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Clinlcal Guidelines & Expert Consensus
Consensus of Chinese experts on cardiovascular MRI in evaluating immune-related adverse cardiac events associated with immune checkpoint inhibitors for malignant tumors
Molecular Imaging Group of Chinese Society of Radiology of Chinese Medical Association
MRI Group of Chinese Society of Radiology Chinese Medical Association
Cardiac-Chest Group of Chinese Society of Radiology Chinese Medical Association
Editorial Board of Chinese Journal of Magnetic Resonance Imaging

Cite this article as: Molecular Imaging Group of Chinese Society of Radiology of Chinese Medical Association, MRI Group of Chinese Society of Radiology Chinese Medical Association, Cardiac-Chest Group of Chinese Society of Radiology Chinese Medical Association, et al. Consensus of Chinese experts on cardiovascular MRI in evaluating immune-related adverse cardiac events associated with immune checkpoint inhibitors for malignant tumors[J]. Chin J Magn Reson Imaging, 2024, 15(12): 10-18. DOI:10.12015/issn.1674-8034.2024.12.002.


[Abstract] In recent years, cancer immunotherapy, particularly immune checkpoint inhibitors (ICIs), has emerged as a significant breakthrough in the treatment of malignant tumors, substantially improving patient outcomes. However, the potential of ICIs to trigger immune-related adverse events (irAEs), including cardiovascular toxicity, poses a significant challenge to cancer immunotherapy. Although the incidence is low, the mortality rate is high. With the increasing use of ICIs, cases of cardiovascular irAEs are on the rise, necessitating the attention of both imaging and clinical physicians. MRI, with its high sensitivity and resolution, plays a pivotal role in the detection and assessment of cardiovascular irAEs. Early diagnosis and evaluation of cardiovascular irAEs through MRI are crucial for patient treatment and prognosis. However, there is currently a lack of unified standardized consensus in China regarding MRI examination and diagnosis of cardiovascular irAEs caused by ICIs. To address this issue, the Molecular Imaging Group, Magnetic Resonance Group, and Cardiothoracic Group of the Radiology Branch of the Chinese Medical Association, in collaboration with the Editorial Board of Chinese Journal of Magnetic Resonance Imaging, have developed a consensus on MRI examination protocols and diagnostic reporting for cardiovascular system irAEs induced by ICIs. This consensus aims to provide a scientific basis for imaging and clinical physicians and to promote the application of MRI technology in the diagnosis of cardiovascular system irAEs.
[Keywords] magnetic resonance imaging;immune checkpoint inhibitors;cardiac events associated with Immune checkpoint inhibitors;clinical application;expert consensus

Molecular Imaging Group of Chinese Society of Radiology of Chinese Medical Association   MRI Group of Chinese Society of Radiology Chinese Medical Association   Cardiac-Chest Group of Chinese Society of Radiology Chinese Medical Association   Editorial Board of Chinese Journal of Magnetic Resonance Imaging  

Corresponding author: SUN H Z (Department of Radiology, Shengjing Hospital Affiliated to China Medical University, Shenyang 110004, China), E-mail: sunhongzan@126.com JU S H (Department of Radiology, Zhongda Hospital Affiliated to Southeast University, Nanjing 210009, China), E-mail: jsh@seu.edu.cn

Conflicts of interest   None.

Received  2024-10-01
Accepted  2024-12-10
DOI: 10.12015/issn.1674-8034.2024.12.002
Cite this article as: Molecular Imaging Group of Chinese Society of Radiology of Chinese Medical Association, MRI Group of Chinese Society of Radiology Chinese Medical Association, Cardiac-Chest Group of Chinese Society of Radiology Chinese Medical Association, et al. Consensus of Chinese experts on cardiovascular MRI in evaluating immune-related adverse cardiac events associated with immune checkpoint inhibitors for malignant tumors[J]. Chin J Magn Reson Imaging, 2024, 15(12): 10-18. DOI:10.12015/issn.1674-8034.2024.12.002.

