Cardiogenic Shock and Hyperinflammatory Syndrome in Young Males With COVID-19

HomeCirculation: Heart FailureVol. 13, No. 10Cardiogenic Shock and Hyperinflammatory Syndrome in Young Males With COVID-19 Free AccessCase ReportPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissionsDownload Articles + Supplements ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toSupplemental MaterialFree AccessCase ReportPDF/EPUBCardiogenic Shock and Hyperinflammatory Syndrome in Young Males With COVID-19 Vinh Q. Chau, Gennaro Giustino, Kiran Mahmood, Estefania Oliveros, Eric Neibart, Mehdi Oloomi, Noah Moss, Sumeet S. Mitter, Johanna P. Contreras, Lori Croft, Gregory Serrao, Aditya G. Parikh, Anuradha Lala, Maria G. Trivieri, Gina LaRocca, Anelechi Anyanwu, Sean P. Pinney and Donna M. Mancini Vinh Q. ChauVinh Q. Chau https://orcid.org/0000-0003-0256-6000 Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Gennaro GiustinoGennaro Giustino Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Kiran MahmoodKiran Mahmood https://orcid.org/0000-0003-1906-5958 Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Estefania OliverosEstefania Oliveros Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Eric NeibartEric Neibart Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. Department of Clinical Infectious Diseases (E.N.), Icahn School of Medicine at Mount Sinai, New York, NY. , Mehdi OloomiMehdi Oloomi Department of Cardiovascular Surgery (M.O., A.A.), Icahn School of Medicine at Mount Sinai, New York, NY. , Noah MossNoah Moss Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Sumeet S. MitterSumeet S. Mitter Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Johanna P. ContrerasJohanna P. Contreras Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Lori CroftLori Croft Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Gregory SerraoGregory Serrao Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Aditya G. ParikhAditya G. Parikh https://orcid.org/0000-0001-9485-9059 Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Anuradha LalaAnuradha Lala Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. Department of Population Health Science (A.L., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Maria G. TrivieriMaria G. Trivieri Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Gina LaRoccaGina LaRocca Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. , Anelechi AnyanwuAnelechi Anyanwu Department of Cardiovascular Surgery (M.O., A.A.), Icahn School of Medicine at Mount Sinai, New York, NY. , Sean P. PinneySean P. Pinney Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. and Donna M. ManciniDonna M. Mancini Correspondence to: Donna Mancini, MD, Division of Cardiology, Department of Medicine, Icahn School of Medicine at Mt Sinai, One Gustave L. Levy Pl, Box 1030, New York, NY 10029. Email E-mail Address: [email protected] https://orcid.org/0000-0002-6050-1785 Zena and Michael A. Wiener Cardiovascular Institute (V.Q.C., G.G., K.M., E.O., E.N., N.M., S.S.M., J.P.C., L.C., G.S., A.G.P., A.L., M.G.T.,G.L., S.P.P., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. Department of Population Health Science (A.L., D.M.M.), Icahn School of Medicine at Mount Sinai, New York, NY. Originally published26 Aug 2020https://doi.org/10.1161/CIRCHEARTFAILURE.120.007485Circulation: Heart Failure. 