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ST-segment elevation in patients presenting with COVID-19: case series

ST-segment elevation in patients presenting with COVID-19: case series CASE SERIES European Heart Journal - Case Reports doi:10.1093/ehjcr/ytaa553 Coronary heart disease ST-segment elevation in patients presenting with COVID-19: case series 1† 2† 3 Mehrdad Saririan , Richard Armstrong , Jon C. George , 4 2 5† Bartosz Olechowski , Stephen O’Connor , James Brian Byrd , and 6 † Andrew R. Chapman * 1 2 3 Division of Cardiology, Valleywise Health/Creighton University, Phoenix, AZ, USA; Department of Cardiology, St James’s Hospital Dublin, Republic of Ireland; Division of Interventional Cardiology, Einstein Medical Center, Philadelphia, PA, USA; Dorset Heart Centre, Royal Bournemouth & Christchurch Hospitals NHS Foundation Trust 5 6 Bournemouth, UK; Division of Cardiovascular Medicine, University of Michigan Medical School, Ann Arbor, MI, USA; and BHF Centre for Cardiovascular Science, University of Edinburgh, Chancellors Building, Royal Infirmary of Edinburgh, Edinburgh EH16 4SA, UK Received 17 May 2020; first decision 12 June 2020; accepted 9 December 2020 Background The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the pathogen responsible for the now pan- demic disease, coronavirus disease (COVID-19). A number of reports have emerged suggesting these patients may present with signs and symptoms consistent with ST-segment elevation myocardial infarction without coronary ar- tery occlusion. ................................................................................................................................................................................................... Case summary We report an international case series of patients with confirmed COVID-19 infection who presented with sus- pected ST-segment elevation myocardial infarction. Three patients with confirmed COVID-19 presented with elec- trocardiogram criteria for ST-segment elevation myocardial infarction. No patient had obstructive coronary disease at coronary angiography. Post-mortem histology in one case demonstrated myocardial ischaemia in the absence of coronary atherothrombosis or myocarditis. ................................................................................................................................................................................................... Discussion Patients with COVID-19 may present with features consistent with ST-segment elevation myocardial infarction and patent coronary arteries. The prevalence and clinical outcomes of this condition require systematic investigation in consecutive unselected patients. Keywords COVID-19 STEMI Histology Case series Case report � � � � Learning points Patients with coronavirus disease (COVID-19) may present with ST-segment elevation, where urgent coronary angiography should be considered in line with established international guidance. In this series, three patients presenting with ST-segment elevation on the electrocardiogram, which may have been consistent with myocardial infarction, had unobstructed coronary arteries at coronary angiography. Studies of consecutive patients with COVID-19 are necessary to identify the true prevalence of ST-segment elevation and myocardial injury on biomarker testing. * Corresponding author. Tel: þ44-131-242-6515, Fax: þ44-131-242-6379, Email: a.r.chapman@ed.ac.uk These authors contributed equally to this work. Handling Editor: Dejan Milasinovic Peer-reviewers: Luigi Biasco and Ying Xuan Gue Compliance Editor: Carlos Minguito Carazo Supplementary Material Editor: Deepti Ranganathan V The Author(s) 2021. Published by Oxford University Press on behalf of the European Society of Cardiology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestrict- ed reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 2 M. Saririan et al. recently started antibiotics for sinusitis but denied any known contact Introduction with persons infected with SARS-CoV-2. His medical history was The severe acute respiratory syndrome coronavirus 2 (SARS-CoV- notable for hypertension and diet-controlled diabetes. His only medi- 2) is a novel pathogen responsible for the pandemic disease, corona- . cations were lisinopril and aspirin. At presentation, he was febrile at virus disease (COVID-19). This is most often a respiratory illness, 39.3 C and his oxygen saturations were 95%. The remainder of his which can be asymptomatic, cause mild upper respiratory tract symp- physical exam was normal, as were his labs, chest X-ray, and ECG. toms, or result in severe bilateral pneumonia, acute respiratory dis- The patient