Возможности магнитно-резонансной томографии сердца с контрастированием в диагностике миокардита различно- го клинического течения
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Stukalova O.V., Gupalo E.M., Chumachenko P.V., et al. The value of cardiovascular magnetic resonance in myocarditis with different clinical presentation. Therapeutic Archive. 2019; 91 (4): 28–36. DOI: 10.26442/00403660.2019.04.000078
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Материалы и методы. В исследование включено 79 пациентов. В группу I вошли 11 больных (8 мужчин и 3 женщины, средний возраст 32,8±11,1 года), госпитализированных с диагнозом «острый коронарный синдром», при этом в ходе обследования исключен острый инфаркт миокарда; группу II сформировали 48 больных (31 мужчина, 17 женщин, 43,1±12,7 года) с клинико-инструментальными признаками дилатационной кардиомиопатии (ДКМП); в группу III вошли 20 больных (12 мужчин и 8 женщин, 39,5±14,0 года) с эпизодами желудочковых тахикардий. Всем пациентам выполнена МРТ; 38 пациентам выполнена эндомиокардиальная биопсия (ЭМБ).
Результаты и обсуждение. По данным ЭМБ признаки активного миокардита выявлены у 10 (34,5%) больных группы II и у 3 (37,5%) больных группы III; признаки постмиокардитического кардиосклероза – соответственно у 8 (27,6%) и 3 (37,5%); минимальные изменения структуры миокарда – у 11 (37,9%) и 2 (25%). У 9 (81,9%) пациентов группы I данные МРТ позволили установить диагноз острого миокардита. Признаки активного воспаления по данным МРТ выявлены в миокарде 5 (10,4%) больных группы II и 7 (35%) больных группы III. У 22 (45,8%) пациентов группы II и 10 (50%) больных группы III данные МРТ соответствовали картине «постмиокардитического кардиосклероза». В 21 случае (43,8%) в группе II и 3 (15%) в группе III данные МРТ позволяли выявить признаки «активного миокардита» с чувствительностью 37,5% при специфичности 83,4%. В то же время при «постмиокардитическом кардиосклерозе» и «минимальных структурных изменениях миокарда» МРТ обладала высокими показателями чувствительности (70 и 71,5%) и специфичности (71,5 и 75% соответственно).
Заключение. МРТ обладает высокой диагностической значимостью у больных с инфарктоподобным течением миокардита. У пациентов с клиническим синдромом ДКМП или аритмиями чувствительность МРТ в выявлении активного миокардита низкая (37,5%) при высокой специфичности (83,4%). При постмиокардитическом кардиосклерозе и минимальных структурных изменениях миокарда применение МРТ является хорошей альтернативой ЭМБ.
Ключевые слова: миокардит, магнитно-резонансная томография сердца, эндомиокардиальная биопсия.
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Objective: to assess the diagnostic meaning of cardiac magnetic resonance imaging (CMR) in various clinical forms of myocarditis.
Materials and methods. 11 (8 men, mean age 32.8±11.1 years) patients (pts), hospitalized with suspected acute coronary syndrome, while an acute myocardial infarction was excluded during the examination (group I); 48 pts (31 men, 43.1±12.7 years), with clinical and instrumental signs of dilated cardiomyopathy (DCM) – group II; and 20 patients (12 men, 39.5±14 years), with episodes of ventricular tachycardia (group III) underwent cardiac magnetic resonance imaging (CMRI). In 38 patients endomyocardial biopsy (EMB) was performed.
Results and discussion. According to EMB, signs of active myocarditis were revealed in 10 (34.5%) group II pts and in 3 (37.5%) group III pts; signs of resolved myocarditis – in 8 (27.6%) patients in group II and in 3 (37.5%); minimal morphological changes – in 11 (37.9%) patients of group II and in 2 (25%) patients of group III. In 9 (81.9%) patients of group I MRI data allowed to establish the diagnosis of acute myocarditis. Signs of active inflammation from MRI data were detected in myocardium 5 (10.4%) in group II pts and 7 (35%) in group III pts. In 22 (45.8%) pts in group II and 10 (50%), CMR data corresponded to the picture of resolved myocarditis. In 21 (43.8%) cases of group II and 3 (15%) of group III, MRI revealed minimal structural changes. In pts with clinical and instrumental signs of DCM and/or ventricular tachycardia MRI allows to identify signs of "active myocarditis" with a sensitivity of 37.5% with a specificity of 83.4%. At the same time, in cases of resolved myocarditis and minimal morphological changes MRI has high sensitivity (70 and 71.5%) and specificity (71.5 and 75%, respectively).