2020;13Other version(s) of this articleYou are viewing the most recent version of this article. Previous versions: August 26, 2020: Ahead of Print From April 20 to May 23, 2020, 7 males ranging from 20 to 42 years-old without baseline cardiovascular risk factors were admitted for high-grade fever, dyspnea, and gastrointestinal symptoms. The study was approved by our institutional review board. Continuous values were expressed as median (range). Time from symptom onset to admission was 4 days (3–21 days). Polymerase chain reaction detected severe acute respiratory syndrome coronavirus-2 (SARS-Cov-2), the virus causing coronavirus disease 2019 (COVID-19), on initial testing in 3 patients. Three patients had multiple polymerase chain reaction testing with at least one being negative for SARS-CoV-2. All patients had SARS-CoV-2 IgG antibodies (Abs) with a median titer of 1:2880 dilution (1:960 to 2880 dilution; negative titer <1:50 dilution) as measured using an assay for IgG Ab for SARS-CoV-2 developed at our institution.1Demographics, clinical presentation, laboratory findings, imaging results, treatments, and outcomes are summarized in the Table. The ethnicity/race was diverse (Middle Eastern [n=2], Black [n=2], Hispanic [n=2], and White [n=1]). The hospital courses for all patients are detailed in Figure I in the Data Supplement. All patients had severe left ventricular dysfunction and vasoplegia. They quickly progressed to mixed shock and multiorgan dysfunction necessitating inotropes, vasopressors, and intraaortic balloon pump support. Troponin I and brain natriuretic peptide levels were elevated (Figure) as were inflammatory biomarkers (Figure and Figure II in the Data Supplement). Coronary angiography was performed on 3 patients that showed normal coronary arteries but elevated left ventricular end diastolic pressures. All patients had cardiac magnetic resonance imaging (Figure IIIA through IIIG in the Data Supplement). Four patients had mild nonspecific late gadolinium enhancement, and none had myocardial edema on T2 weighted imaging.Table. Demographics, Clinical Presentation, Laboratory and Imaging Findings, Treatments, and Outcomes of PatientsReferencePatient 1Patient 2Patient 3Patient 4Patient 5Patient 6Patient 7Demographics Age, y, sex34, Male33, Male42, Male20, Male24, Male20, Male24, Male Race/EthnicityMiddle EasternBlackWhiteMiddle EasternBlackHispanicHispanicMedical history and medsNoneAlcohol abuseNoneNoneNoneNoneAlcohol AbuseClinical presentation Duration of symptom onset to admission, days203213441 Initial symptomsFever, chest pain, dyspnea, GI symptoms, neck pain, rashFever, dyspnea, GI symptoms, rashFever, chest pain, cough, rashFever, headache, GI symptoms, neck painFever, dyspneaFever, dyspnea, myalgia, GI symptoms, neck painFever, dyspnea, myalgia, GI symptoms Admission vital signsT 39.3C, BP 124/77 mm Hg, HR 123 bpm, 99% on RAT 36.3C, BP 114/67 mm Hg, HR 117 bpm, 99% on RAT 37.1C, BP 122/76 mm Hg, HR 105 bpm, 97% on RAT 37.8C, BP 91/60 mm Hg, HR 137 bpm, 100% on RAT 38.9C, BP 88/65 mm Hg, HR 130 bpm, 98% on FiO2 80%T 38.3C, BP 81/56 mm Hg, HR 137 bpm, 98% on RAT 38.6C, BP 102/51 mm Hg, HR 145 bpm, 100% on HFNC 70% at 40 L/min Maximal temperature, °C39.336.338.839.238.938.340.2Laboratory results Initial interleukin-6, pg/mL0.0–5.033372961.67.999343175.6 Follow-up interleukin-6, pg/mL*0.0–5.01.42839.45.86.51.47.3 Peak CRP, mg/L0–5.0402125326317415339309.0 Follow-up CRP, mg/L*0–5.0142.66420.6454.918.5 Peak ferritin, ng/mL30–40013 252359598311 483266032657619 Peak D-dimer, ug/mL0.0–0.53.396.41.414.23203.820 Peak troponin, ng/mL0.00–0.032.236.73.121.957.83.670.07 Peak BNP, pg/mL0.0–100.0152510 92181913935304322830Microbiology