did not meet the established criteria for SARS-CoV-2 tress syndrome, and death. In hospitalized patients with COVID-19, testing and he was discharged with strict instructions to self- 1,2 myocardial injury is observed in between 23% and 27.8% of cases. quarantine. Here, we describe a series of patients with COVID-19 who pre- . . On Day 11, the patient returned to the hospital with shortness of sented to three international centres with ST-segment elevation, and . . breath. There was no chest pain. He was in respiratory distress discuss their presenting features, clinical findings, and outcomes. . with oxygen saturations of 85% on 15 L/min. He was immediately The usefulness of a paper describing electrocardiogram (ECG) . moved to a negative-pressure isolation room and was intubated. changes suggestive of ST-segment elevation myocardial infarction in . Lymphopenia (1%; normal range 14.6–47.9%) was present. His arter- the context of COVID-19 infection was identified when authors ial blood gas after intubation on 100% FiO demonstrated a pH of noted discussion of such cases on social media. Two authors sug- . 7.28, P0 200 mmHg, PCO 38.4 mmHg, HCO3 18 mmol/L, and 2 2 gested this possibility on Twitter and were contacted by the authors . Lactate of 4.1 mmol/L. Shortly after intubation, he developed supra- who contributed cases. We included cases in which patients had con- ventricular tachycardia at a rate of 198 b.p.m. (Supplementary mater- firmed SARS-CoV-2 infection on viral polymerase chain reaction, and ial online, Figure S1) which was successfully treated with intravenous excluded those who were negative on testing or where coronary (IV) adenosine. The post-conversion ECG showed 2 mm of antero- angiography was not undertaken. Informed consent was obtained lateral ST-elevation without reciprocal depression (Supplementary from patients or their relatives where appropriate. Formal . material online, Figure S2). Initial troponin I was 6283 ng/L (normal Institutional Review Board approval was not required from any par- . . range <40 ng/L). Chest X-ray showed new bilateral airspace opacities ticipating centre. . (Supplementary material online, Figure S3). The on-call interventional Timeline Case presentation cardiologist suspected myopericarditis and deferred immediate angiography. Case 1 The patient became progressively hypotensive and was started on A 61-year-old male presented to the Emergency Department with high-dose norepinephrine and vasopressin with empirical ceftriax- generalized body aches, fever, and worsening cough (Figure 1). He one, azithromycin, and hydroxychloroquine. The patient was given ST-segment elevation in patients presenting with COVID-19 3 Figure 1 Key timepoints during each case illness. Figure 2 Lab activating electrocardiogram, echocardiogram, and coronary angiography findings in Case 1. 4 M. Saririan et al. Figure 3 Histology from left ventricular section taken at post- mortem in Case 1. Video 1 Coronary arteriography cine imaging from Case 1. a loading dose of ticagrelor and IV heparin. The troponin was 7457 ng/L 3 h after the first ECG, and by 12 h had decreased to 5852 ng/L. A transthoracic echocardiogram showed moderate left ventricular systolic dysfunction (Figure 2). The serum troponin con- tinued to fall to 2159 ng/L, and by Day 12, the patient had been weaned from vasopressors. However, his renal function rapidly deteriorated (baseline creatinine 0.89 mg/dL, peak 6.19 mg/dL, nor- mal range 0.84–1.21 mg/dL), such that by Day 13, he was anuric and continuous veno-venous hemofiltration (CVVH) was started. A repeat ECG on Day 15 showed recurrent global ST-elevation pattern (Figure 2). Coronary angiography was undertaken which revealed no luminal stenosis or thrombosis, with preserved TIMI 3 flow in all coronary arteries (Movies 1–3). Left ventriculography revealed mild apical hypokinesis (Supplementary material online, Movie S4). The patient was returned to the intensive care unit (ICU) with a presumptive diagnosis of COVID-19 associated myocarditis, and IV solumedrol and intravenous immunoglobulin (IVIG) were started. His troponin continued to decrease, last measured at 768 ng/L. Video 2 Coronary arteriography cine imaging from Case 1. Despite aggressive supportive measures, the patient became pro- gressively hypotensive and acidotic. His final ECG demonstrated a dramatic shark fin pattern indicative of a diffuse myocardial process (Supplementary material online, Figure S4) and shortly thereafter he went into cardiac arrest (pulseless electrical activity). He was on CVVH with a final potassium recorded at 6.0 mmol/L (normal range 3.5–5 mmol/L). COVID-19 infection was confirmed