Investigative Magnetic Resonance Imaging

Korean Society of Magnetic Resonance in Medicine (대한자기공명의과학회)
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Recent Update of Advanced Imaging for Diagnosis of Cardiac Sarcoidosis: Based on the Findings of Cardiac Magnetic Resonance Imaging and Positron Emission Tomography

  • Chang, Suyon (Department of Radiology, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Lee, Won Woo (Department of Nuclear Medicine, Seoul National University Bundang Hospital) ;
  • Chun, Eun Ju (Department of Radiology, Seoul National University Bundang Hospital)
  • Received : 2018.12.27
  • Accepted : 2019.03.26
  • Published : 2019.06.30
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Abstract

Sarcoidosis is a multisystem disease characterized by noncaseating granulomas. Cardiac involvement is known to have poor prognosis because it can manifest as a serious condition such as the conduction abnormality, heart failure, ventricular arrhythmia, or sudden cardiac death. Although early diagnosis and early treatment is critical to improve patient prognosis, the diagnosis of CS is challenging in most cases. Diagnosis usually relies on endomyocardial biopsy (EMB), but its diagnostic yield is low due to the incidence of patchy myocardial involvement. Guidelines for the diagnosis of CS recommend a combination of clinical, electrocardiographic, and imaging findings from various modalities, if EMB cannot confirm the diagnosis. Especially, the role of advanced imaging such as cardiac magnetic resonance (CMR) imaging and positron emission tomography (PET), has shown to be important not only for the diagnosis, but also for monitoring treatment response and prognostication. CMR can evaluate cardiac function and fibrotic scar with good specificity. Late gadolinium enhancement (LGE) in CMR shows a distinctive enhancement pattern for each disease, which may be useful for differential diagnosis of CS from other similar diseases. Effectively, T1 or T2 mapping techniques can be also used for early recognition of CS. In the meantime, PET can detect and quantify metabolic activity and can be used to monitor treatment response. Recently, the use of a hybrid CMR-PET has introduced to allow identify patients with active CS with excellent co-localization and better diagnostic accuracy than CMR or PET alone. However, CS may show various findings with a wide spectrum, therefore, radiologists should consider the possible differential diagnosis of CS including myocarditis, dilated cardiomyopathy (DCM), hypertrophic cardiomyopathy, amyloidosis, and arrhythmogenic right ventricular cardiomyopathy. Radiologists should recognize the differences in various diseases that show the characteristics of mimicking CS, and try to get an accurate diagnosis of CS.

