Sex-specific differences in myocardial injury incidence after COVID-19 mRNA-1273 booster vaccination.
COVID-19
COVID-19 booster vaccination
Cardiac troponin
Myocardial injury
Myocarditis
mRNA vaccine
Journal
European journal of heart failure
ISSN: 1879-0844
Titre abrégé: Eur J Heart Fail
Pays: England
ID NLM: 100887595
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
revised:
04
07
2023
received:
13
03
2023
accepted:
05
07
2023
medline:
1
11
2023
pubmed:
20
7
2023
entrez:
20
7
2023
Statut:
ppublish
Résumé
To explore the incidence and potential mechanisms of oligosymptomatic myocardial injury following COVID-19 mRNA booster vaccination. Hospital employees scheduled to undergo mRNA-1273 booster vaccination were assessed for mRNA-1273 vaccination-associated myocardial injury, defined as acute dynamic increase in high-sensitivity cardiac troponin T (hs-cTnT) concentration above the sex-specific upper limit of normal on day 3 (48-96 h) after vaccination without evidence of an alternative cause. To explore possible mechanisms, antibodies against interleukin-1 receptor antagonist (IL-1RA), the SARS-CoV-2-nucleoprotein (NP) and -spike (S1) proteins and an array of 14 inflammatory cytokines were quantified. Among 777 participants (median age 37 years, 69.5% women), 40 participants (5.1%; 95% confidence interval [CI] 3.7-7.0%) had elevated hs-cTnT concentration on day 3 and mRNA-1273 vaccine-associated myocardial injury was adjudicated in 22 participants (2.8% [95% CI 1.7-4.3%]). Twenty cases occurred in women (3.7% [95% CI 2.3-5.7%]), two in men (0.8% [95% CI 0.1-3.0%]). Hs-cTnT elevations were mild and only temporary. No patient had electrocardiographic changes, and none developed major adverse cardiac events within 30 days (0% [95% CI 0-0.4%]). In the overall booster cohort, hs-cTnT concentrations (day 3; median 5, interquartile range [IQR] 4-6 ng/L) were significantly higher compared to matched controls (n = 777, median 3 [IQR 3-5] ng/L, p < 0.001). Cases had comparable systemic reactogenicity, concentrations of anti-IL-1RA, anti-NP, anti-S1, and markers quantifying systemic inflammation, but lower concentrations of interferon (IFN)-λ1 (IL-29) and granulocyte-macrophage colony-stimulating factor (GM-CSF) versus persons without vaccine-associated myocardial injury. mRNA-1273 vaccine-associated myocardial injury was more common than previously thought, being mild and transient, and more frequent in women versus men. The possible protective role of IFN-λ1 (IL-29) and GM-CSF warrant further studies.
Substances chimiques
2019-nCoV Vaccine mRNA-1273
EPK39PL4R4
Granulocyte-Macrophage Colony-Stimulating Factor
83869-56-1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1871-1881Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2023 The Authors. European Journal of Heart Failure published by John Wiley & Sons Ltd on behalf of European Society of Cardiology.
Références
Heidecker B, Dagan N, Balicer R, Eriksson U, Rosano G, Coats A, et al. Myocarditis following COVID-19 vaccine: Incidence, presentation, diagnosis, pathophysiology, therapy, and outcomes put into perspective. A clinical consensus document supported by the Heart Failure Association of the European Society of Cardiology (ESC) and the ESC Working Group on Myocardial and Pericardial Diseases. Eur J Heart Fail 2022;24:2000-2018. https://doi.org/10.1002/ejhf.2669
Goyal M, Ray I, Mascarenhas D, Kunal S, Sachdeva RA, Ish P. Myocarditis post-SARS-CoV-2 vaccination: A systematic review. QJM 2023;116:7-25. https://doi.org/10.1093/qjmed/hcac064
Wong HL, Hu M, Zhou CK, Lloyd PC, Amend KL, Beachler DC, et al. Risk of myocarditis and pericarditis after the COVID-19 mRNA vaccination in the USA: A cohort study in claims databases. Lancet 2022;399:2191-2199. https://doi.org/10.1016/S0140-6736(22)00791-7