post-mortem, and an autopsy was performed. Left ventricular sections demon- strated focal eosin uptake indicative of myocardial ischaemia (Figure 3) with no evidence of atherothrombosis or myocarditis. These findings may be in keeping with type 2 myocardial infarction from profound myocardial oxygen supply mismatch in the context of significant refractory hypotension and acidaemia. Case 2 A 59-year-old female with a past medical history of chronic obstruct- ive pulmonary disease and hypertension was brought in by ambu- lance after being found minimally responsive on the ground by neighbours. Her initial observations showed oxygen saturations of 80% on room air with altered mental status. She was intubated on ar- Video 3 Coronary arteriography cine imaging from Case 1. rival to the emergency department. Following intubation, the ECG (Figure 4) revealed ST-segment elevations in V1–V4 and reciprocal ST-segment elevation in patients presenting with COVID-19 5 Figure 4 Lab activating electrocardiogram, computed tomography chest, echocardiogram, and coronary angiography findings in Case 2. ST-depressions in leads II, III, and aVF. Due to concerns about motion abnormality after correction of hypoxaemia, type 2 myocar- COVID-19 and inability to obtain further medical history, computed dial infarction seems a likely aetiology. tomography (CT) of the head, and chest was performed which revealed bilateral lower lung lobe infiltrates and pulmonary oedema . Case 3 with moderate calcification in the mid-left anterior descending artery A 69-year-old female complained of acute onset chest tightness and (Figure 3). Bedside echocardiogram demonstrated reduced left ven- dyspnoea. A 12-lead ECG revealed left bundle branch block which tricular ejection fraction of 40% with antero-apical wall hypokinesis. was known (Supplementary material online, Figure S6). She denied After discussion between the emergency department, cardiology, any recent travel and had no known exposure to SARS-CoV-2. She and ICU teams, a decision was made to perform coronary angiog- . had a previous history of non-ischaemic heart failure with reduced raphy. Moderate diffuse atherosclerotic disease was observed in the . ejection fraction and was on appropriately tailored heart failure ther- left system with no significant luminal obstruction elsewhere (Figure 4 apy including bisoprolol, ramipril, spironolactone, and furosemide. and Supplementary material online, Movies S5 and S6) corresponding Her baseline NYHA class was II, with a dry NT-proBNP of 899 ng/L to the ECG findings. Left ventricular end-diastolic pressure was ele- (normal range <175 ng/L) 4 months previously. An implantable vated at 30 mmHg. cardioverter-defibrillator was placed in 2004, however, given recov- The peak troponin I concentration was elevated at 2390 ng/L. A . . ery in left ventricular function the device was not replaced when it formal echocardiogram on Day 2 of hospitalization revealed normal . . reached end of life in 2018. Other background history was significant left ventricular function with no significant wall motion abnormalities. . for motor neurone disease, diagnosed 4 years previously, and the pa- A repeat ECG demonstrated resolution of the ST-segment elevation . tient required assistance in activities of daily living. and residual T-wave inversion (Supplementary material online, Figure . Initial assessment showed temperature 35.6 C, blood pressure S5). The patient was extubated on Day 3 and tested positive for . 132/85, heart rate 103, oxygen saturations 87% on 4 L via nasal can- COVID-19. The attending clinician suspected myopericarditis. The nula and a respiratory rate of 33. Examination revealed reduced air patient was maintained in isolation for an additional day and as they . entry at both lung bases. Chest X-ray revealed bilateral infiltrates were noted to be back at baseline, they were discharged home with . (Supplementary material online, Figure S7). Blood panel revealed instruction to self-quarantine for a further 14 days. Given the brisk improvement in ECG changes and the resolution of regional wall white cell count of 10.2 and lymphocytes of 4.4. Initial high-sensitivity 6 M. Saririan et al. Figure 5 Lab activating electrocardiogram, echocardiogram, and coronary angiography findings in Case 3. troponin T concentrations were 51 ng/L, rising to 504 ng/L on serial . Discussion testing. NT-proBNP was elevated at 16 857 ng/L. The patient was . This case series describes three patients who developed ST-segment managed as presumed Non ST-segment elevation acute coronary . elevation suspicious for myocardial infarction in the context of syndrome (NSTE-ACS) with