COVID-19
2020; Lippincott Williams & Wilkins; Volume: 142; Issue: 11 Linguagem: Inglês
10.1161/circulationaha.120.049252
ISSN1524-4539
AutoresDaniel Knight, Tushar Kotecha, Yousuf Razvi, Liza Chacko, James Brown, Paramjit Jeetley, James Goldring, Michael Jacobs, Lucy Lamb, Rupert Negus, Anthony Wolff, James Moon, Hui Xue, Peter Kellman, Niket Patel, Marianna Fontana,
Tópico(s)Long-Term Effects of COVID-19
ResumoHomeCirculationVol. 142, No. 11COVID-19 Free AccessLetterPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessLetterPDF/EPUBCOVID-19Myocardial Injury in Survivors Daniel S. Knight, Tushar Kotecha, Yousuf Razvi, Liza Chacko, James T. Brown, Paramjit S. Jeetley, James Goldring, Michael Jacobs, Lucy E. Lamb, Rupert Negus, Anthony Wolff, James C. Moon, Hui Xue, Peter Kellman, Niket Patel and Marianna Fontana Daniel S. KnightDaniel S. Knight Daniel Knight, MBBS, MD, Department of Cardiology, Royal Free London NHS Foundation Trust, Pond St, London, NW3 2QG, United Kingdom. Email E-mail Address: [email protected] Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). Institute of Cardiovascular Science, University College London, United Kingdom (D.S.K., J.T.B., J.C.M., N.P.). , Tushar KotechaTushar Kotecha https://orcid.org/0000-0003-0059-4817 Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). , Yousuf RazviYousuf Razvi Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). , Liza ChackoLiza Chacko Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). National Amyloidosis Centre, Division of Medicine, University College London, United Kingdom (L.C., M.F.). , James T. BrownJames T. Brown Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). Institute of Cardiovascular Science, University College London, United Kingdom (D.S.K., J.T.B., J.C.M., N.P.). , Paramjit S. JeetleyParamjit S. Jeetley Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). , James GoldringJames Goldring Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). , Michael JacobsMichael Jacobs Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). , Lucy E. LambLucy E. Lamb Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). Academic Department of Defence Medicine, Royal Centre for Defence Medicine, ICT Centre, Edgbaston, Birmingham, United Kingdom (L.E.L.). , Rupert NegusRupert Negus Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). , Anthony WolffAnthony Wolff https://orcid.org/0000-0002-6780-4551 Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). , James C. MoonJames C. Moon Institute of Cardiovascular Science, University College London, United Kingdom (D.S.K., J.T.B., J.C.M., N.P.). Barts Heart Centre, Barts Health NHS Trust, West Smithfield, London, United Kingdom (J.C.M.). , Hui XueHui Xue https://orcid.org/0000-0002-4561-5530 National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD (H.X., P.K.). , Peter KellmanPeter Kellman National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD (H.X., P.K.). , Niket PatelNiket Patel Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). Institute of Cardiovascular Science, University College London, United Kingdom (D.S.K., J.T.B., J.C.M., N.P.). and Marianna FontanaMarianna Fontana Royal Free London NHS Foundation Trust, United Kingdom (D.S.K., T.K., Y.R., L.C., J.T.B., P.S.J., J.G., M.J., L.E.L., R.N., A.W., N.P., M.F.). National Amyloidosis Centre, Division of Medicine, University College London, United Kingdom (L.C., M.F.). Originally published14 Jul 2020https://doi.org/10.1161/CIRCULATIONAHA.120.049252Circulation. 2020;142:1120–1122Other version(s) of this articleYou are viewing the most recent version of this article. Previous versions: July 14, 2020: Ahead of Print Hospitalized patients with coronavirus disease 2019 (COVID-19) frequently have myocardial injury with troponin elevation,1–4 but the underlying causes beyond acute coronary syndromes and pulmonary emboli are ill defined. We used cardiovascular magnetic resonance (CMR) during early convalescence to assess the presence, type, and extent of myocardial injury in troponin-positive patients with COVID-19.All patients with COVID-19 discharged from the Royal Free London NHS Foundation Trust until April 30, 2020 were reviewed (Figure). Diagnosis was either by (1) positive oro/nasopharyngeal throat swab for severe acute respiratory syndrome coronavirus 2 by reverse transcriptase polymerase chain reaction or (2) negative swabs for severe acute respiratory syndrome coronavirus 2 but the triad of viral illness symptoms (≥1 of cough, fever, myalgia), typical blood biomarkers (≥1 of new lymphopenia, high d-dimer, high ferritin, elevated liver transaminases), and probable likelihood of COVID-19 infection on thoracic imaging. A CMR scan (1.5T, Magnetom Aera, Siemens Healthcare) was offered to patients discharged with a COVID-19 diagnosis and myocardial injury as indicated by elevated high-sensitivity troponin