results SARS-CoV-2 PCRInitial (−20 days) detected, repeat not detected twiceInitial (−5 days) detected, repeat not detected twiceDetectedNot detected twice, repeat detectedNot detected twiceDetectedDetected SARS-CoV-2 Ab titer (dilution)28802880288096028809602880Cardiac catheterization RHC(Dobutamine) RAP 15 mm Hg. PAP 31/21 (24) mm Hg. PCWP 21 mm Hg. CO 3.2 L/min. CI 1.6 L/min/m2. SVR 1216 DynesNoneNoneNone(Epinephrine and norepinephrine) RAP 28 mm Hg. PAP 48/28 (35) mm Hg. PCWP 26 mm Hg. CO 5.7 L/min. CI 2.7 L/min/m2. SVR 486 Dynes(Epinephrine and dobutamine) RAP 11 mm Hg. PAP 42/23 (29) mm Hg. PCWP 23 mm Hg, CO 5.0 L/min. CI 3 L/min/m2. SVR 848 DynesNone LHCNormal angiogram. LVEDP 23 mm HgNoneNormal angiogram. LVEDP 28 mm HgNoneNoneNormal angiogram. LVEDP 25 mm HgNone Endomyocardial biopsyNo inflammatory cell infiltrates in myocardiumNoneNoneNoneNoneNoneNoneImaging ECGSinus tachycardia, diffuse ST elevationSinus tachycardiaSinus tachycardia, inferolateral ST elevationSinus tachycardiaAtrial fibrillationSinus tachycardiaSinus tachycardia XR/CTCT: No PE. Bilateral multifocal opacities. Cervical lymphadenopathy.XR: Mild bilateral opacities.CT: No PE. Mild atelectasis.XR: Normal.XR: Mildly diffuse bilateral opacities.XR: Normal.XR: Mild bilateral opacities. Initial TTELVEF 23%. LVEDD 5 cm. +++RV dysfunction. ++TR. +MRLVEF 35%. LVEDD 5.7 cm. Normal RV. +++MR +++TRLVEF 35%. LVEDD 6.4 cm. Inferolateral hypokinesis. +RV dysfunction. +MRLVEF 35%. LVEDD 5.5 cm. ++RV dysfunction. +MR +TRLVEF 35%, LVEDD 5.0 cm. +RV dysfunctionLVEF 20%. LVEDD 4.3 cm.+++RV dysfunctionLVEF 25-30%. LVEDD 5.5 cm. Mild LVH. Normal RV. Repeat TTELVEF 50%, normal RV. No valve disease.LVEF 50%, normal RV. No valve disease.LVEF 50%, +RV dysfunction. +MRLVEF 50%, normal RV. +MRLVEF 55%, normal RV. No valve disease.LVEF 50%, normal RV. No valve disease.LVEF 60%, normal RV. No valve disease. Cardiac MRIDay 8: LVEF, 52%. RVEF, 52%. Minimal LGE. No edema on T2W.Day 14: LVEF, 63%. RVEF, 49%. Mild LVH. No LGE. No edema on T2W.Day 6: LVEF, 55%. RVEF, 45%. Minimal LGE. No edema on T2W.Day 2: LVEF, 45%. RVEF, 35%. Minimal LGE. No edema on T2W.Day 19: LVEF, 50%. RVEF, 56%. No LGE. No edema on T2W.Day 4: LVEF, 45%. RVEF, 60%. Minimal LGE. No edema on T2W.Day 8: LVEF, 57%, RVEF, 64%. Minimal LGE. No edema on T2W.ComplicationsNoneAKI needing HDAtrial fibrillationNoneSevere ARDS (intubation, PF ratio 80). AKI needed HD. Atrial fibrillationRespiratory failure (intubation)EncephalopathyTreatment Inotrope or vasopressor useDobutamineNorepinephrine, milrinoneDobutamineNorepinephrine, dobutamineEpinephrine, norepinephrine, vasopressin, dobutamineEpinephrine, dobutaminePhenylephrine, epinephrine, dobutamine Mechanical circulatory supportIABPNoNoNoIABPIABPNo Duration of pharm/mechanical hemodynamic support, d5.533.55.52.53.77 Steroid useMethylprednisolone 1 mg/(kg·d) ×5 d, taperMethylprednisolone 1 mg/(kg·d) ×5 d, taperMethylprednisolone 1 mg/(kg·d) ×5 d, taperMethylprednisolone 1 mg/(kg·d) ×5 d, taperMethylprednisolone 1 mg/(kg·d) ×5 d, taperMethylprednisolone 1 mg/(kg·d) ×5 d, taperMethylprednisolone 1 mg/(kg·d) ×5 d, taper Convalescent plasmaNoNoNoNoNoYes (day 2)No AnticoagulationYesYesYesYesYesYesYesOutcomeDischargedDischargedDischargedDischargedDischargedDischargedDischarged Length of hospital stay, d131878101210+ denotes mild; ++, moderate; and +++, severe. AKI indicates acute kidney injury; ARDS, acute respiratory distress syndrome; BNP, brain natriuretic peptide; BP, blood pressure; CI, cardiac index; CO, cardiac