decompensated heart failure and load- . COVID-19 infection, who were found to have no angiographic evi- ing dose dual antiplatelets, therapeutic low molecular weight heparin, dence of atherothrombotic type 1 myocardial infarction. In all cases, high-dose IV diuretics, and IV nitrates were administered. On Day 2 type 2 myocardial infarction due to myocardial oxygen supply mis- of admission, a run of rapidly conducted atrial fibrillation was treated . match in the context of critical illness was felt to be the most likely successfully with IV digoxin. . aetiology. In one case, post-mortem examination of myocardial tissue On Day 3 of admission, progressive dyspnoea, chest pain, hypoten- at autopsy demonstrated evidence of ischaemia without thrombosis sion, and oliguria developed and ECG changes were noted with or myocarditis. progressive dynamic concordant ST-elevation in V1–V2 and ST- . Myocardial injury has been described in up to 12% of hospitalized depression in V3–V5 (Figure 5). Bedside transthoracic echocardiog- 3,4 patients with COVID-19, and up to 20% of those requiring inten- raphy revealed impaired left ventricular function which was similar to 4,5 sive care. One study suggested a high prevalence of abnormal find- baseline. The primary percutaneous coronary intervention pathway . ings on cardiac magnetic resonance imaging scans in patients with was activated and the patient emergently transferred. Coronary angi- . 6 . COVID-19 infection. Similarly, a global survey of echocardiography ography was performed via a radial approach, which revealed no ob- findings including 1272 patients with COVID-19 across 69 countries structive atheroma or thrombus (Supplementary material online, found abnormalities in almost half of all patients. However, all find- Movies S7–S9). The presumptive aetiology of her decompensated ings to date are susceptible to selection and reporting bias. heart failure was type 2 myocardial infarction secondary to hypoxia . There are a number of plausible mechanisms for both direct and and hypotension due to critical illness, or myocarditis. On Day 4 of her indirect myocardial injury due to COVID-19. Direct effects may be admission, SARS-CoV-2 swabs returned as positive. Given her history mediated by the SARS-CoV-2 virus harnessing angiotensin- of motor neurone disease and progressive clinical decline, limits of . converting enzyme-2 receptor to gain access into the host cell. . Angiotensin-converting enzyme-2 is expressed within the myocar- treatment were discussed, and comfort measures instituted with help dium and up-regulated in heart disease, and patients with from palliative care colleagues. The patient died on Day 7 of admission. ST-segment elevation in patients presenting with COVID-19 7 cardiovascular disease may therefore be more vulnerable. This may with significant morbidity and mortality, we believe it is important to lead to endothelial cell and microvascular dysfunction or occlusion. consider these observations in the context of the emerging evidence A recent case report from Bergamo, Italy, described evidence of cor- base. Importantly, we identified but did not include four cases of pos- onary microthrombi at post-mortem in a patient with COVID-19 sible STEMI in patients with clinically suspected COVID-19 as viral who presented with ST-segment elevation without obstructive cor- . PCR swabs were negative for SARS-CoV-2. We would note the sen- onary disease. This is consistent with reports of pulmonary micro- . sitivity for this test is reportedly as low as 70%, and where the clinical vascular thrombosis in patients with COVID-19, and diagnostic suspicion for COVID-19 is high, patients should be retested and iso- criteria for disseminated intravascular coagulation have been lated as appropriate. observed in 71.4% of non-survivors with COVID-19. COVID-19 and infection with other coronaviruses may lead to 13–15 myocarditis. A recent report described lone COVID-19 myo- Conclusion carditis in a patient with no respiratory symptoms, and fulminant Patients with COVID-19 may present with ST-segment elevation sug- COVID-19-induced myocarditis has been described and treated with 13 gestive of myocardial infarction in the absence of atherothrombosis. corticosteroids and human immunoglobulin. In addition, transfusion At present, the true prevalence of STEMI in COVID-19 cannot be of convalescent plasma with an SARS-CoV-2–specific antibody (IgG) . determined and guidelines recommend we continue to approach all in addition to corticosteroid therapy has been described, leading to 16 . patients with ST-elevation with a high index of suspicion for coronary improvement in clinical