Diagnosis of cardiac sarcoidosis: a primer for non-imagers.
Advanced cardiac imaging
Cardiac MRI
Cardiac PET
Cardiac sarcoidosis
Hybrid imaging
Journal
Heart failure reviews
ISSN: 1573-7322
Titre abrégé: Heart Fail Rev
Pays: United States
ID NLM: 9612481
Informations de publication
Date de publication:
07 2022
07 2022
Historique:
accepted:
25
05
2021
pubmed:
30
6
2021
medline:
18
6
2022
entrez:
29
6
2021
Statut:
ppublish
Résumé
Sarcoidosis is a multisystem granulomatous disorder that can potentially involve any organ. Cardiac involvement in sarcoidosis has been reported in up to 25% of patients based on autopsy and imaging studies. The gold standard for diagnosing cardiac sarcoidosis is endomyocardial biopsy demonstrating non-caseating granulomas; however, this technique lacks sensitivity due to the patchy nature of myocardial involvement. This, along with the non-specific clinical presentation, renders the diagnosis of cardiac sarcoidosis extremely challenging. Difficulties in obtaining histopathologic diagnosis and the advances in imaging modalities have led to a paradigm shift toward non-invasive imaging in the diagnosis of cardiac sarcoidosis. Advances in cardiac imaging modalities have also allowed unprecedented insights into the prevalence and natural history of cardiac sarcoidosis. This review discusses the role of non-invasive imaging for diagnosis, risk stratification, and monitoring the response to therapies in cardiac sarcoidosis. Echocardiography remains the first-line modality due to widespread availability and affordability. Cardiac magnetic resonance imaging (CMR) can be used to study cardiac structure, function, and most importantly tissue characterization to detect inflammation and fibrosis. Fluoro-deoxy glucose positron emission tomography (FDG PET) is the gold standard for non-invasive detection of cardiac inflammation, and it offers the unique ability to assess response to therapeutic interventions. Hybrid imaging is a promising technique that allows us to combine the unique strengths of CMR and FDG PET. Understanding the advantages and disadvantages of each of these imaging modalities is crucial in order to tailor the diagnostic algorithm and utilize the most appropriate modality for each patient.
Identifiants
pubmed: 34185203
doi: 10.1007/s10741-021-10126-5
pii: 10.1007/s10741-021-10126-5
doi:
Substances chimiques
Fluorodeoxyglucose F18
0Z5B2CJX4D
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1223-1233Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
James DG, Sharma OP (2002) From Hutchinson to now: a historical glimpse. Curr Opin Pulm Med 8(5):416–423. https://doi.org/10.1097/00063198-200209000-00013
doi: 10.1097/00063198-200209000-00013
pubmed: 12172446
Iannuzzi MC, Rybicki BA (2007) Genetics of sarcoidosis: candidate genes and genome scans. Proc Am Thorac Soc 4(1):108–116. https://doi.org/10.1513/pats.200607-141JG
doi: 10.1513/pats.200607-141JG
pubmed: 17202299
pmcid: 2647608
Newman LS, Rose CS, Bresnitz EA et al (2004) A case control etiologic study of sarcoidosis: environmental and occupational risk factors. Am J Respir Crit Care Med 170(12):1324–1330. https://doi.org/10.1164/rccm.200402-249OC
doi: 10.1164/rccm.200402-249OC
pubmed: 15347561
Naruse TK, Matsuzawa Y, Ota M et al (2000) HLA-DQB1*0601 is primarily associated with the susceptibility to cardiac sarcoidosis. Tissue Antigens 56(1):52–57. https://doi.org/10.1034/j.1399-0039.2000.560107.x
Takashige N, Naruse TK, Matsumori A et al (1999) Genetic polymorphisms at the tumour necrosis factor loci (TNFA and TNFB) in cardiac sarcoidosis. Tissue Antigens 54(2):191–193. https://doi.org/10.1034/j.1399-0039.1999.540211.x
doi: 10.1034/j.1399-0039.1999.540211.x
pubmed: 10488747