Conclusion. CMR has high diagnostic significance in patients with infarct-like course of myocarditis. In patients with clinical syndrome of dilated cardiomyopathy or arrhythmias, the sensitivity of MRI in detecting active myocarditis is low (37.5%) with high specificity (83.4%). In cases of minimal structural changes in the myocardium and resolved inflammation, CMR is a good alternative to EMB.
Keywords: myocarditis, magnetic resonance imaging, endomyovascular biopsy.
2. Cooper LT Jr. Myocarditis. N Engl J Med. 2009 Apr 9;360(15):1526-38. doi: 10.1056/NEJMra0800028
3. Frustaci A, Chimenti C, Maseri A. Global bi-ventricular dysfunction in patients with symptomatic coronary artery disease may be caused by myocarditis. Circulation. 1999;99:1295-9. doi: 10.1161/01.CIR.99.10.1295
4. Миокардиты. Клинические рекомендации Национального общества по изучению сердечной недостаточности и заболеваний миокарда. 2016 г. Доступно по ссылке: http://docs.wixstatic.com/ugd/ e9c42f_d35dfe56900e4c4f836625820ebd3005.docx?dn=%D0%9A%D0%A0153.docx (Ссылка активна на 20.05.2018) [Miokardity: Klinicheskie rekomendatsii natsionalnogo obschestva po izucheniiy serdechnoi nedostatochnosti i zabolevaniy miokarda [Myocarditis. Clinical recommendations of the National Society for the Study of Heart Failure and Myocardial Diseases]. 2016. Available at: http://docs.wixstatic.com/ugd/e9c42f_d35dfe56900e4c4f836625820ebd3005.docx?dn=%D0%9A%D0%A0153.docx (Accessed May 20, 2018) (In Russ.)].
5. Maisch B, Portig I, Ristic A, Hufnagel G, Pankuweit S. Definition of inflammatory cardiomyopathy (myocarditis): On the way to consensus. A status report. Herz. 2000;25:200-9. doi: 10.1007/s000590050007
6. Cooper LT, Baughman KL, Feldman AM, Frustaci A, Jessup M, Kuhl U, et al. The role of endomyocardial biopsy in the management of cardiovascular disease: A scientific statement from the American Heart Association, the American College of Cardiology, and the European Society of Cardiology. JACC. 2007;50(19):1914-31. doi: 10.1016/j.jacc.2007.09.008
7. Friedrich MG, Sechtem U, Schulz-Menger J, Holmvang G, Alakija P, Cooper LT, et al. Cardiovascular magnetic resonance in myocarditis: A JACC white paper. J Am Coll Cardiol. 2009;53:1475-87. doi: 10.1016/j.jacc.2009.02.007
8. Mahrholdt H, Wagner A, Judd RM, Sechtem U, Kim RJ. Delayed enhancement cardiovascular magnetic resonance assessment of non-ischaemic cardiomyopathies. Eur Heart J. 2005;26:1461-74. doi: 10.1093/eurheartj/ehi258
9. Стукалова О.В. Магнитно-резонансная томография сердца с отсроченным контрастированием – новый метод диагностики заболеваний сердца. Российский электронный журнал лучевой диагностики. 2013;3(1):7-17. Доступно по ссылке: http://www.rejr.ru/english-version/vol-3-1-2013.htm. Ссылка активна на 20.05.2018 [Stukalova OV. Late-enhancement contrast cardiac MRI – new diagnostic tool in cardiac diseases. Rossiiskii Elektronnyi Zhurnal Luchevoi Diagnostiki = REJR. 2013;3(1):7-17. Available at: http://www.rejr.ru/english-version/vol-3-1-2013.html. Accessed May 20, 2018 (In Russ.)].