output; CRP, C-reactive protein; CT, computed tomography; GI, gastrointestinal; HD, hemodialysis; HFNC, high flow nasal cannula; HR, heart rate; IABP, intraaortic balloon pump; LGE, late gadolinium enhancement; LHC, left heart catheterization; LVEDD, LV end diastolic diameter; LVEDP, left ventricular end diastolic pressure; LVEF, left ventricular ejection fraction; MR, mitral regurgitation; MRI, magnetic resonance imaging; PAP, pulmonary artery pressures; PCR, polymerase chain reaction; PCWP, pulmonary capillary wedge pressure; PE, pulmonary embolism; PF ratio, PaO2 to FiO2 ratio; RA, room air; RAP, right atrial pressures; RHC, right heart catheterization; RV, right ventricle; RVEF, RV ejection fraction; SARS-Cov-2, severe acute respiratory syndrome coronavirus-2; SVR, systemic vascular resistance; T, temperature; T2W, T2 weighted imaging; TR, tricuspid regurgitation; TTE, transthoracic echocardiogram; and XR, x-ray.* Follow-up CRP and interleukin-6 were performed 5–13 days after initial testing were done.Download figureDownload PowerPointFigure. Cardiovascular and inflammatory trends during hospitalization. Trends of left ventricular ejection fraction (LVEF; A), troponin I (B), brain natriuretic peptide (C), interleukin-6 (D), C-reactive protein (E), and ferritin (F). Latest available values reflect the latest value or discharge value. ULN indicates upper limit of normal.All patients were treated with methylprednisolone 1 mg/kg daily2 because of their elevated inflammatory biomarker profiles and all also received therapeutic anticoagulation with unfractionated or low-molecular weight heparin.3 All patients were successfully titrated off pharmacological and mechanical hemodynamic support within 3.7 days (2.5–7.0 days). Interleukin-6, C-reactive protein, and lymphopenia improved at time of discharge as did all end-organ function. Discharge ranged from 7 to 18 days after hospitalization.DiscussionTo our knowledge, we describe the first case series of young males with COVID-19 and elevated titers of SARS-CoV-2 Ab who presented with hyperinflammatory biomarker profiles and multiorgan dysfunction including biventricular failure. The profound shock exhibited by these patients resolved quickly following treatment with moderate-dose steroids, anticoagulation, and supportive care.The primary manifestations of COVID-19 in our patients were new-onset biventricular failure and vasoplegia that progressed to shock with multiorgan dysfunction. Strikingly, all patients were young males without baseline cardiovascular risk factors. The role of sex-based and genetic characteristics or other factors remains unknown in this syndrome.4 All patients had a hyperinflammatory profile which has been associated with vasoplegia and heart failure.5 Moreover, lymphopenia (and potentially high SARS-CoV-2 Ab titers) could be an indicator of a dysregulated immune system, augmenting the inflammatory cascade and tissue injury.6 Though SARS-CoV-2 Abs are presumed to have protective and neutralizing properties,1 the elevated levels of Ab could have played a pathogenic role in the observed hyperinflammatory response.6 In SARS-CoV, nonneutralizing antibodies could cause an inflammatory cascade and enhancement of viral entry via antibody-dependent enhancement mechanism.6 Alternatively, these cases may represent a new phenomenon in adults analogous to that recently described in the pediatric population.7 Several patients did have nonspecific rashes and other overlapping features though none had clinical