state in a patient with myocardial injury. . artery occlusion, to minimize delay to diagnosis and maximize treat- These treatments have not demonstrated efficacy in clinical trials. . ment benefit. Although histopathological characteristics of COVID-19 are simi- lar to previously described coronaviruses causing SARS and Middle Eastern respiratory syndrome, pathological cardiac manifestations Lead author biography are poorly described. Whilst interstitial mononuclear inflammatory infiltrates have been observed at post-mortem in a patient with myo- Dr Andrew R. Chapman is a cardial injury during their COVID-19 illness in our case, there was Specialist Registrar and Clinical no evidence of myocarditis nor thrombosis. Lecturer in Cardiology at the Royal It is possible the findings observed at autopsy are simply reflective Infirmary of Edinburgh and University of pathophysiological changes in type 2 myocardial infarction, which of Edinburgh, Scotland, UK. may have occurred due to profound refractory hypotension and acidosis, as is commonly observed in critically unwell patients requir- ing circulatory support. Indeed, all presented cases had clear evi- dence of myocardial oxygen supply or demand imbalance without evidence of atherothrombosis, satisfying the diagnostic criteria for type 2 myocardial infarction as per the Fourth Universal Definition of Myocardial Infarction. In order to fully understand the mechanism of ST-elevation in patients with COVID-19, studies of consecutive patients who have undergone coronary angiography are required. In the largest case 21 Supplementary material series of 18 patients, only 50% underwent coronary angiography. Where invasive coronary angiography is indicated, this should be Supplementary material is available at European Heart Journal - Case undertaken with full personal protective equipment. Non-invasive Reports online. imaging may aid diagnosis. The presence of a regional wall motion ab- Slide sets: A fully edited slide set detailing this case and suitable for normality on echocardiography increases the likelihood of an acute local presentation is available online as Supplementary data. atherothrombotic lesion and may lead clinicians to undertake coron- ary angiography. Conversely, the lack of regional changes may pro- Consent: The authors confirm that written consent for submission vide reassurance and lead to alternative non-invasive imaging and publication of this case series including images and associated methods such as CT coronary angiography or cardiac MRI. text has been obtained from the patients in line with COPE guidance. As STEMI is more common in patients with recent respiratory in- Conflict of interest: none declared. fection, we would reiterate recommendations from the European Society of Cardiology Guidance for the Diagnosis and Management Funding: A.R.C. is supported by a Starter Grant for Clinical of Cardiovascular Disease during the COVID-19 pandemic, to Lecturers from the Academy of Medical Sciences [SGL021\1075]. promptly assess patients with ST-segment elevation in line with exist- There are no other funding declarations. ing treatment protocols and consider urgent coronary angiography where acute coronary syndrome is suspected. References There are several limitations to our analysis. This is a selected case 1. Yang X, Yu Y, Xu J, Shu H, Xia J, Liu H et al. Clinical course and outcomes of series, and our findings cannot be generalized to all patients with critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: a single- COVID-19. However, in an evolving pandemic condition associated centered, retrospective, observational study. Lancet Respir Med 2020;8:475–481. 8 M. Saririan et al. 2. Guo T, Fan Y, Chen M, Wu X, Zhang L, He T et al. Cardiovascular implications 13. Hu H, Ma F, Wei X, Fang Y. Coronavirus fulminant myocarditis saved with gluco- of fatal outcomes of patients with coronavirus disease 2019 (COVID-19). JAMA corticoid and human immunoglobulin. Eur Heart J 2020; doi: Cardiol 2020;5:811. . 10.1093/eurheartj/ehaa190. 14. Inciardi RM, Lupi L, Zaccone G, Italia L, Raffo M, Tomasoni D et al. Cardiac in- 3. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y et al. Clinical features of patients volvement in a patient with coronavirus disease 2019 (COVID-19). JAMA Cardiol infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020;395: . 2020;5:819. 497–506. . 15. Alhogbani T. Acute myocarditis associated with novel Middle east respiratory 4. Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J et al. Clinical characteristics of 138 syndrome coronavirus. Ann Saudi Med 2016;36:78–80. hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, 16. Shen C, Wang Z, Zhao F, Yang Y, Li J, Yuan J et al. Treatment of 5 critically ill China. JAMA 2020;323:1061. patients with COVID-19 with convalescent plasma. JAMA 2020;323:1582. 5. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z et al. Clinical course and risk factors for 17. Ding Y, Wang H, Shen H, Li Z, Geng J, Han H et al. The clinical pathology of se- mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective . vere acute respiratory syndrome (SARS): a report from China. J Pathol 2003;200: cohort study. Lancet 2020;395:1054–1062. 282–289. 6. Puntmann VO, Carerj ML, Wieters I, Fahim M, Arendt C, Hoffmann J et al. . 18. Ng DL, Al Hosani F, Keating MK, Gerber SI, Jones TL, Metcalfe MG et al. Outcomes of cardiovascular magnetic resonance imaging in patients recently . Clinicopathologic, immunohistochemical, and ultrastructural findings of a fatal recovered from coronavirus disease 2019 (COVID-19). JAMA Cardiol 2020;5: case of middle east respiratory syndrome coronavirus infection in the United Arab Emirates, April 2014. Am J Pathol 2016;186:652–658. 7. Dweck MA, Bularga A, Hahn RT, Bing R, Lee KK, Chapman AR et al. Global . 19. Xu Z, Shi L, Wang Y, Zhang J, Huang L, Zhang C et al. Pathological findings of evaluation of echocardiography in patients with COVID-19. Eur Heart J - COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Cardiovasc Imag 2020;21:949–958. Med 2020;8:420–422. 8. Chapman AR, Bularga A, Mills NL. High-sensitivity cardiac troponin can be an . . 20. Sandoval Y, Jaffe AS. Type 2 myocardial infarction: JACC review topic of the ally in the fight against COVID-19. Circulation 2020;141:1733–1735. week. J Am Coll Cardiol 2019;73:1846–1860. 9. Chen L, Li X, Chen M, Feng Y, Xiong C. The ACE2 expression in human heart 21. Bangalore S, Sharma A, Slotwiner A, Yatskar L, Harari R, Shah B et al. ST-seg- indicates new potential mechanism of heart injury among patients infected with . ment elevation in patients with covid-19—a case series. N Engl J Med 2020;382: SARS-CoV-2. Cardiovasc Res 2020;116:1097–1100. . 2478–2480. 10. Guagliumi G, Sonzogni A, Pescetelli I, Pellegrini D, Finn AV. Microthrombi and 22. Cosyns B, Lochy S, Luchian ML, Gimelli A, Pontone G, Allard SD et al. The role ST-segment-elevation myocardial infarction in COVID-19. Circulation 2020;142: of cardiovascular imaging for myocardial injury in hospitalized COVID-19 804–809. . patients. Eur Heart J Cardiovasc Imaging 2020;21:709–714. 11. Danzi GB, Loffi M, Galeazzi G, Gherbesi E. Acute pulmonary embolism and 23. Cuervo G, Viasus D, Carratala J. Acute myocardial infarction after laboratory- COVID-19 pneumonia: a random association? Eur Heart J 2020; May 14;41(19): . confirmed influenza infection. N Engl J Med 2018;378:2540. 24. The European Society for Cardiology. ESC Guidance for the Diagnosis and 12. Tang N, Li D, Wang X, Sun Z. Abnormal coagulation parameters are associated . Management of CV Disease during the COVID-19 Pandemic. https://www.escar with poor prognosis in patients with novel coronavirus pneumonia. J Thromb . dio.org/Education/COVID-19-and-Cardiology/ESC-COVID-19-Guidance (10 Haemost 2020;18:844–847. June 2020). http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png European Heart Journal - Case Reports Oxford University Press

ST-segment elevation in patients presenting with COVID-19: case series

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Abstract

CASE SERIES European Heart Journal - Case Reports doi:10.1093/ehjcr/ytaa553 Coronary heart disease ST-segment elevation in patients presenting with COVID-19: case series 1† 2† 3 Mehrdad Saririan , Richard Armstrong , Jon C. George , 4 2 5† Bartosz Olechowski , Stephen O’Connor , James Brian Byrd , and 6 † Andrew R. Chapman * 1 2 3 Division of Cardiology, Valleywise Health/Creighton University, Phoenix, AZ, USA; Department of Cardiology, St James’s Hospital Dublin, Republic of Ireland; Division of Interventional Cardiology, Einstein Medical Center, Philadelphia, PA, USA; Dorset Heart Centre, Royal Bournemouth & Christchurch Hospitals NHS Foundation Trust 5 6 Bournemouth, UK; Division of Cardiovascular Medicine, University of Michigan Medical School, Ann Arbor, MI, USA; and BHF Centre for Cardiovascular Science, University of Edinburgh, Chancellors Building, Royal Infirmary of Edinburgh, Edinburgh EH16 4SA, UK Received 17 May 2020; first decision 12 June 2020; accepted 9 December 2020 Background The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the pathogen responsible for the now pan- demic disease, coronavirus disease (COVID-19). A number of reports have emerged suggesting these patients may present with signs and symptoms consistent with