Silverman KJ, Hutchins GM, Bulkley BH (1978) Cardiac sarcoid: a clinicopathologic study of 84 unselected patients with systemic sarcoidosis. Circulation 58(6):1204–1211. https://doi.org/10.1161/01.cir.58.6.1204
doi: 10.1161/01.cir.58.6.1204
pubmed: 709777
Iwai K, Takemura T, Kitaichi M, Kawabata Y, Matsui Y (1993) Pathological studies on sarcoidosis autopsy. II. Early change, mode of progression and death pattern. Acta Pathol Jpn 43(7–8):377–85. https://doi.org/10.1111/j.1440-1827.1993.tb01149.x
Ungprasert P, Carmona EM, Utz JP, Ryu JH, Crowson CS, Matteson EL (2016) Epidemiology of Sarcoidosis 1946–2013: a population-based study. Mayo Clin Proc 91(2):183–188. https://doi.org/10.1016/j.mayocp.2015.10.024
doi: 10.1016/j.mayocp.2015.10.024
pubmed: 26727158
Baughman RP, Teirstein AS, Judson MA et al (2001) Clinical characteristics of patients in a case control study of sarcoidosis. Am J Respir Crit Care Med 164(10 Pt 1):1885–1889. https://doi.org/10.1164/ajrccm.164.10.2104046
doi: 10.1164/ajrccm.164.10.2104046
pubmed: 11734441
Iwai K, Tachibana T, Takemura T, Matsui Y, Kitaichi M, Kawabata Y (1993) Pathological studies on sarcoidosis autopsy. I. epidemiological features of 320 cases in Japan. Acta Pathol Jpn 43(7–8):372–376. https://doi.org/10.1111/j.1440-1827.1993.tb01148.x
Perry A, Vuitch F (1995) Causes of death in patients with sarcoidosis. a morphologic study of 38 autopsies with clinicopathologic correlations. Arch Pathol Lab Med 119(2):167–172
Lynch JP 3rd, Hwang J, Bradfield J, Fishbein M, Shivkumar K, Tung R (2014) Cardiac involvement in sarcoidosis: evolving concepts in diagnosis and treatment. Semin Respir Crit Care Med 35(3):372–390. https://doi.org/10.1055/s-0034-1376889
doi: 10.1055/s-0034-1376889
pubmed: 25007089
pmcid: 4253029
Birnie DH, Nery PB, Ha AC, Beanlands RS (2016) Cardiac Sarcoidosis. J Am Coll Cardiol 68(4):411–421. https://doi.org/10.1016/j.jacc.2016.03.605
doi: 10.1016/j.jacc.2016.03.605
pubmed: 27443438
Kandolin R, Lehtonen J, Graner M et al (2011) Diagnosing isolated cardiac sarcoidosis. J Intern Med 270(5):461–468. https://doi.org/10.1111/j.1365-2796.2011.02396.x
doi: 10.1111/j.1365-2796.2011.02396.x
pubmed: 21535250
Youssef G, Leung E, Mylonas I et al (2012) The use of 18F-FDG PET in the diagnosis of cardiac sarcoidosis: a systematic review and metaanalysis including the Ontario experience. J Nucl Med 53(2):241–248. https://doi.org/10.2967/jnumed.111.090662
doi: 10.2967/jnumed.111.090662
pubmed: 22228794
Greulich S, Deluigi CC, Gloekler S et al (2013) CMR imaging predicts death and other adverse events in suspected cardiac sarcoidosis. JACC Cardiovasc Imaging 6(4):501–511. https://doi.org/10.1016/j.jcmg.2012.10.021
doi: 10.1016/j.jcmg.2012.10.021
pubmed: 23498675
Kandolin R, Lehtonen J, Airaksinen J et al (2015) Cardiac sarcoidosis: epidemiology, characteristics, and outcome over 25 years in a nationwide study. Circulation 131(7):624–632. https://doi.org/10.1161/circulationaha.114.011522
doi: 10.1161/circulationaha.114.011522
pubmed: 25527698
Birnie DH, Sauer WH, Bogun F et al (2014) HRS expert consensus statement on the diagnosis and management of arrhythmias associated with cardiac sarcoidosis. Heart Rhythm 11(7):1305–1323. https://doi.org/10.1016/j.hrthm.2014.03.043
doi: 10.1016/j.hrthm.2014.03.043
pubmed: 24819193
Yazaki Y, Isobe M, Hiroe M et al (2001) Prognostic determinants of long-term survival in Japanese patients with cardiac sarcoidosis treated with prednisone. Am J Cardiol 88(9):1006–1010. https://doi.org/10.1016/s0002-9149(01)01978-6
doi: 10.1016/s0002-9149(01)01978-6
pubmed: 11703997