[1]
BAGCHI S, YUAN R, ENGLEMAN E G. Immune checkpoint inhibitors for the treatment of cancer: clinical impact and mechanisms of response and resistance[J]. Annu Rev Pathol, 2021, 16: 223-249. DOI: 10.1146/annurev-pathol-042020-042741.
[2]
THOMPSON J A, SCHNEIDER B J, BRAHMER J, et al. NCCN guidelines insights: management of immunotherapy-related toxicities, version 1.2020[J]. J Natl Compr Canc Netw, 2020, 18(3): 230-241. DOI: 10.6004/jnccn.2020.0012.
[3]
WANG D, BAUERSACHS J, BERLINER D. Immune checkpoint inhibitor associated myocarditis and cardiomyopathy: A translational review[J/OL]. Biology, 2023, 12(3): 472 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/36979163/. DOI: 10.3390/biology12030472.
[4]
JOHNSON D B, BALKO J M, COMPTON M L, et al. Fulminant myocarditis with combination immune checkpoint blockade[J]. N Engl J Med, 2016, 375(18): 1749-1755. DOI: 10.1056/NEJMoa1609214.
[5]
D'SOUZA M, NIELSEN D, SVANE I M, et al. The risk of cardiac events in patients receiving immune checkpoint inhibitors: a nationwide Danish study[J]. Eur Heart J, 2021, 42(16): 1621-1631. DOI: 10.1093/eurheartj/ehaa884.
[6]
SALEM J E, MANOUCHEHRI A, MOEY M, et al. Cardiovascular toxicities associated with immune checkpoint inhibitors: an observational, retrospective, pharmacovigilance study[J]. Lancet Oncol, 2018, 19(12): 1579-1589. DOI: 10.1016/S1470-2045(18)30608-9.
[7]
MAHMOOD S S, FRADLEY M G, COHEN J V, et al. Myocarditis in patients treated with immune checkpoint inhibitors[J]. J Am Coll Cardiol, 2018, 71(16): 1755-1764. DOI: 10.1016/j.jacc.2018.02.037.
[8]
ATALLAH-YUNES S A, KADADO A J, KAUFMAN G P, et al. Immune checkpoint inhibitor therapy and myocarditis: a systematic review of reported cases[J]. J Cancer Res Clin Oncol, 2019, 145(6): 1527-1557. DOI: 10.1007/s00432-019-02927-x.
[9]
YUN S, VINCELETTE N D, MANSOUR I, et al. Late onset ipilimumab-induced pericarditis and pericardial effusion: a rare but life threatening complication[J/OL]. Case Rep Oncol Med, 2015, 2015: 794842 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/25918658/. DOI: 10.1155/2015/794842.
[10]
KONG X Y, CHEN L, SU Z H, et al. Toxicities associated with immune checkpoint inhibitors: a systematic study[J]. Int J Surg, 2023, 109(6): 1753-1768. DOI: 10.1097/JS9.0000000000000368.
[11]
BERZ A M, BOUGHDAD S, VIETTI-VIOLI N, et al. Imaging assessment of toxicity related to immune checkpoint inhibitors[J/OL]. Front Immunol, 2023, 14: 1133207 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/36911692/. DOI: 10.3389/fimmu.2023.1133207.
[12]
FARON A, ISAAK A, MESROPYAN N, et al. Cardiac MRI depicts immune checkpoint inhibitor-induced myocarditis: a prospective study[J]. Radiology, 2021, 301(3): 602-609. DOI: 10.1148/radiol.2021210814.
[13]
FERREIRA V M, SCHULZ-MENGER J, HOLMVANG G, et al. Cardiovascular magnetic resonance in NonischemicMyocardial inflammation: expert recommendations[J]. J Am Coll Cardiol, 2018, 72(24): 3158-3176. DOI: 10.1016/j.jacc.2018.09.072.
[14]
THAVENDIRANATHAN P, ZHANG L L, ZAFAR A, et al. Myocardial T1 and T2 mapping by magnetic resonance in PatientsWithImmune checkpoint inhibitor-associated myocarditis[J]. J Am Coll Cardiol, 2021, 77(12): 1503-1516. DOI: 10.1016/j.jacc.2021.01.050.
[15]
PALASKAS N, LOPEZ-MATTEI J, DURAND J B, et al. Immune checkpoint inhibitor myocarditis: pathophysiological characteristics, diagnosis, and treatment[J/OL]. J Am Heart Assoc, 2020, 9(2): e013757 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/31960755/. DOI: 10.1161/JAHA.119.013757.
[16]
SHARMA A, ALEXANDER G, CHU J H, et al. Immune checkpoint inhibitors and cardiotoxicity: a comparative meta-analysis of observational studies and randomized controlled trials[J/OL]. J Am Heart Assoc, 2024, 13(10): e032620 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/38761070/. DOI: 10.1161/JAHA.123.032620.
[17]