vasculitis on coronary angiograms, and some patients had mild nonspecific late gadolinium enhancement on cardiac magnetic resonance imaging.Based on prior positions on the use of steroids in COVID-19,2,8 we used moderate-dose steroids to treat our patients with dramatic improvement in their shock and end-organ dysfunction. Systemic steroids may have a role in immune system dysregulation related to sepsis.8 We reasoned that the benefits of this therapy and low risk patient profile outweighed the morbid risk of multiorgan failure.The clinical syndrome appeared to manifest later in the course of COVID-19 disease which would differentiate it from other studies on acute myocardial injury related to COVID-19.9 The presence of elevated titers of SARS-CoV-2 Abs in our patients suggest prior viral exposure several weeks before admission.2,10 Indeed, their presentations coincided with the latter part of the COVID-19 pandemic in New York City. Taken together, the combined cardiogenic and vasodilatory shock with multiorgan dysfunction may represent a new clinical phenotype of COVID-19. This syndrome should be considered as part of the differential diagnosis in patients with hyperinflammatory biomarker profiles even if the SARS-CoV-2 polymerase chain reaction is negative and while awaiting for SARS-CoV-2 Ab titers.ConclusionsIn summary, we seek to alert the medical community about a subset of patients with COVID-19 with a novel clinical presentation of combined cardiogenic and vasodilatory shock related to a hyperinflammatory syndrome and elevated SARS-CoV-2 IgG Ab titers. This syndrome appears to be steroid responsive.AcknowledgmentsWe thank the numerous healthcare workers who have cared for our patients as well as others during the coronavirus disease 2019 (COVID-19) pandemic.DisclosuresDr Pinney serves as a consultant for Abbott Laboratories, CareDx, Medtronic, and Procyrion. Dr Serrao serves as a consultant for Procyrion. Dr Mitter has received honoraria from Abbott Laboratories and Cowen & Co. The other authors report no conflicts.FootnotesThe Data Supplement is available at https://www.ahajournals.org/doi/suppl/10.1161/CIRCHEARTFAILURE.120.007485.For Disclosures, see page 559.Correspondence to: Donna Mancini, MD, Division of Cardiology, Department of Medicine, Icahn School of Medicine at Mt Sinai, One Gustave L. Levy Pl, Box 1030, New York, NY 10029. Email donna.mancini@mountsinai.orgReferences1. Stadlbauer D, Amanat F, Chromikova V, Jiang K, Strohmeier S, Arunkumar GA, Tan J, Bhavsar D, Capuano C, Kirkpatrick E, et al. SARS-CoV-2 seroconversion in humans: a detailed protocol for a serological assay, antigen production, and test setup.Curr Protoc Microbiol. 2020; 57:e100. doi: 10.1002/cpmc.100CrossrefMedlineGoogle Scholar2. Villar J, Confalonieri M, Pastores SM, Meduri GU. Rationale for prolonged corticosteroid treatment in the acute respiratory distress syndrome caused by coronavirus disease 2019.Critical Care Explorations. 2020; 2:e0111. doi: 10.1097/CCE.0000000000000111CrossrefMedlineGoogle Scholar3. Paranjpe I, Fuster V, Lala A, Russak AJ, Glicksberg BS, Levin MA, Charney AW, Narula J, Fayad ZA, Bagiella E, et al. Association of treatment dose anticoagulation with in-hospital survival among hospitalized patients with COVID-19.J Am Coll Cardiol. 2020; 76:122–124. doi: 10.1016/j.jacc.2020.05.001CrossrefMedlineGoogle Scholar4. Gebhard C, Regitz-Zagrosek V, Neuhauser HK, Morgan R, Klein SL. Impact of sex and gender on COVID-19 outcomes in Europe.Biol Sex Differ. 