Roberts WC, Becker TM, Hall SA (2018) Usefulness of total 12-lead QRS voltage as a clue to diagnosis of patients with cardiac sarcoidosis severe enough to warrant orthotopic heart transplant. JAMA Cardiol 3(1):64–68. https://doi.org/10.1001/jamacardio.2017.4172
doi: 10.1001/jamacardio.2017.4172
pubmed: 29141071
Cain MA, Metzl MD, Patel AR et al (2014) Cardiac sarcoidosis detected by late gadolinium enhancement and prevalence of atrial arrhythmias. Am J Cardiol 113(9):1556–1560. https://doi.org/10.1016/j.amjcard.2014.01.434
doi: 10.1016/j.amjcard.2014.01.434
pubmed: 24731652
Okada DR, Smith J, Derakhshan A et al (2018) Ventricular arrhythmias in cardiac sarcoidosis. Circulation 138(12):1253–1264. https://doi.org/10.1161/circulationaha.118.034687
doi: 10.1161/circulationaha.118.034687
pubmed: 30354431
Naruse Y, Sekiguchi Y, Nogami A et al (2014) Systematic treatment approach to ventricular tachycardia in cardiac sarcoidosis. Circ Arrhythm Electrophysiol 7(3):407–413. https://doi.org/10.1161/circep.113.000734
doi: 10.1161/circep.113.000734
pubmed: 24837644
Coleman GC, Shaw PW, Balfour PC Jr et al (2017) Prognostic value of myocardial scarring on CMR in patients with cardiac sarcoidosis. JACC Cardiovasc Imaging 10(4):411–420. https://doi.org/10.1016/j.jcmg.2016.05.009
doi: 10.1016/j.jcmg.2016.05.009
pubmed: 27450877
Blankstein R, Osborne M, Naya M et al (2014) Cardiac positron emission tomography enhances prognostic assessments of patients with suspected cardiac sarcoidosis. J Am Coll Cardiol 63(4):329–336. https://doi.org/10.1016/j.jacc.2013.09.022
doi: 10.1016/j.jacc.2013.09.022
pubmed: 24140661
Litovsky SH, Burke AP, Virmani R (1996) Giant cell myocarditis: an entity distinct from sarcoidosis characterized by multiphasic myocyte destruction by cytotoxic T cells and histiocytic giant cells. Mod Pathol: an official journal of the United States and Canadian Academy of Pathology, Inc. 9(12):1126–34
Fathima S, Roberts WC (2019) Comparison of clinical and morphologic findings in patients with cardiac sarcoidosis severe enough to warrant heart transplantation in those with -vs- those without non-caseating granulomas in the explanted heart (burnt-out sarcoid). Am J Cardiol 124(4):599–603. https://doi.org/10.1016/j.amjcard.2019.05.020
doi: 10.1016/j.amjcard.2019.05.020
pubmed: 31235064
Ardehali H, Howard DL, Hariri A et al (2005) A positive endomyocardial biopsy result for sarcoid is associated with poor prognosis in patients with initially unexplained cardiomyopathy. Am Heart J 150(3):459–463. https://doi.org/10.1016/j.ahj.2004.10.006
doi: 10.1016/j.ahj.2004.10.006
pubmed: 16169324
Sekiguchi M, Hiroe M, Take M, Hirosawa K (1980) Clinical and histopathological profile of sarcoidosis of the heart and acute idiopathic myocarditis. concepts through a study employing endomyocardial biopsy. II. Myocarditis. Jpn Circ J 44(4):264–73. https://doi.org/10.1253/jcj.44.264
Hiraga H, Yuwai K, Hiroe M (2007) Diagnostic standard and guidelines for sarcoidosis. Jpn J Sarcoidosis Granulomatous Disord 27:89–102
Terasaki F, Yoshinaga K (2017) New guidelines for diagnosis of cardiac sarcoidosis in Japan. Ann Nucl Cardiol 3(1):42–45. https://doi.org/10.17996/anc.17-00042
doi: 10.17996/anc.17-00042
Mehta D, Lubitz SA, Frankel Z et al (2008) Cardiac involvement in patients with sarcoidosis: diagnostic and prognostic value of outpatient testing. Chest 133(6):1426–1435. https://doi.org/10.1378/chest.07-2784
doi: 10.1378/chest.07-2784
pubmed: 18339784
Crouser ED (2020) Diagnosis and detection of sarcoidosis. An official American Thoracic Society clinical practice guideline 201(8):e26–e51. https://doi.org/10.1164/rccm.202002-0251ST
Bargout R, Kelly RF (2004) Sarcoid heart disease: clinical course and treatment. Int J Cardiol 97(2):173–182. https://doi.org/10.1016/j.ijcard.2003.07.024
doi: 10.1016/j.ijcard.2003.07.024