PALASKAS N L, ALI H J, KOUTROUMPAKIS E, et al. Cardiovascular toxicity of immune therapies for cancer[J/OL]. BMJ, 2024, 385: e075859 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/38749554/. DOI: 10.1136/bmj-2023-075859.
[18]
TAMURA Y, TAMURA Y, TAKEMURA R, et al. Longitudinal strain and troponin I elevation in patients undergoing immune checkpoint inhibitor therapy[J]. JACC CardioOncol, 2022, 4(5): 673-685. DOI: 10.1016/j.jaccao.2022.10.007.
[19]
MOSLEHI J J, SALEM J E, SOSMAN J A, et al. Increased reporting of fatal immune checkpoint inhibitor-associated myocarditis[J/OL]. Lancet, 2018, 391(10124): 933 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/29536852/. DOI: 10.1016/S0140-6736(18)30533-6.
[20]
YAMAGUCHI S, MORIMOTO R, OKUMURA T, et al. Late-onset fulminant myocarditis with immune checkpoint inhibitor nivolumab[J/OL]. Can J Cardiol, 2018, 34(6): 812.e1-e3 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/29801747/. DOI: 10.1016/j.cjca.2018.03.007.
[21]
TOCCHETTI C G, FARMAKIS D, KOOP Y, et al. Cardiovascular toxicities of immune therapies for cancer - a scientific statement of the Heart Failure Association (HFA) of the ESC and the ESC Council of Cardio-Oncology[J]. Eur J Heart Fail, 2024, 26(10): 2055-2076. DOI: 10.1002/ejhf.3340.
[22]
GANATRA S, NEILAN T G. Immune checkpoint inhibitor-associated myocarditis[J]. Oncologist, 2018, 23(8): 879-886. DOI: 10.1634/theoncologist.2018-0130.
[23]
SPALLAROSSA P, TINI G, SAROCCHI M, et al. Identification and management of immune checkpoint inhibitor-related myocarditis: use troponin wisely[J]. J Clin Oncol, 2019, 37(25): 2201-2205. DOI: 10.1200/JCO.18.02464.
[24]
AWADALLA M, MAHMOOD S S, GROARKE J D, et al. Global longitudinal strain and cardiac events in patients with immune checkpoint inhibitor-related myocarditis[J]. J Am Coll Cardiol, 2020, 75(5): 467-478. DOI: 10.1016/j.jacc.2019.11.049.
[25]
EDERHY S, DEVOS P, PINNA B, et al. 18F-fluorodeoxyglucose positron emission tomography/computed tomography imaging for the diagnosis of immune checkpoint inhibitor-associated myocarditis[J]. Arch Cardiovasc Dis, 2022, 115(2): 114-116. DOI: 10.1016/j.acvd.2021.12.001.
[26]
FINKE D, HECKMANN M B, HERPEL E, et al. Early detection of checkpoint inhibitor-associated myocarditis using 68Ga-FAPI PET/CT[J/OL]. Front Cardiovasc Med, 2021, 8: 614997 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/33718446/. DOI: 10.3389/fcvm.2021.614997.
[27]
NENSA F, KLOTH J, TEZGAH E, et al. Feasibility of FDG-PET in myocarditis: comparison to CMR using integrated PET/MRI[J]. J Nucl Cardiol, 2018, 25(3): 785-794. DOI: 10.1007/s12350-016-0616-y.
[28]
OSINGA T E, OOSTING S F, VAN DER MEER P, et al. Immune checkpoint inhibitor-associated myocarditis: case reports and areview of the literature[J]. Neth Heart J, 2022, 30(6): 295-301. DOI: 10.1007/s12471-021-01655-7.
[29]
Chinese Anti-Cancer Association Integrated Oncology Cardiology Branch, Chinese Medical Association Cardiovascular Disease Branch Oncology Cardiology Group, Chinese Medical Doctor Association Cardiovascular Internal Medicine Division Oncology Cardiology Professional Committee, et al. Chinese expert consensus on the surveillance and management of immune checkpoint inhibitor-related myocarditis (2020 version)[J]. Chin J Clin Oncol, 2020, 47(20): 1027-1038. DOI: 10.3969/j.issn.1000-8179.2020.20.148.
[30]
MESSROGHLI D R, MOON J C, FERREIRA V M, et al. Clinical recommendations for cardiovascular magnetic resonance mapping of T1, T2, T2* and extracellular volume: a consensus statement by the Society for Cardiovascular Magnetic Resonance (SCMR) endorsed by the European Association for Cardiovascular Imaging (EACVI)[J/OL]. J Cardiovasc Magn Reson, 2017, 19(1): 75 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/28992817/. DOI: 10.1186/s12968-017-0389-8.
[31]
ZHANG L L, AWADALLA M, MAHMOOD S S, et al. Cardiovascular magnetic resonance in immune checkpoint inhibitor-associated myocarditis[J]. Eur Heart J, 2020, 41(18): 1733-1743. DOI: 10.1093/eurheartj/ehaa051.