Keywords

References

  1. Statement on sarcoidosis. Joint Statement of the American Thoracic Society (ATS), the European Respiratory Society (ERS) and the World Association of Sarcoidosis and Other Granulomatous Disorders (WASOG) adopted by the ATS Board of Directors and by the ERS Executive Committee, February 1999. Am J Respir Crit Care Med 1999;160:736-755 https://doi.org/10.1164/ajrccm.160.2.ats4-99
  2. Schatka I, Bengel FM. Advanced imaging of cardiac sarcoidosis. J Nucl Med 2014;55:99-106 https://doi.org/10.2967/jnumed.112.115121
  3. Silverman KJ, Hutchins GM, Bulkley BH. Cardiac sarcoid: a clinicopathologic study of 84 unselected patients with systemic sarcoidosis. Circulation 1978;58:1204-1211 https://doi.org/10.1161/01.CIR.58.6.1204
  4. Lynch JP 3rd, Hwang J, Bradfield J, Fishbein M, Shivkumar K, Tung R. Cardiac involvement in sarcoidosis: evolving concepts in diagnosis and treatment. Semin Respir Crit Care Med 2014;35:372-390 https://doi.org/10.1055/s-0034-1376889
  5. Yazaki Y, Isobe M, Hiroe M, et al. Prognostic determinants of long-term survival in Japanese patients with cardiac sarcoidosis treated with prednisone. Am J Cardiol 2001;88:1006-1010 https://doi.org/10.1016/S0002-9149(01)01978-6
  6. Ardehali H, Howard DL, Hariri A, et al. A positive endomyocardial biopsy result for sarcoid is associated with poor prognosis in patients with initially unexplained cardiomyopathy. Am Heart J 2005;150:459-463 https://doi.org/10.1016/j.ahj.2004.10.006
  7. Hillerdal G, Nou E, Osterman K, Schmekel B. Sarcoidosis: epidemiology and prognosis. A 15-year European study. Am Rev Respir Dis 1984;130:29-32
  8. Morimoto T, Azuma A, Abe S, et al. Epidemiology of sarcoidosis in Japan. Eur Respir J 2008;31:372-379 https://doi.org/10.1183/09031936.00075307
  9. Varron L, Cottin V, Schott AM, Broussolle C, Seve P. Late-onset sarcoidosis: a comparative study. Medicine (Baltimore) 2012;91:137-143 https://doi.org/10.1097/MD.0b013e3182569f91
  10. Perry A, Vuitch F. Causes of death in patients with sarcoidosis. A morphologic study of 38 autopsies with clinicopathologic correlations. Arch Pathol Lab Med 1995;119:167-172
  11. Iwai K, Tachibana T, Takemura T, Matsui Y, Kitaichi M, Kawabata Y. Pathological studies on sarcoidosis autopsy. I. Epidemiological features of 320 cases in Japan. Acta Pathol Jpn 1993;43:372-376
  12. Mehta D, Lubitz SA, Frankel Z, et al. Cardiac involvement in patients with sarcoidosis: diagnostic and prognostic value of outpatient testing. Chest 2008;133:1426-1435 https://doi.org/10.1378/chest.07-2784
  13. Rosen Y. Pathology of sarcoidosis. Semin Respir Crit Care Med 2007;28:36-52 https://doi.org/10.1055/s-2007-970332
  14. Uemura A, Morimoto S, Hiramitsu S, Kato Y, Ito T, Hishida H. Histologic diagnostic rate of cardiac sarcoidosis: evaluation of endomyocardial biopsies. Am Heart J 1999;138:299-302 https://doi.org/10.1016/S0002-8703(99)70115-8
  15. Tavora F, Cresswell N, Li L, Ripple M, Solomon C, Burke A. Comparison of necropsy findings in patients with sarcoidosis dying suddenly from cardiac sarcoidosis versus dying suddenly from other causes. Am J Cardiol 2009;104:571-577 https://doi.org/10.1016/j.amjcard.2009.03.068
  16. Birnie DH, Nery PB, Ha AC, Beanlands RS. Cardiac sarcoidosis. J Am Coll Cardiol 2016;68:411-421 https://doi.org/10.1016/j.jacc.2016.03.605
  17. Youssef G, Beanlands RS, Birnie DH, Nery PB. Cardiac sarcoidosis: applications of imaging in diagnosis and directing treatment. Heart 2011;97:2078-2087 https://doi.org/10.1136/hrt.2011.226076
  18. Sekhri V, Sanal S, Delorenzo LJ, Aronow WS, Maguire GP. Cardiac sarcoidosis: a comprehensive review. Arch Med Sci 2011;7:546-554
  19. Hiraga HHM, Iwai K. Guidelines for diagnosis of cardiac sarcoidosis: study report on diffuse pulmonary diseases (in Japanese). Tokyo: The Japanese Ministry of Health and Welfare, 1993:23-24
  20. Soejima K, Yada H. The work-up and management of patients with apparent or subclinical cardiac sarcoidosis: with emphasis on the associated heart rhythm abnormalities. J Cardiovasc Electrophysiol 2009;20:578-583 https://doi.org/10.1111/j.1540-8167.2008.01417.x
  21. Youssef G, Leung E, Mylonas I, et al. The use of 18F-FDG PET in the diagnosis of cardiac sarcoidosis: a systematic review and metaanalysis including the Ontario experience. J Nucl Med 2012;53:241-248 https://doi.org/10.2967/jnumed.111.090662