T (hsTnT, >14 ng/L). Exclusions were hospitalization with acute coronary syndromes or pulmonary emboli, known cardiac pathology likely to cause scar, age ≥80 years, severe renal impairment, pregnancy, medical unsuitability, and standard CMR contraindications. CMR included cines, native myocardial T1 and T2 mapping, early and late gadolinium enhancement (LGE) with, if no contraindications, adenosine stress perfusion imaging. The CMR diagnosis of myocarditis followed published expert recommendations.5 Ethical approval was obtained (London Hampstead Research Ethics Committee, reference 19/LO/1561), and all patients provided written informed consent.Download figureDownload PowerPointFigure. CONSORT diagram of patient selection for CMR (Left) with examples of CMR study diagnoses (Right). The top case shows an example of CMR images of a patient with myocarditis. The basal short-axis slice with LGE showed a subepicardial scar of the basal inferolateral wall (red arrow), and the corresponding native T1 map demonstrated elevated myocardial T1 in the corresponding area consistent with myocardial scar or edema or both. The middle case shows an example of a potential ischemic etiology for troponin leak. There is anterolateral subendocardial LGE (red arrow) signifying myocardial infarction along with septal inducible myocardial ischemia (asterisk) on quantitative stress perfusion maps performed during adenosine-induced hyperemia. The bottom case shows sample CMR images of a patient with a dual diagnosis of extensive inducible myocardial ischemia along with myocarditis. The LGE showed diffuse patchy subepicardial enhancement of the myocardium predominantly in the basal inferolateral wall (red arrows) with the T2 map showing associated myocardial edema. Quantitative stress perfusion maps showed extensive inducible ischemia predominantly in the left anterior descending and right coronary artery territories. ACS indicates acute coronary syndromes; CMR, cardiovascular magnetic resonance; COVID-19, coronavirus disease 2019; eGFR, estimated glomerular filtration rate; hsTnT, high-sensitivity troponin T; IHD, ischemic heart disease; LGE, late gadolinium enhancement; MRI, magnetic resonance imaging; PE, pulmonary emboli; RT-PCR, reverse transcriptase polymerase chain reaction; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2; –ve, negative; and +ve, positive.The majority (71%) of the 828 reverse transcriptase polymerase chain reaction–positive patients had elevated hsTnT, which was associated with higher inpatient mortality (elevated versus normal hsTnT: 239/586 [41%] died versus 20/242 [8%], respectively, P<0.001). Fifty-one patients were referred for CMR, 22 of whom had ≥1 identifiable causes of troponin elevation (6 with acute coronary syndromes, 12 with pulmonary emboli) or known cardiac pathology (7 had a history of ischemic heart disease) or both. The remaining 29 patients who were included in the final analysis had unexplained myocardial injury and no cause for previous myocardial scarring, 19 of whom (66%) underwent additional adenosine stress perfusion. The intervals between CMR and symptom onset, diagnosis, or discharge were 46±15 days, 37±10 days, and 27±11 days, respectively.Of the 29 patients with elevated hsTnT of unknown cause (average age 64±9 years), most were male (24, 83%) and were reverse transcriptase polymerase chain reaction positive (28, 97%). Median inpatient stay was 9 days (6–16), and 10 (34%) patients required intensive care unit ventilatory support. Admission hsTnT levels were 23.0 ng/L (19.0–32.8). Patients had lymphopenia (lymphocyte count 0.76±0.37×109/L) and elevated C-reactive protein (227.8±126.5 mg/L) during admission. On CMR, 20 (69%) patients had residual lung parenchymal changes. Four (14%) had pleural effusions and 2 (7%) had pericardial effusions. Mean biventricular systolic function for the overall cohort was normal (left ventricular ejection fraction 67.7±11.4%, right ventricular ejection fraction 63.7%±9.5%); 1 patient had mild left ventricular dysfunction, and 1 had severe biventricular dysfunction. With the use of the LGE technique and (where possible) stress perfusion imaging, 20 patients (69%) had an identifiable mechanism of myocardial injury (Figure), classified as nonischemic heart disease–related (11 patients, 38%), ischemic heart disease–related (5, 17%), or dual ischemic and nonischemic pathology (4, 14%).A nonischemic cause of elevated hsTnT was conferred by the presence of noninfarct pattern LGE (not corresponding to a coronary territory and sparing the endocardium). The LGE patterns were myocarditis-like in 13 patients (45%) by international criteria,5 with 2 other patients having nonspecific midwall LGE only. These patients all had normal left ventricular function (left ventricular ejection fraction 70.4±6.9%) with no regional wall motion abnormalities. The