[32]
CADOUR F, CAUTELA J, RAPACCHI S, et al. Cardiac MRI features and prognostic value in immune checkpoint inhibitor-induced myocarditis[J]. Radiology, 2022, 303(3): 512-521. DOI: 10.1148/radiol.211765.
[33]
LUETKENS J A, SCHLESINGER-IRSCH U, KUETTING D L, et al. Feature-tracking myocardial strain analysis in acute myocarditis: diagnostic value and association with myocardial oedema[J]. Eur Radiol, 2017, 27(11): 4661-4671. DOI: 10.1007/s00330-017-4854-4.
[34]
GONG J Y, DROBNI Z D, ZAFAR A, et al. Pericardial disease in patients treated with immune checkpoint inhibitors[J/OL]. J Immunother Cancer, 2021, 9(6): e002771 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/34145031/. DOI: 10.1136/jitc-2021-002771.
[35]
LEWINTER M M. Clinical practice. acute pericarditis[J]. N Engl J Med, 2014, 371(25): 2410-2416. DOI: 10.1056/NEJMcp1404070.
[36]
ESCUDIER M, CAUTELA J, MALISSEN N, et al. Clinical features, management, and outcomes of immune checkpoint inhibitor-related cardiotoxicity[J]. Circulation, 2017, 136(21): 2085-2087. DOI: 10.1161/CIRCULATIONAHA.117.030571.
[37]
BALL S, GHOSH R K, WONGSAENGSAK S, et al. Cardiovascular toxicities of immune checkpoint inhibitors: JACC review topic of the week[J]. J Am Coll Cardiol, 2019, 74(13): 1714-1727. DOI: 10.1016/j.jacc.2019.07.079.
[38]
LYON A R, YOUSAF N, BATTISTI N M L, et al. Immune checkpoint inhibitors and cardiovascular toxicity[J/OL]. Lancet Oncol, 2018, 19(9): e447-e458 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/30191849/. DOI: 10.1016/S1470-2045(18)30457-1.
[39]
ADLER Y, CHARRON P, IMAZIO M, et al. 2015 ESC Guidelines for the diagnosis and management of pericardial diseases: the Task Force for the Diagnosis and Management of Pericardial Diseases of the European Society of Cardiology (ESC)Endorsed by: the European Association for Cardio-Thoracic Surgery (EACTS)[J]. Eur Heart J, 2015, 36(42): 2921-2964. DOI: 10.1093/eurheartj/ehv318.
[40]
ALTAN M, TOKI M I, GETTINGER S N, et al. Immune checkpoint inhibitor-associated pericarditis[J]. J Thorac Oncol, 2019, 14(6): 1102-1108. DOI: 10.1016/j.jtho.2019.02.026.
[41]
MORIYAMA S, FUKATA M, TATSUMOTO R, et al. Refractory constrictive pericarditis caused by an immune checkpoint inhibitor properly managed with infliximab: a case report[J/OL]. Eur Heart J Case Rep, 2021, 5(1): ytab002 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/33644656/. DOI: 10.1093/ehjcr/ytab002.
[42]
CREMER P C, KLEIN A L, IMAZIO M. Diagnosis, risk stratification, and treatment of pericarditis: a review[J]. JAMA, 2024, 332(13): 1090-1100. DOI: 10.1001/jama.2024.12935.
[43]
ZHENG Y, LIU T. Interpretation of consensus on assessment and management of acute coronary syndrome and acute pericardial disease by ESC Committee of Cardiac Oncology[J]. Chin J Evid Based Cardiovasc Med, 2022, 14(5): 513-514. DOI: 10.3969/j.issn.1674-4055.2022.05.01.
[44]
ANTONOPOULOS A S, VRETTOS A, ANDROULAKIS E, et al. Cardiac magnetic resonance imaging of pericardial diseases: a comprehensive guide[J]. Eur Heart J Cardiovasc Imaging, 2023, 24(8): 983-998. DOI: 10.1093/ehjci/jead092.
[45]
CHETRIT M, XU B, KWON D H, et al. Imaging-guided therapies for PericardialDiseases[J]. JACC Cardiovasc Imaging, 2020, 13(6): 1422-1437. DOI: 10.1016/j.jcmg.2019.08.027.
[46]
IMAZIO M, ADLER Y. Management of pericardial effusion[J]. Eur Heart J, 2013, 34(16): 1186-1197. DOI: 10.1093/eurheartj/ehs372.
[47]
BRAHMER J R, LACCHETTI C, SCHNEIDER B J, et al. Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: American society of clinical oncology clinical practice guideline[J]. J Clin Oncol, 2018, 36(17): 1714-1768. DOI: 10.1200/JCO.2017.77.6385.
[48]
PATEL R P, PARIKH R, GUNTURU K S, et al. Cardiotoxicity of immune checkpoint inhibitors[J/OL]. Curr Oncol Rep, 2021, 23(7): 79 [2024-11-25]. https://pubmed.ncbi.nlm.nih.gov/33937956/. DOI: 10.1007/s11912-021-01070-6.

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