  22. Blankstein R, Osborne M, Naya M, et al. Cardiac positron emission tomography enhances prognostic assessments of patients with suspected cardiac sarcoidosis. J Am Coll Cardiol 2014;63:329-336 https://doi.org/10.1016/j.jacc.2013.09.022
  23. Kouranos V, Wells AU, Sharma R, Underwood SR, Wechalekar K. Advances in radionuclide imaging of cardiac sarcoidosis. Br Med Bull 2015;115:151-163 https://doi.org/10.1093/bmb/ldv033
  24. Birnie DH, Sauer WH, Bogun F, et al. HRS expert consensus statement on the diagnosis and management of arrhythmias associated with cardiac sarcoidosis. Heart Rhythm 2014;11:1305-1323
  25. Hulten E, Aslam S, Osborne M, Abbasi S, Bittencourt MS, Blankstein R. Cardiac sarcoidosis-state of the art review. Cardiovasc Diagn Ther 2016;6:50-63
  26. Jeudy J, Burke AP, White CS, Kramer GB, Frazier AA. Cardiac sarcoidosis: the challenge of radiologic-pathologic correlation: from the radiologic pathology archives. Radiographics 2015;35:657-679 https://doi.org/10.1148/rg.2015140247
  27. 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;285:63-72 https://doi.org/10.1148/radiol.2017162732
  28. Kouranos V, Tzelepis GE, Rapti A, et al. Complementary role of CMR to conventional screening in the diagnosis and prognosis of cardiac sarcoidosis. JACC Cardiovasc Imaging 2017;10:1437-1447 https://doi.org/10.1016/j.jcmg.2016.11.019
  29. Patel MR, Cawley PJ, Heitner JF, et al. Detection of myocardial damage in patients with sarcoidosis. Circulation 2009;120:1969-1977 https://doi.org/10.1161/CIRCULATIONAHA.109.851352
  30. Greulich S, Deluigi CC, Gloekler S, et al. CMR imaging predicts death and other adverse events in suspected cardiac sarcoidosis. JACC Cardiovasc Imaging 2013;6:501-511 https://doi.org/10.1016/j.jcmg.2012.10.021
  31. Ise T, Hasegawa T, Morita Y, et al. Extensive late gadolinium enhancement on cardiovascular magnetic resonance predicts adverse outcomes and lack of improvement in LV function after steroid therapy in cardiac sarcoidosis. Heart 2014;100:1165-1172 https://doi.org/10.1136/heartjnl-2013-305187
  32. Crouser ED, Ono C, Tran T, He X, Raman SV. Improved detection of cardiac sarcoidosis using magnetic resonance with myocardial T2 mapping. Am J Respir Crit Care Med 2014;189:109-112 https://doi.org/10.1164/rccm.201309-1668LE
  33. Perez IE, Garcia MJ, Taub CC. Multimodality imaging in cardiac sarcoidosis: is there a winner? Curr Cardiol Rev 2016;12:3-11 https://doi.org/10.2174/1573403X11666150318110406
  34. Orii M, Imanishi T, Akasaka T. Assessment of cardiac sarcoidosis with advanced imaging modalities. Biomed Res Int 2014;2014:897956 https://doi.org/10.1155/2014/897956
  35. Roberts WC, McAllister HA, Jr., Ferrans VJ. Sarcoidosis of the heart. A clinicopathologic study of 35 necropsy patients (group 1) and review of 78 previously described necropsy patients (group 11). Am J Med 1977;63:86-108 https://doi.org/10.1016/0002-9343(77)90121-8
  36. Greulich S, Kitterer D, Latus J, et al. Comprehensive cardiovascular magnetic resonance assessment in patients with sarcoidosis and preserved left ventricular ejection fraction. Circ Cardiovasc Imaging 2016;9:e005022
  37. Ferreira VM, Piechnik SK. Seeing beyond the obvious: subclinical cardiac sarcoidosis revealed by cardiovascular magnetic resonance mapping. Circ Cardiovasc Imaging 2016;9:e005592
  38. Hinojar R, Foote L, Arroyo Ucar E, et al. Native T1 in discrimination of acute and convalescent stages in patients with clinical diagnosis of myocarditis: a proposed diagnostic algorithm using CMR. JACC Cardiovasc Imaging 2015;8:37-46 https://doi.org/10.1016/j.jcmg.2014.07.016
  39. Manoushagian SJ, Lakhter V, Patil PV. Multimodality imaging in the diagnosis and management of cardiac sarcoidosis. J Nucl Cardiol 2017;24:29-33 https://doi.org/10.1007/s12350-016-0721-y
  40. Langah R, Spicer K, Gebregziabher M, Gordon L. Effectiveness of prolonged fasting 18f-FDG PET-CT in the detection of cardiac sarcoidosis. J Nucl Cardiol 2009;16:801-810 https://doi.org/10.1007/s12350-009-9110-0
  41. Ishimaru S, Tsujino I, Takei T, et al. Focal uptake on 18F-fluoro-2-deoxyglucose positron emission tomography images indicates cardiac involvement of sarcoidosis. Eur Heart J 2005;26:1538-1543 https://doi.org/10.1093/eurheartj/ehi180