Ferdinands JM, Rao S, Dixon BE, Mitchell PK, DeSilva MB, Irving SA, et al. Waning 2-dose and 3-dose effectiveness of mRNA vaccines against COVID-19-associated emergency department and urgent care encounters and hospitalizations among adults during periods of Delta and Omicron variant predominance - VISION Network, 10 states, August 2021-January 2022. MMWR Morb Mortal Wkly Rep 2022;71:255-263. https://doi.org/10.15585/mmwr.mm7107e2
Canetti M, Barda N, Gilboa M, Indenbaum V, Asraf K, Gonen T, et al. Six-month follow-up after a fourth BNT162b2 vaccine dose. N Engl J Med 2022;387:2092-2094. https://doi.org/10.1056/NEJMc2211283
Mueller D, Puelacher C, Honegger U, Walter JE, Badertscher P, Schaerli N, et al. Direct comparison of cardiac troponin T and I using a uniform and a sex-specific approach in the detection of functionally relevant coronary artery disease. Clin Chem 2018;64:1596-1606. https://doi.org/10.1373/clinchem.2018.286971
Giannitsis E, Kurz K, Hallermayer K, Jarausch J, Jaffe AS, Katus HA. Analytical validation of a high-sensitivity cardiac troponin T assay. Clin Chem 2010;56:254-261. https://doi.org/10.1373/clinchem.2009.132654
Thurner L, Kessel C, Fadle N, Regitz E, Seidel F, Kindermann I, et al. IL-1RA antibodies in myocarditis after SARS-CoV-2 vaccination. N Engl J Med 2022;387:1524-1527. https://doi.org/10.1056/NEJMc2205667
Hirsiger JR, Weigang S, Walz AC, Fuchs J, Daly ML, Eggimann S, et al. Passive immunization against COVID-19 by anti-SARS-CoV-2 spike IgG in commercially available immunoglobulin preparations in severe antibody deficiency. J Allergy Clin Immunol 2022;10:2452-2455.e3. https://doi.org/10.1016/j.jaip.2022.06.020
Prepoudis A, Koechlin L, Nestelberger T, Boeddinghaus J, Lopez-Ayala P, Wussler D, et al. Incidence, clinical presentation, management, and outcome of acute pericarditis and myopericarditis. Eur Heart J Acute Cardiovasc Care 2022;11:137-147. https://doi.org/10.1093/ehjacc/zuab108
Zhang L, Awadalla M, Mahmood SS, Nohria A, Hassan MZO, Thuny F, et al. Cardiovascular magnetic resonance in immune checkpoint inhibitor-associated myocarditis. Eur Heart J 2020;41:1733-1743. https://doi.org/10.1093/eurheartj/ehaa051
Ho D, Imai K, King G, Stuart EA. MatchIt: Nonparametric preprocessing for parametric causal inference. J Stat Softw 2011;42:1-28. https://doi.org/10.18637/jss.v042.i08
Sexson Tejtel SK, Munoz FM, Al-Ammouri I, Savorgnan F, Guggilla RK, Khuri-Bulos N, et al. Myocarditis and pericarditis: Case definition and guidelines for data collection, analysis, and presentation of immunization safety data. Vaccine 2022;40:1499-1511. https://doi.org/10.1016/j.vaccine.2021.11.074
Cordero A, Cazorla D, Escribano D, Quintanilla MA, López-Ayala JM, Berbel PP, et al. Myocarditis after RNA-based vaccines for coronavirus. Int J Cardiol 2022;353:131-134. https://doi.org/10.1016/j.ijcard.2022.01.037
Haaf P, Kuster GM, Mueller C, Berger CT, Monney P, Burger P, et al. The very low risk of myocarditis and pericarditis after mRNA COVID-19 vaccination should not discourage vaccination. Swiss Med Wkly 2021;151:w30087. https://doi.org/10.4414/smw.2021.w30087
Penna C, Mercurio V, Tocchetti CG, Pagliaro P. Sex-related differences in COVID-19 lethality. Br J Pharmacol 2020;177:4375-4385. https://doi.org/10.1111/bph.15207
Feld JJ, Kandel C, Biondi MJ, Kozak RA, Zahoor MA, Lemieux C, et al. Peginterferon lambda for the treatment of outpatients with COVID-19: A phase 2, placebo-controlled randomised trial. Lancet Respir Med 2021;9:498-510. https://doi.org/10.1016/s2213-2600(20)30566-x
Santer DM, Li D, Ghosheh Y, Zahoor MA, Prajapati D, Hansen BE, et al. Interferon-λ treatment accelerates SARS-CoV-2 clearance despite age-related delays in the induction of T cell immunity. Nat Commun 2022;13:6992. https://doi.org/10.1038/s41467-022-34709-4