median extent of the myocarditis-pattern LGE was 2 (1–2.5) segments with no significant residual myocardial edema in the overall cohort (peak myocardial T2 51.0 ms [49–54] in patients with myocarditis-like LGE versus 51.0 ms [48–53] nonmyocarditis, P=0.68). Peak C-reactive protein (211±103 versus 255±150 mg/L, P=0.35) and hsTnT (25.0 [18.5–37.5] versus 27.0 ng/L [20.3–47.0], P=0.48) were not significantly elevated in comparison with patients without myocarditis. Four of the patients admitted to the intensive care unit had evidence of myocarditis (40% of the intensive care unit subgroup).Nine of the 29 patients were considered to have an ischemic cause of their elevated hsTnT. Of these, 7 had inducible ischemia, 1 had a prior unknown myocardial infarction by LGE, and 1 had both inducible ischemia and a prior infarction by LGE. When present, inducible ischemia was multiterritorial in half of these cases (ischemic burden 7.3±5.8 segments). Four patients had dual ischemic and nonischemic pathology: 2 had myocarditis-pattern LGE and inducible ischemia, and 2 had nonspecific midwall LGE along with either inducible ischemia or a myocardial infarction.In summary, myocardial injury is common in hospitalized patients with COVID-19 and not exclusive to those with acute coronary syndromes or pulmonary emboli. In this single-center, single–time point convalescent study, myocardial injury was associated with cardiac abnormalities detected by CMR where troponin elevation is unexplained even when cardiac function is normal. The main limitation of this study is its cross-sectional design, which prompts caution regarding the causality of myocardial injury and its relationship to previous COVID-19 infection. Nevertheless, CMR frequently revealed occult coronary artery disease, high rates of myocarditis-like LGE, and sometimes dual pathology. The lack of edema in these patients suggests that the myocarditis-like scar may be permanent. Further serial study would clarify this and assess the long-term clinical consequences of these findings.AcknowledgmentsWe thank S. Anderson, lead radiographer, for her invaluable contribution to this work.Sources of FundingDr Knight is directly supported by the National Institute for Health Research (NIHR) University College London Hospitals (UCLH) Biomedical Research Centre. Dr Moon is directly supported by the UCLH and Barts NIHR Biomedical Research Centres and through a British Heart Foundation (BHF) Accelerator Award. Dr Fontana is funded by a BHF Intermediate Fellowship.DisclosuresNone.Footnotes*Drs Knight and Kotecha contributed equally.†Drs Patel and Fontana contributed equally.https://www.ahajournals.org/journal/circThe data, analytic methods, and study materials will be made available to other researchers for purposes of reproducing the results or replicating the procedure on reasonable request to the corresponding author.Daniel Knight, MBBS, MD, Department of Cardiology, Royal Free London NHS Foundation Trust, Pond St, London, NW3 2QG, United Kingdom. Email dan.knight@nhs.netReferences1. Guo T, Fan Y, Chen M, Wu X, Zhang L, He T, Wang H, Wan J, Wang X, Lu Z. Cardiovascular Implications of fatal outcomes of patients with coronavirus disease 2019 (COVID-19).JAMA Cardiol. 2020; 5:1–8. doi: 10.1001/jamacardio.2020.1017CrossrefGoogle Scholar2. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J, Gu X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.Lancet. 2020; 395:497–506. doi: 10.1016/S0140-6736(20)30183-30185CrossrefMedlineGoogle Scholar3. Shi S, Qin M, Shen B, Cai Y, Liu T, Yang F, Gong W, Liu X, Liang J, Zhao Q, et al. Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China.JAMA Cardiol. 2020; 5:802–810. doi: 10.1001/jamacardio.2020.0950CrossrefMedlineGoogle Scholar4. Wei JF, Huang FY, Xiong TY, Liu Q, Chen H, Wang H, Huang H, Luo YC, Zhou X, Liu ZY, et al. Acute myocardial injury is common in patients with COVID-19 and impairs their prognosis.Heart. 2020; 106:1154–1159. doi: 10.1136/heartjnl-2020-317007CrossrefMedlineGoogle Scholar5. Ferreira VM, Schulz-Menger J, Holmvang G, Kramer CM, Carbone I, Sechtem U, Kindermann I, Gutberlet M, Cooper LT, Liu P, et al. Cardiovascular magnetic resonance in nonischemic myocardial inflammation: expert recommendations.J Am Coll Cardiol. 2018; 72:3158–3176. doi: 10.1016/j.jacc.2018.09.072CrossrefMedlineGoogle Scholar eLetters(0)eLetters should relate to an article recently published in the journal and are not a forum for providing unpublished data. Comments are reviewed for appropriate use of tone and language. Comments are not peer-reviewed. Acceptable comments are posted to the journal website only. Comments are not published in an issue and are not indexed in PubMed. Comments should be no longer than 500 words and will only be posted online. References are limited to 10. 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