2020; 11:29. doi: 10.1186/s13293-020-00304-9CrossrefMedlineGoogle Scholar5. Van Linthout S, Tschöpe C. Inflammation - cause or consequence of heart failure or both?Curr Heart Fail Rep. 2017; 14:251–265. doi: 10.1007/s11897-017-0337-9CrossrefMedlineGoogle Scholar6. Iwasaki A, Yang Y. The potential danger of suboptimal antibody responses in COVID-19.Nat Rev Immunol. 2020; 20:339–341. doi: 10.1038/s41577-020-0321-6CrossrefMedlineGoogle Scholar7. Riphagen S, Gomez X, Gonzalez-Martinez C, Wilkinson N, Theocharis P. Hyperinflammatory shock in children during COVID-19 pandemic.Lancet. 2020; 395:1607–1608. doi: 10.1016/S0140-6736(20)31094-1CrossrefMedlineGoogle Scholar8. Heming N, Sivanandamoorthy S, Meng P, Bounab R, Annane D. Immune effects of corticosteroids in sepsis.Front Immunol. 2018; 9:1736. doi: 10.3389/fimmu.2018.01736CrossrefMedlineGoogle Scholar9. Bonow RO, Fonarow GC, O'Gara PT, Yancy CW. Association of coronavirus disease 2019 (COVID-19) with myocardial injury and mortality.JAMA Cardiol. 2020; 5:751–753. doi: 10.1001/jamacardio.2020.1105CrossrefMedlineGoogle Scholar10. Xiang F, Wang X, He X, Peng Z, Yang B, Zhang J, Zhou Q, Ye H, Ma Y, Li H, et al. Antibody detection and dynamic characteristics in patients with COVID-19.Clin Infect Dis. 2020:ciaa461. doi: 10.1093/cid/ciaa461CrossrefGoogle Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Calcaterra V, Zanelli S, Foppiani A, Verduci E, Benatti B, Bollina R, Bombaci F, Brucato A, Cammarata S, Calabrò E, Cirnigliaro G, Della Torre S, Dell'osso B, Moltrasio C, Marzano A, Nostro C, Romagnuolo M, Trotta L, Savasi V, Smiroldo V and Zuccotti G (2024) Long COVID in Children, Adults, and Vulnerable Populations: for an C, E, L, V, and (2024) Cardiovascular COVID-19 Syndrome Clinical and New on G, M, A, A, F, I, G, M, L, E, and (2024) Cardiac in With Syndrome in Adults, of the Heart M, I, J, L, C, D, N, D, L, F, I, P, A, V, A, M, D, J, S, S, and heart and of the on Cardiovascular A, and Cardiovascular in the of M, M, M, A, J, P, Gomez J, K, A, A, and Association of and in COVID-19 Heart and M, S, R, M, Z, A, M, I and review and on the on risk clinical and of inflammatory syndrome in adults of Medicine & and of and to in Syndrome in Children, R, A, M, M, and SARS-CoV-2 We of Clinical Medicine, A, M, M, and Young With Syndrome of Initial COVID-19 With No COVID-19 M, A, and and of in the A, S, B, N, P, T, K, M, A, and Clinical of COVID-19 in young combined of the Heart Association COVID-19 Cardiovascular and the Outcomes for Cardiac in H, and Wang and treatment and Syndrome Shock in a With A, and Syndrome in with with M, N, S, H, R, A, K, J, E, M, and Immune and dysregulation to in Syndrome in in Z, E, E, M, C, H, K, Y, J, and V The Impact of COVID-19 on the Cardiovascular Health of From a and Heart J, and on Cardiovascular and in Adults, of Clinical Medicine, T, and Syndrome in of Medicine, H, Z, Li N, Zhang Z, B, Peng Y, Zhou and Wang COVID-19 and Cardiovascular From to Clinical and Z, A, E, D, and Syndrome Mild COVID-19 in a of Clinical D, and D, and The heart and N, I, M, and as an of Syndrome in Adults, of Clinical G, D, L, and Syndrome in With of of Clinical I, T, J, A, J, M, M, and COVID-19 Clinical in Cardiology, L, H, X, Xiang M, V, Wang and The of and heart in and in Cardiovascular Medicine, M, R, and cases of inflammatory syndrome in at a in Medicine K, R, A, C, Y, A, A, C, I, K, C, and inflammatory syndrome case The of the J, Z, Z, K, G, A, and COVID-19 and the cardiovascular an The of the G, A, R, P, and Syndrome in an