  42. Harisankar CN, Mittal BR, Agrawal KL, Abrar ML, Bhattacharya A. Utility of high fat and low carbohydrate diet in suppressing myocardial FDG uptake. J Nucl Cardiol 2011;18:926-936 https://doi.org/10.1007/s12350-011-9422-8
  43. Betensky BP, Tschabrunn CM, Zado ES, et al. Longterm follow-up of patients with cardiac sarcoidosis and implantable cardioverter-defibrillators. Heart Rhythm 2012;9:884-891 https://doi.org/10.1016/j.hrthm.2012.02.010
  44. Ahmadian A, Brogan A, Berman J, et al. Quantitative interpretation of FDG PET/CT with myocardial perfusion imaging increases diagnostic information in the evaluation of cardiac sarcoidosis. J Nucl Cardiol 2014;21:925-939 https://doi.org/10.1007/s12350-014-9901-9
  45. Gormsen LC, Haraldsen A, Kramer S, Dias AH, Kim WY, Borghammer P. A dual tracer (68)Ga-DOTANOC PET/CT and (18)F-FDG PET/CT pilot study for detection of cardiac sarcoidosis. EJNMMI Res 2016;6:52 https://doi.org/10.1186/s13550-016-0207-6
  46. Manabe O, Hirata K, Shozo O, et al. (18)F-fluoromisonidazole (FMISO) PET may have the potential to detect cardiac sarcoidosis. J Nucl Cardiol 2017;24:329-331 https://doi.org/10.1007/s12350-016-0495-2
  47. Ohira H, Tsujino I, Ishimaru S, et al. Myocardial imaging with 18F-fluoro-2-deoxyglucose positron emission tomography and magnetic resonance imaging in sarcoidosis. Eur J Nucl Med Mol Imaging 2008;35:933-941 https://doi.org/10.1007/s00259-007-0650-8
  48. Dweck MR, Abgral R, Trivieri MG, et al. Hybrid magnetic resonance imaging and positron emission tomography with fluorodeoxyglucose to diagnose active cardiac sarcoidosis. JACC Cardiovasc Imaging 2018;11:94-107 https://doi.org/10.1016/j.jcmg.2017.02.021
  49. Wicks EC, Menezes LJ, Barnes A, et al. Diagnostic accuracy and prognostic value of simultaneous hybrid 18F-fluorodeoxyglucose positron emission tomography/magnetic resonance imaging in cardiac sarcoidosis. Eur Heart J Cardiovasc Imaging 2018;19:757-767 https://doi.org/10.1093/ehjci/jex340
  50. Ishida Y, Yoshinaga K, Miyagawa M, et al. Recommendations for (18)F-fluorodeoxyglucose positron emission tomography imaging for cardiac sarcoidosis: Japanese Society of Nuclear Cardiology recommendations. Ann Nucl Med 2014;28:393-403 https://doi.org/10.1007/s12149-014-0806-0
  51. Friedrich MG, Sechtem U, Schulz-Menger J, et al. Cardiovascular magnetic resonance in myocarditis: a JACC white paper. J Am Coll Cardiol 2009;53:1475-1487 https://doi.org/10.1016/j.jacc.2009.02.007
  52. Yilmaz A, Ferreira V, Klingel K, Kandolf R, Neubauer S, Sechtem U. Role of cardiovascular magnetic resonance imaging (CMR) in the diagnosis of acute and chronic myocarditis. Heart Fail Rev 2013;18:747-760 https://doi.org/10.1007/s10741-012-9356-5
  53. Yazaki Y, Isobe M, Hiramitsu S, et al. Comparison of clinical features and prognosis of cardiac sarcoidosis and idiopathic dilated cardiomyopathy. Am J Cardiol 1998;82:537-540 https://doi.org/10.1016/S0002-9149(98)00377-4
  54. Vignaux O. Cardiac sarcoidosis: spectrum of MRI features. AJR Am J Roentgenol 2005;184:249-254 https://doi.org/10.2214/ajr.184.1.01840249
  55. Moraes GL, Higgins CB, Ordovas KG. Delayed enhancement magnetic resonance imaging in nonischemic myocardial disease. J Thorac Imaging 2013;28:84-92; quiz 93-95 https://doi.org/10.1097/RTI.0b013e3182828f89
  56. Marcus FI, McKenna WJ, Sherrill D, et al. Diagnosis of arrhythmogenic right ventricular cardiomyopathy/dysplasia: proposed modification of the task force criteria. Circulation 2010;121:1533-1541 https://doi.org/10.1161/CIRCULATIONAHA.108.840827
  57. Steckman DA, Schneider PM, Schuller JL, et al. Utility of cardiac magnetic resonance imaging to differentiate cardiac sarcoidosis from arrhythmogenic right ventricular cardiomyopathy. Am J Cardiol 2012;110:575-579 https://doi.org/10.1016/j.amjcard.2012.04.029
  58. Bartlett ML, Bacharach SL, Voipio-Pulkki LM, Dilsizian V. Artifactual inhomogeneities in myocardial PET and SPECT scans in normal subjects. J Nucl Med 1995;36:188-195
  59. Tahara N, Tahara A, Nitta Y, et al. Heterogeneous myocardial FDG uptake and the disease activity in cardiac sarcoidosis. JACC Cardiovasc Imaging 2010;3:1219-1228 https://doi.org/10.1016/j.jcmg.2010.09.015

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