10. Abdel-Aty H, Simonetti O, Friedrich MG. T2-weighted cardiovascular magnetic resonance imaging. J Magnet Resonance Imag. 2007;26:452-9. doi: 10.1002/jmri.21028
11. Schulz-Menger J, Maisch B, Abdel-Aty H, Pankuweit S. Integrated biomarkers in cardiomyopathies: Cardiovascular magnetic resonance imaging combined with molecular and immunologic markers – a stepwise approach for diagnosis and treatment. Herz. 2007;32:458-72. doi: 10.1007/s00059-007-3046-4
12. Rottgen R, Christiani R, Freyhardt P, Gutberlet M, Schultheiss HP, Hamm B, et al. Magnetic resonance imaging findings in acute myocarditis and correlation with immunohistological parameters. Eur Radiol. 2011;21:1259-66. doi: 10.1007/s00330-010-2022-1
13. Lurz P, Daehnert I, Gutberlet M, Desch S. Renal sympathetic denervation in resistant hypertension late after surgical repair for aortic coarctation. Eur Heart J. 2013;34:3500. doi: 10.1093/eurheartj/eht228
14. Magnani JW, Dec GW. Myoarditits: Current trends in diagnosis and treatment. Circulation. 2006;113:876-90. doi: 10.1161/CIRCULATIONAHA.105.584532
15. Murphy JG, Franz RP. Endomyocardial biopsy in myocarditis. In: Cooper LT, ed. Myocarditis: From Bench to Bedside. Totowa, NJ: Humana Press; 2003.
16. Abdel-Aty H, Boyé P, Zagrosek A, Wassmuth R, Kumar A, Messroghli D, Bock P, Dietz R, Friedrich MG, Schulz-Menger J. Diagnostic performance of cardiovascular magnetic resonance in patients with suspected acute myocarditis: comparison of different approaches. J Am Coll Cardiol. 2005 Jun 7;45(11):1815-22. doi: 10.1016/j.jacc.2004.11.069
17. Aretz HT, Billingham ME, Edwards WD, Factor SM, Fallon JT, lio JJ Jr, et al. Myocarditis. A histopathologic definition and classification. Am J Cardiovasc Pathol. 1987;1:3-14.
18. Angelini A, Calzolari V, Calabrese F, et al. Myocarditis mimicking acute myocardial infarction: role of endomyocardial biopsy in the differential diagnosis. Heart. 2000;84:245-50. doi: 10.1136/heart.84.3.245
19. Hauck AJ, Kearney DL, Edwards WD. Evaluation of postmortem endomyocardial biopsy specimens from 38 patients with lymphocytic myocarditis: implications for role of sampling error. Mayo Clin Proc. 1989;64:1235-45. doi: 10.1016/S0025-6196(12)61286-5
20. Shanes JG, Ghali J, Billingham ME, et al. Interobserver variability in the pathologic interpretation of endomyocardial biopsy results. Circulation. 1987;75:401-5. doi: 10.1161/01.CIR.75.2.401
21. Shirani J, Freant LJ, Roberts WC. Gross and semiquantitative histologic findings in mononuclear cell myocarditis causing sudden death, and implications for endomyocardial biopsy. Am J Cardiol. 1993;72:952-7.