pubmed: 15458680
Nureki S, Miyazaki E, Nishio S et al (2014) Interventricular septal thickening as an early manifestation of cardiac sarcoidosis. Int Heart J 55(2):181–183. https://doi.org/10.1536/ihj.13-243
doi: 10.1536/ihj.13-243
pubmed: 24632961
Kurmann R, Mankad SV, Mankad R (2018) Echocardiography in sarcoidosis. Curr Cardiol Rep 20(11):118. https://doi.org/10.1007/s11886-018-1065-9
Slart RH, Glaudemans AW, Lancellotti P, Hyafil F, Blankstein R, Schwartz RG, & Masci PG (2017) A joint procedural position statement on imaging in cardiac sarcoidosis: from the Cardiovascular and Inflammation & Infection Committees of the European Association of Nuclear Medicine, the European Association of Cardiovascular Imaging, and the American Society of Nuclear Cardiology. Eur Heart J Cardiovasc Imaging 18(10):1073–1089. https://doi.org/10.1093/ehjci/jex146
Patel MB, Mor-Avi V, Murtagh G et al (2016) Right heart involvement in patients with sarcoidosis. Echocardiography (Mount Kisco, NY) 33(5):734–741. https://doi.org/10.1111/echo.13163
doi: 10.1111/echo.13163
Vasaiwala SC, Finn C, Delpriore J et al (2009) Prospective study of cardiac sarcoid mimicking arrhythmogenic right ventricular dysplasia. J Cardiovasc Electrophysiol 20(5):473–476. https://doi.org/10.1111/j.1540-8167.2008.01351.x
doi: 10.1111/j.1540-8167.2008.01351.x
pubmed: 19017339
Aggarwal NR, Snipelisky D, Young PM, Gersh BJ, Cooper LT, Chareonthaitawee P (2015) Advances in imaging for diagnosis and management of cardiac sarcoidosis. Eur Heart J Cardiovasc Imaging 16(9):949–958. https://doi.org/10.1093/ehjci/jev142
doi: 10.1093/ehjci/jev142
pubmed: 26104960
Saleh Y, Abdelkarim O, Herzallah K, Abela GS (2020) Anthracycline-induced cardiotoxicity: mechanisms of action, incidence, risk factors, prevention, and treatment. Heart Fail Rev. https://doi.org/10.1007/s10741-020-09968-2
Murtagh G, Laffin LJ, Patel KV et al (2016) Improved detection of myocardial damage in sarcoidosis using longitudinal strain in patients with preserved left ventricular ejection fraction. Echocardiography (Mount Kisco, NY) 33(9):1344–1352. https://doi.org/10.1111/echo.13281
doi: 10.1111/echo.13281
Felekos I, Aggeli C, Gialafos E et al (2018) Global longitudinal strain and long-term outcomes in asymptomatic extracardiac sarcoid patients with no apparent cardiovascular disease. Echocardiography (Mount Kisco, NY) 35(6):804–808. https://doi.org/10.1111/echo.13846
doi: 10.1111/echo.13846
Al-Mallah MH, Shareef MN (2011) The role of cardiac magnetic resonance imaging in the assessment of non-ischemic cardiomyopathy. Heart Fail Rev 16(4):369–380. https://doi.org/10.1007/s10741-010-9221-3
doi: 10.1007/s10741-010-9221-3
pubmed: 21170585
Patel MR, Cawley PJ, Heitner JF et al (2009) Detection of myocardial damage in patients with sarcoidosis. Circulation 120(20):1969–1977. https://doi.org/10.1161/circulationaha.109.851352
doi: 10.1161/circulationaha.109.851352
pubmed: 19884472
pmcid: 2778859
Smedema JP, Snoep G, van Kroonenburgh MP et al (2005) Evaluation of the accuracy of gadolinium-enhanced cardiovascular magnetic resonance in the diagnosis of cardiac sarcoidosis. J Am Coll Cardiol 45(10):1683–1690. https://doi.org/10.1016/j.jacc.2005.01.047
doi: 10.1016/j.jacc.2005.01.047
pubmed: 15893188
Crawford T, Mueller G, Sarsam S et al (2014) Magnetic resonance imaging for identifying patients with cardiac sarcoidosis and preserved or mildly reduced left ventricular function at risk of ventricular arrhythmias. Circ Arrhythm Electrophysiol 7(6):1109–1115. https://doi.org/10.1161/circep.113.000156
doi: 10.1161/circep.113.000156
pubmed: 25266311