Lang FM, Lee KM, Teijaro JR, Becher B, Hamilton JA. GM-CSF-based treatments in COVID-19: Reconciling opposing therapeutic approaches. Nat Rev Immunol 2020;20:507-514. https://doi.org/10.1038/s41577-020-0357-7
Galani IE, Triantafyllia V, Eleminiadou EE, Koltsida O, Stavropoulos A, Manioudaki M, et al. Interferon-λ mediates non-redundant front-line antiviral protection against influenza virus infection without compromising host fitness. Immunity 2017;46:875-890.e6. https://doi.org/10.1016/j.immuni.2017.04.025
Chrysanthopoulou A, Kambas K, Stakos D, Mitroulis I, Mitsios A, Vidali V, et al. Interferon lambda1/IL-29 and inorganic polyphosphate are novel regulators of neutrophil-driven thromboinflammation. J Pathol 2017;243:111-122. https://doi.org/10.1002/path.4935
Reis G, Moreira Silva EAS, Medeiros Silva DC, Thabane L, Campos VHS, Ferreira TS, et al.; TOGETHER Investigators. Early treatment with pegylated interferon lambda for Covid-19. N Engl J Med 2023;388:518-528. https://doi.org/10.1056/NEJMoa2209760
Altman NL, Berning AA, Saxon CE, Adamek KE, Wagner JA, Slavov D, et al. Myocardial injury and altered gene expression associated with SARS-CoV-2 infection or mRNA vaccination. JACC Basic Transl Sci 2023;8:124-137. https://doi.org/10.1016/j.jacbts.2022.08.005
Levi N, Moravsky G, Weitsman T, Amsalem I, Bar-Sheshet Itach S, Algur N, et al. A prospective study on myocardial injury after BNT162b2 mRNA COVID-19 fourth dose vaccination in healthy persons. Eur J Heart Fail 2023;25:313-318. https://doi.org/10.1002/ejhf.2687
Mansanguan S, Charunwatthana P, Piyaphanee W, Dechkhajorn W, Poolcharoen A, Mansanguan C. Cardiovascular manifestation of the BNT162b2 mRNA COVID-19 vaccine in adolescents. Trop Med Infect Dis 2022;7:196. https://doi.org/10.3390/tropicalmed7080196
Patone M, Mei XW, Handunnetthi L, Dixon S, Zaccardi F, Shankar-Hari M, et al. Risks of myocarditis, pericarditis, and cardiac arrhythmias associated with COVID-19 vaccination or SARS-CoV-2 infection. Nat Med 2022;28:410-422. https://doi.org/10.1038/s41591-021-01630-0
Naveed Z, Li J, Wilton J, Spencer M, Naus M, García HAV, et al. Comparative risk of myocarditis/pericarditis following second doses of BNT162b2 and mRNA-1273 coronavirus vaccines. J Am Coll Cardiol 2022;80:1900-1908. https://doi.org/10.1016/j.jacc.2022.08.799
Dickerman BA, Gerlovin H, Madenci AL, Kurgansky KE, Ferolito BR, Figueroa Muñiz MJ, et al. Comparative effectiveness of BNT162b2 and mRNA-1273 vaccines in U.S. veterans. N Engl J Med 2021;386:105-115. https://doi.org/10.1056/NEJMoa2115463
Islam N, Sheils NE, Jarvis MS, Cohen K. Comparative effectiveness over time of the mRNA-1273 (Moderna) vaccine and the BNT162b2 (Pfizer-BioNTech) vaccine. Nat Commun 2022;13:2377. https://doi.org/10.1038/s41467-022-30059-3
Arness MK, Eckart RE, Love SS, Atwood JE, Wells TS, Engler RJ, et al. Myopericarditis following smallpox vaccination. Am J Epidemiol 2004;160:642-651. https://doi.org/10.1093/aje/kwh269
Ling RR, Ramanathan K, Tan FL, Tai BC, Somani J, Fisher D, et al. Myopericarditis following COVID-19 vaccination and non-COVID-19 vaccination: A systematic review and meta-analysis. Lancet Respir Med 2022;10:679-688. https://doi.org/10.1016/s2213-2600(22)00059-5
Engler RJ, Nelson MR, Collins LC Jr, Spooner C, Hemann BA, Gibbs BT, et al. A prospective study of the incidence of myocarditis/pericarditis and new onset cardiac symptoms following smallpox and influenza vaccination. PLoS One 2015;10:e0118283. https://doi.org/10.1371/journal.pone.0118283
Patone M, Mei XW, Handunnetthi L, Dixon S, Zaccardi F, Shankar-Hari M, et al. Risk of myocarditis after sequential doses of COVID-19 vaccine and SARS-CoV-2 infection by age and sex. Circulation 2022;146:743-754. https://doi.org/10.1161/CIRCULATIONAHA.122.059970