22. Assomull RG, Prasad SK, Lyne J, Smith G, Burman ED, Khan M, et al. Cardiovascular magnetic resonance, fibrosis, and prognosis in dilated cardiomyopathy. J Am Coll Cardiol. 2006;48:1977-85. doi: 10.1016/j.jacc.2006.07.049
23. Fulton WF. Anastomotic enlargement and ischaemic myocardial damage. Br Heart J. 1964 Jan;26:1-15. doi: 10.1136/hrt.26.1.1
24. Davies MJ, Fulton WF, Robertson WB. The relation of coronary thrombosis to ischaemic myocardial necrosis. J Pathol. 1979 Feb;127(2):99-110. doi: 10.1002/path.1711270208
25. Leurent G, Langella B, Fougerou C, Lentz PA, Larralde A, Bedossa M, Boulmier D, Le Breton H. Diagnostic contributions of cardiac magnetic resonance imaging in patients presenting with elevated troponin, acute chest pain syndrome and unobstructed coronary arteries. Arch Cardiovasc Dis. 2011 Mar;104(3):161-70. doi: 10.1016/j.acvd.2011.01.005
26. Dec GW Jr, Waldman H, Southern J, Fallon JT, Hutter AM Jr, Palacios I. Viral myocarditis mimicking acute myocardial infarction. J Am Coll Cardiol. 1992;20:85-9. doi: 10.1016/0735-1097(92)90141-9
27. Kuhl U, Pauschinger M, Bock T, et al. Parvovirus B19 infection mimicking acute myocardial infarction. Circulation. 2003;108:945-50. doi: 10.1161/01.CIR.0000085168.02782.2C
28. Francone M, Chimenti C, Galea N, Scopelliti F, Verardo R, Galea R, et al. Cmr sensitivity varies with clinical presentation and extent of cell necrosis in biopsy-proven acute myocarditis. JACC. Cardiovasc Imaging. 2014;7:254-63. doi: 10.1016/j.jcmg.2013.10.011
29. Agewall S, Beltrame JF, Reynolds HR, et al. ESC working group position paper on myocardial infarction with non-obstructive coronary arteries. Eur Heart J. 2017;38:143-53. doi: 10.1093/eurheartj/ehw149
30. Isner JM, Virm JR, Itscoitz SB, et al. Left and right ventricular myocardial infarction in idiopathic dilated cardiomyopathy. Am Heart J. 1980;99:235-42. doi: 10.1016/0002-8703(80)90771-1
31. McCrohon JA, Moon JC, Prasad SK, McKenna WJ, Lorenz CH, Coats AJ, Pennell DJ. Differentiation of heart failure related to dilated cardiomyopathy and coronary artery disease using gadolinium-enhanced cardiovascular magnetic resonance. Circulation. 2003 Jul 8;108(1):54-9. Epub 2003 Jun 23. doi: 10.1161/01.CIR.0000078641.19365.4C
32. Flynn JE, Mann FD. The presence and pathogenesis of endocardial and subendocardial degeneration, mural thrombi, and thromboses of the thebesian veins in cardiac failure from causes other than myocardial infarction. Am Heart J. 1946 Jun;31:757-68. doi: 10.1016/0002-8703(46)90502-9
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1. Feldman AM, McNamara D. Myocarditis. N Engl J Med. 2000;343:1388-98. doi: 10.1056/NEJM200011093431908
2. Cooper LT Jr. Myocarditis. N Engl J Med. 2009 Apr 9;360(15):1526-38. doi: 10.1056/NEJMra0800028
3. Frustaci A, Chimenti C, Maseri A. Global bi-ventricular dysfunction in patients with symptomatic coronary artery disease may be caused by myocarditis. Circulation. 1999;99:1295-9. doi: 10.1161/01.CIR.99.10.1295
4. Miokardity: Klinicheskie rekomendatsii natsionalnogo obschestva po izucheniiy serdechnoi nedostatochnosti i zabolevaniy miokarda [Myocarditis. Clinical recommendations of the National Society for the Study of Heart Failure and Myocardial Diseases. 2016. Available at: http://docs.wixstatic.com/ugd/e9c42f_d35dfe56900e4c4f836625820ebd3005.docx?dn=%D0%9A%D0%A0153.docx (Accessed May 20, 2018) (In Russ.)].