Aljizeeri A, Sulaiman A, Alhulaimi N, Alsaileek A, Al-Mallah MH (2017) Cardiac magnetic resonance imaging in heart failure: where the alphabet begins! Heart Fail Rev 22(4):385–399. https://doi.org/10.1007/s10741-017-9609-4
doi: 10.1007/s10741-017-9609-4
pubmed: 28432605
Nishiyama Y, Yamamoto Y, Fukunaga K et al (2006) Comparative evaluation of 18F-FDG PET and 67Ga scintigraphy in patients with sarcoidosis. J Nucl Med 47(10):1571–1576
pubmed: 17015889
Yamagishi H, Shirai N, Takagi M et al (2003) Identification of cardiac sarcoidosis with (13)N-NH(3)/(18)F-FDG PET. J Nucl Med 44(7):1030–1036
pubmed: 12843216
El-Tallawi KC, Parikh R, Nabi F, Maclayton PI, Trachtenberg BH, Al-Mallah M (2020) A positive Tc-99m PYP scan in a patient with cardiac sarcoidosis. J Nucl Cardiol. https://doi.org/10.1007/s12350-020-02158-5
Treglia G, Annunziata S, Sobic-Saranovic D, Bertagna F, Caldarella C, Giovanella L (2014) The role of 18F-FDG-PET and PET/CT in patients with sarcoidosis: an updated evidence-based review. Acad Radiol 21(5):675–684. https://doi.org/10.1016/j.acra.2014.01.008
doi: 10.1016/j.acra.2014.01.008
pubmed: 24703482
Dorbala S, Di Carli MF, Delbeke D et al (2013) SNMMI/ASNC/SCCT guideline for cardiac SPECT/CT and PET/CT 1.0. J Nucl Med 54(8):1485–1507. https://doi.org/10.2967/jnumed.112.105155
Scholtens AM, Verberne HJ, Budde RP, Lam MG (2016) Additional heparin preadministration improves cardiac glucose metabolism suppression over low-carbohydrate diet alone in 18F-FDG PET imaging. J Nucl Med 57(4):568–573. https://doi.org/10.2967/jnumed.115.166884
doi: 10.2967/jnumed.115.166884
pubmed: 26659348
Okumura W, Iwasaki T, Toyama T et al (2004) Usefulness of fasting 18F-FDG PET in identification of cardiac sarcoidosis. J Nucl Med 45(12):1989–1998
pubmed: 15585472
Khalaf S, Al-Mallah MH (2020) Fluorodeoxyglucose applications in cardiac PET: viability, inflammation, infection, and beyond. Methodist Debakey Cardiovasc J 16(2):122–129. https://doi.org/10.14797/mdcj-16-2-122
doi: 10.14797/mdcj-16-2-122
pubmed: 32670472
pmcid: 7350806
Osborne MT, Hulten EA, Murthy VL et al (2017) Patient preparation for cardiac fluorine-18 fluorodeoxyglucose positron emission tomography imaging of inflammation. J Nucl Cardiol 24(1):86–99. https://doi.org/10.1007/s12350-016-0502-7
doi: 10.1007/s12350-016-0502-7
pubmed: 27277502
Osborne MT, Hulten EA, Singh A et al (2014) Reduction in 18 F-fluorodeoxyglucose uptake on serial cardiac positron emission tomography is associated with improved left ventricular ejection fraction in patients with cardiac sarcoidosis. J Nucl Cardiol 21(1):166–174. https://doi.org/10.1007/s12350-013-9828-6
doi: 10.1007/s12350-013-9828-6
pubmed: 24307261
Rosenthal DG, Parwani P, Murray TO et al (2019) Long-term corticosteroid-sparing immunosuppression for cardiac sarcoidosis. J Am Heart Assoc 8(18):e010952. https://doi.org/10.1161/jaha.118.010952
Nekolla SG, Martinez-Moeller A, Saraste A (2009) PET and MRI in cardiac imaging: from validation studies to integrated applications. Eur J Nucl Med Mol Imaging 36(Suppl 1):S121–S130. https://doi.org/10.1007/s00259-008-0980-1
doi: 10.1007/s00259-008-0980-1
pubmed: 19104798
Dweck MR, Abgral R, Trivieri MG et al (2018) Hybrid magnetic resonance imaging and positron emission tomography with fluorodeoxyglucose to diagnose active cardiac sarcoidosis. JACC Cardiovasc Imaging 11(1):94–107. https://doi.org/10.1016/j.jcmg.2017.02.021
doi: 10.1016/j.jcmg.2017.02.021
pubmed: 28624396
Vita T, Okada DR, Veillet-Chowdhury M et al (2018) Complementary value of cardiac magnetic resonance imaging and positron emission tomography/computed tomography in the assessment of cardiac sarcoidosis. Circ Cardiovasc Imaging 11(1):e007030. https://doi.org/10.1161/circimaging.117.007030
doi: 10.1161/circimaging.117.007030
pubmed: 29335272
pmcid: 6381829