Lai FTT, Chan EWW, Huang L, Cheung CL, Chui CSL, Li X, et al. Prognosis of myocarditis developing after mRNA COVID-19 vaccination compared with viral myocarditis. J Am Coll Cardiol 2022;80:2255-2265. https://doi.org/10.1016/j.jacc.2022.09.049
Heymans S, Dawson D, Fuster V, Metra M, Tocchetti CG. Myocarditis following SARS-CoV2 mRNA vaccination against COVID-19: Facts and open questions. J Am Coll Cardiol 2022;80:1363-1365. https://doi.org/10.1016/j.jacc.2022.08.003
Moreira ED, Kitchin N, Xu X, Dychter SS, Lockhart S, Gurtman A, et al. Safety and efficacy of a third dose of BNT162b2 Covid-19 vaccine. N Engl J Med 2022;386:1910-1921. https://doi.org/10.1056/NEJMoa2200674
Task Force for the management of COVID-19 of the European Society of Cardiology. European Society of Cardiology guidance for the diagnosis and management of cardiovascular disease during the COVID-19 pandemic: Part 1-epidemiology, pathophysiology, and diagnosis. Eur Heart J 2022;43:1033-1058. https://doi.org/10.1093/eurheartj/ehab696
Rosano G, Jankowska EA, Ray R, Metra M, Abdelhamid M, Adamopoulos S, et al. COVID-19 vaccination in patients with heart failure: A position paper of the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail 2021;23:1806-1818. https://doi.org/10.1002/ejhf.2356
Itzhaki Ben Zadok O, Shaul AA, Ben-Avraham B, Yaari V, Ben Zvi H, Shostak Y, et al. Immunogenicity of the BNT162b2 mRNA vaccine in heart transplant recipients - A prospective cohort study. Eur J Heart Fail 2021;23:1555-1559. https://doi.org/10.1002/ejhf.2199
Puelacher C, Buse GL, Seeberger D, Sazgary L, Marbot S, Lampart A, et al. Perioperative myocardial injury after noncardiac surgery. Circulation 2018;137:1221-1232. https://doi.org/10.1161/CIRCULATIONAHA.117.030114
Mueller C, Giannitsis E, Jaffe AS, Huber K, Mair J, Cullen L, et al. Cardiovascular biomarkers in patients with COVID-19. Eur Heart J Acute Cardiovasc Care 2021;10:310-319. https://doi.org/10.1093/ehjacc/zuab009
Sandoval Y, Januzzi JL, Jaffe AS. Cardiac troponin for assessment of myocardial injury in COVID-19: JACC review topic of the week. J Am Coll Cardiol 2020;76:1244-1258. https://doi.org/10.1016/j.jacc.2020.06.068
Sou SM, Puelacher C, Twerenbold R, Wagener M, Honegger U, Reichlin T, et al. Direct comparison of cardiac troponin I and cardiac troponin T in the detection of exercise-induced myocardial ischemia. Clin Biochem 2016;49:421-432. https://doi.org/10.1016/j.clinbiochem.2015.12.005
du Fay de Lavallaz J, Zehntner T, Puelacher C, Walter J, Strebel I, Rentsch K, et al. Rhabdomyolysis: A noncardiac source of increased circulating concentrations of cardiac troponin T? J Am Coll Cardiol 2018;72:2936-2937. https://doi.org/10.1016/j.jacc.2018.09.050
du Fay de Lavallaz J, Prepoudis A, Wendebourg MJ, Kesenheimer E, Kyburz D, Daikeler T, et al.; BASEL XII Investigators. Skeletal muscle disorders: A noncardiac source of cardiac troponin T. Circulation 2022;145:1764-1779. https://doi.org/10.1161/CIRCULATIONAHA.121.058489
Giger RD, du Fay de Lavallaz J, Prepoudis A, Stoll T, Lopez-Ayala P, Glarner N, et al. Rhabdomyolysis: A noncardiac source of increased circulating concentrations of cardiac troponin T? J Am Coll Cardiol 2020;76:2685-2687. https://doi.org/10.1016/j.jacc.2020.08.088
Bularga A, Oskoui E, Fujisawa T, Jenks S, Sutherland R, Apple FS, et al. Macrotroponin complex as a cause for cardiac troponin increase after COVID-19 vaccination and infection. Clin Chem 2022;68:1015-1019. https://doi.org/10.1093/clinchem/hvac100
Thygesen K, Alpert JS, Jaffe AS, Chaitman BR, Bax JJ, Morrow DA, et al. ESC Scientific Document Group. Fourth universal definition of myocardial infarction (2018). Eur Heart J 2019;40:237-269. https://doi.org/10.1093/eurheartj/ehy462