5. Maisch B, Portig I, Ristic A, Hufnagel G, Pankuweit S. Definition of inflammatory cardiomyopathy (myocarditis): On the way to consensus. A status report. Herz. 2000;25:200-9. doi: 10.1007/s000590050007
6. Cooper LT, Baughman KL, Feldman AM, Frustaci A, Jessup M, Kuhl U, et al. The role of endomyocardial biopsy in the management of cardiovascular disease: A scientific statement from the American Heart Association, the American College of Cardiology, and the European Society of Cardiology. JACC. 2007;50(19):1914-31. doi: 10.1016/j.jacc.2007.09.008
7. Friedrich MG, Sechtem U, Schulz-Menger J, Holmvang G, Alakija P, Cooper LT, et al. Cardiovascular magnetic resonance in myocarditis: A JACC white paper. J Am Coll Cardiol. 2009;53:1475-87. doi: 10.1016/j.jacc.2009.02.007
8. Mahrholdt H, Wagner A, Judd RM, Sechtem U, Kim RJ. Delayed enhancement cardiovascular magnetic resonance assessment of non-ischaemic cardiomyopathies. Eur Heart J. 2005;26:1461-74. doi: 10.1093/eurheartj/ehi258
9. Stukalova OV. Late-enhancement contrast cardiac MRI – new diagnostic tool in cardiac diseases. Rossiiskii Elektronnyi Zhurnal Luchevoi Diagnostiki = REJR. 2013;3(1):7-17. Available at: http://www.rejr.ru/english-version/vol-3-1-2013.html. Accessed May 20, 2018 (In Russ.).
10. Abdel-Aty H, Simonetti O, Friedrich MG. T2-weighted cardiovascular magnetic resonance imaging. J Magnet Resonance Imag. 2007;26:452-9. doi: 10.1002/jmri.21028
11. Schulz-Menger J, Maisch B, Abdel-Aty H, Pankuweit S. Integrated biomarkers in cardiomyopathies: Cardiovascular magnetic resonance imaging combined with molecular and immunologic markers – a stepwise approach for diagnosis and treatment. Herz. 2007;32:458-72. doi: 10.1007/s00059-007-3046-4
12. Rottgen R, Christiani R, Freyhardt P, Gutberlet M, Schultheiss HP, Hamm B, et al. Magnetic resonance imaging findings in acute myocarditis and correlation with immunohistological parameters. Eur Radiol. 2011;21:1259-66. doi: 10.1007/s00330-010-2022-1
13. Lurz P, Daehnert I, Gutberlet M, Desch S. Renal sympathetic denervation in resistant hypertension late after surgical repair for aortic coarctation. Eur Heart J. 2013;34:3500. doi: 10.1093/eurheartj/eht228
14. Magnani JW, Dec GW. Myoarditits: Current trends in diagnosis and treatment. Circulation. 2006;113:876-90. doi: 10.1161/CIRCULATIONAHA.105.584532
15. Murphy JG, Franz RP. Endomyocardial biopsy in myocarditis. In: Cooper LT, ed. Myocarditis: From Bench to Bedside. Totowa, NJ: Humana Press; 2003.
16. Abdel-Aty H, Boyé P, Zagrosek A, Wassmuth R, Kumar A, Messroghli D, Bock P, Dietz R, Friedrich MG, Schulz-Menger J. Diagnostic performance of cardiovascular magnetic resonance in patients with suspected acute myocarditis: comparison of different approaches. J Am Coll Cardiol. 2005 Jun 7;45(11):1815-22. doi: 10.1016/j.jacc.2004.11.069
17. Aretz HT, Billingham ME, Edwards WD, Factor SM, Fallon JT, lio JJ Jr, et al. Myocarditis. A histopathologic definition and classification. Am J Cardiovasc Pathol. 1987;1:3-14.
18. Angelini A, Calzolari V, Calabrese F, et al. Myocarditis mimicking acute myocardial infarction: role of endomyocardial biopsy in the differential diagnosis. Heart. 2000;84:245-50. doi: 10.1136/heart.84.3.245
19. Hauck AJ, Kearney DL, Edwards WD. Evaluation of postmortem endomyocardial biopsy specimens from 38 patients with lymphocytic myocarditis: implications for role of sampling error. Mayo Clin Proc. 1989;64:1235-45. doi: 10.1016/S0025-6196(12)61286-5
20. Shanes JG, Ghali J, Billingham ME, et al. Interobserver variability in the pathologic interpretation of endomyocardial biopsy results. Circulation. 1987;75:401-5. doi: 10.1161/01.CIR.75.2.401
21. Shirani J, Freant LJ, Roberts WC. Gross and semiquantitative histologic findings in mononuclear cell myocarditis causing sudden death, and implications for endomyocardial biopsy. Am J Cardiol. 1993;72:952-7.
