatric systemic lupus erthemathosus. J Magn Reson Imaging 2010; 32(2): 283-8.
[http://dx.doi.org/10.1002/jmri.22251] [PMID: 20677252]
[68]
Zimny A, Szmyrka-Kaczmarek M, Szewczyk P, et al. In vivo evaluation of brain damage in the course of systemic lupus erythematosus using magnetic resonance spectroscopy, perfusion-weighted and diffusion-tensor imaging. Lupus 2014; 23(1): 10-9.
[http://dx.doi.org/10.1177/0961203313511556] [PMID: 24192079]
[69]
Wang PI, Cagnoli PC, McCune WJ, et al. Perfusion-weighted MR imaging in cerebral lupus erythematosus. Acad Radiol 2012; 19(8): 965-70.
[http://dx.doi.org/10.1016/j.acra.2012.03.023] [PMID: 22608862]
[70]
Mavrogeni S, Koutsogeorgopoulou L, Markousis-Mavrogenis G, et al. Cardiovascular magnetic resonance detects silent heart disease missed by echocardiography in systemic lupus erythematosus. Lupus 2018; 27(4): 564-71.
[http://dx.doi.org/10.1177/0961203317731533] [PMID: 28927316]
[71]
Mavrogeni SI, Kitas GD, Dimitroulas T, et al. Cardiovascular magnetic resonance in rheumatology: Current status and recommendations for use. Int J Cardiol 2016; 217: 135-48.
[http://dx.doi.org/10.1016/j.ijcard.2016.04.158] [PMID: 27179903]
[72]
Bellenger NG, Burgess MI, Ray SG, et al. Comparison of left ventricular ejection fraction and volumes in heart failure by echocardiography, radionuclide ventriculography and cardiovascular magnetic resonance; are they interchangeable? Eur Heart J 2000; 21(16): 1387-96.
[http://dx.doi.org/10.1053/euhj.2000.2011] [PMID: 10952828]
[73]
Zhang Y, Corona-Villalobos CP, Kiani AN, et al. Myocardial T2 mapping by cardiovascular magnetic resonance reveals subclinical myocardial inflammation in patients with systemic lupus erythematosus. Int J Cardiovasc Imaging 2015; 31(2): 389-97.
[http://dx.doi.org/10.1007/s10554-014-0560-3] [PMID: 25352245]
[74]
Mavrogeni S, Bratis K, Markussis V, et al. The diagnostic role of cardiac magnetic resonance imaging in detecting myocardial inflammation in systemic lupus erythematosus. Differentiation from viral myocarditis. Lupus 2013; 22(1): 34-43.
[http://dx.doi.org/10.1177/0961203312462265] [PMID: 23035042]
[75]
Mavrogeni SI, Sfikakis PP, Markousis-Mavrogenis G, et al. Cardiovascular magnetic resonance imaging pattern in patients with autoimmune rheumatic diseases and ventricular tachycardia with preserved ejection fraction. Int J Cardiol 2019; 284: 105-9.
[76]
Hinojar R, Foote L, Sangle S, 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.
[http://dx.doi.org/10.1016/j.ijcard.2016.07.182] [PMID: 27521546]
[77]
Lagan J, Schmitt M, Miller CA. Clinical applications of multi-parametric CMR in myocarditis and systemic inflammatory diseases. Int J Cardiovasc Imaging 2018; 34(1): 35-54.
[http://dx.doi.org/10.1007/s10554-017-1063-9] [PMID: 28130644]
[78]
Mavrogeni S, Bratis K, Koutsogeorgopoulou L, et al. Myocardial perfusion in peripheral Raynaud’s phenomenon. Evaluation using stress cardiovascular magnetic resonance. Int J Cardiol 2017; 228(228): 444-8.
[http://dx.doi.org/10.1016/j.ijcard.2016.11.242] [PMID: 27870974]
[79]
Ishimori ML, Martin R, Berman DS, et al. Myocardial ischemia in the absence of obstructive coronary artery disease in systemic lupus erythematosus. JACC Cardiovasc Imaging 2011; 4(1): 27-33.
[http://dx.doi.org/10.1016/j.jcmg.2010.09.019] [PMID: 21232700]
[80]
Böhm I. Novel approach to improve molecular imaging research: Correlation between macroscopic and molecular pathological findings in patients. Eur J Radiol 2011; 79(3): 365-8.
[http://dx.doi.org/10.1016/j.ejrad.2010.08.030] [PMID: 20863640]

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