22. Assomull RG, Prasad SK, Lyne J, Smith G, Burman ED, Khan M, et al. Cardiovascular magnetic resonance, fibrosis, and prognosis in dilated cardiomyopathy. J Am Coll Cardiol. 2006;48:1977-85. doi: 10.1016/j.jacc.2006.07.049
23. Fulton WF. Anastomotic enlargement and ischaemic myocardial damage. Br Heart J. 1964 Jan;26:1-15. doi: 10.1136/hrt.26.1.1
24. Davies MJ, Fulton WF, Robertson WB. The relation of coronary thrombosis to ischaemic myocardial necrosis. J Pathol. 1979 Feb;127(2):99-110. doi: 10.1002/path.1711270208
25. Leurent G, Langella B, Fougerou C, Lentz PA, Larralde A, Bedossa M, Boulmier D, Le Breton H. Diagnostic contributions of cardiac magnetic resonance imaging in patients presenting with elevated troponin, acute chest pain syndrome and unobstructed coronary arteries. Arch Cardiovasc Dis. 2011 Mar;104(3):161-70. doi: 10.1016/j.acvd.2011.01.005
26. Dec GW Jr, Waldman H, Southern J, Fallon JT, Hutter AM Jr, Palacios I. Viral myocarditis mimicking acute myocardial infarction. J Am Coll Cardiol. 1992;20:85-9. doi: 10.1016/0735-1097(92)90141-9
27. Kuhl U, Pauschinger M, Bock T, et al. Parvovirus B19 infection mimicking acute myocardial infarction. Circulation. 2003;108:945-50. doi: 10.1161/01.CIR.0000085168.02782.2C
28. Francone M, Chimenti C, Galea N, Scopelliti F, Verardo R, Galea R, et al. Cmr sensitivity varies with clinical presentation and extent of cell necrosis in biopsy-proven acute myocarditis. JACC. Cardiovasc Imaging. 2014;7:254-63. doi: 10.1016/j.jcmg.2013.10.011
29. Agewall S, Beltrame JF, Reynolds HR, et al. ESC working group position paper on myocardial infarction with non-obstructive coronary arteries. Eur Heart J. 2017;38:143-53. doi: 10.1093/eurheartj/ehw149
30. Isner JM, Virm JR, Itscoitz SB, et al. Left and right ventricular myocardial infarction in idiopathic dilated cardiomyopathy. Am Heart J. 1980;99:235-42. doi: 10.1016/0002-8703(80)90771-1
31. McCrohon JA, Moon JC, Prasad SK, McKenna WJ, Lorenz CH, Coats AJ, Pennell DJ. Differentiation of heart failure related to dilated cardiomyopathy and coronary artery disease using gadolinium-enhanced cardiovascular magnetic resonance. Circulation. 2003 Jul 8;108(1):54-9. Epub 2003 Jun 23. doi: 10.1161/01.CIR.0000078641.19365.4C
32. Flynn JE, Mann FD. The presence and pathogenesis of endocardial and subendocardial degeneration, mural thrombi, and thromboses of the thebesian veins in cardiac failure from causes other than myocardial infarction. Am Heart J. 1946 Jun;31:757-68. doi: 10.1016/0002-8703(46)90502-9
1 Научно-исследовательский институт клинической кардиологии им. А.Л. Мясникова ФГБУ «Национальный медицинский исследовательский центр кардиологии» Минздрава России, Москва, Россия;
2 ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России (Сеченовский Университет), Москва, Россия
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O.V. Stukalova 1, E.M. Gupalo 1, P.V. Chumachenko 1, A.N. Samko 1, E.A. Butorova 1, R.M. Shakhnovich 1, N.A. Mironova 1, O.Yu. Narusov 1, A.A. Safiullina 1, M.A. Shariya 1, S.P. Golitsyn 1, S.K. Ternovoy 1,2, I.E. Chazova 1
1 A.L. Myasnikov Research Institute of Clinical Cardiology of National Medical Research Center of Cardiology of the Ministry of Health of Russia, Moscow, Russia;
2 I.M. Sechenov First Moscow State Medical University (Sechenov University) of the Ministry of Health of Russia, Moscow, Russia