ST-segment elevation myocardial infarction without coronary ar- tery occlusion. ................................................................................................................................................................................................... Case summary We report an international case series of patients with confirmed COVID-19 infection who presented with sus- pected ST-segment elevation myocardial infarction. Three patients with confirmed COVID-19 presented with elec- trocardiogram criteria for ST-segment elevation myocardial infarction. No patient had obstructive coronary disease at coronary angiography. Post-mortem histology in one case demonstrated myocardial ischaemia in the absence of coronary atherothrombosis or myocarditis. ................................................................................................................................................................................................... Discussion Patients with COVID-19 may present with features consistent with ST-segment elevation myocardial infarction and patent coronary arteries. The prevalence and clinical outcomes of this condition require systematic investigation in consecutive unselected patients. Keywords COVID-19 STEMI Histology Case series Case report � � � � Learning points Patients with coronavirus disease (COVID-19) may present with ST-segment elevation, where urgent coronary angiography should be considered in line with established international guidance. In this series, three patients presenting with ST-segment elevation on the electrocardiogram, which may have been consistent with myocardial infarction, had unobstructed coronary arteries at coronary angiography. Studies of consecutive patients with COVID-19 are necessary to identify the true prevalence of ST-segment elevation and myocardial injury on biomarker testing. * Corresponding author. Tel: þ44-131-242-6515, Fax: þ44-131-242-6379, Email: a.r.chapman@ed.ac.uk These authors contributed equally to this work. Handling Editor: Dejan Milasinovic Peer-reviewers: Luigi Biasco and Ying Xuan Gue Compliance Editor: Carlos Minguito Carazo Supplementary Material Editor: Deepti Ranganathan V The Author(s) 2021. Published by Oxford University Press on behalf of the European Society of Cardiology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestrict- ed reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 2 M. Saririan et al. recently started antibiotics for sinusitis but denied any known contact Introduction with persons infected with SARS-CoV-2. His medical history was The severe acute respiratory syndrome coronavirus 2 (SARS-CoV- notable for hypertension and diet-controlled diabetes. His only medi- 2) is a novel pathogen responsible for the pandemic disease, corona- . cations were lisinopril and aspirin. At presentation, he was febrile at virus disease (COVID-19). This is most often a respiratory illness, 39.3 C and his oxygen saturations were 95%. The remainder of his which can be asymptomatic, cause mild upper respiratory tract symp- physical exam was normal, as were his labs, chest X-ray, and ECG. toms, or result in severe bilateral pneumonia, acute respiratory dis- The patient did not meet the established criteria for SARS-CoV-2 tress syndrome, and death. In hospitalized patients with COVID-19, testing and he was discharged with strict instructions to self- 1,2 myocardial injury is observed in between 23% and 27.8% of cases. quarantine. Here, we describe a series of patients with COVID-19 who pre- . . On Day 11, the patient returned to the hospital with shortness of sented to three international centres with ST-segment elevation, and . . breath. There was no chest pain. He was in respiratory distress discuss their presenting features, clinical findings, and outcomes. . with oxygen saturations of 85% on 15 L/min. He was immediately The usefulness of a paper describing electrocardiogram (ECG) . moved to a negative-pressure isolation room and was intubated. changes suggestive of ST-segment elevation myocardial infarction in . Lymphopenia (1%; normal range 14.6–47.9%) was present. His arter- the context of COVID-19 infection was identified when authors ial blood gas after intubation on 100% FiO demonstrated a pH of noted discussion of such cases on social media. Two authors sug- . 7.28, P0 200 mmHg, PCO 38.4 mmHg, HCO3 18 mmol/L, and 2 2 gested this possibility on Twitter and were contacted by the authors . Lactate of 4.1 mmol/L. Shortly after intubation, he developed supra- who contributed cases. We included cases in which patients had con- ventricular tachycardia at a rate of 198 b.p.m. (Supplementary mater- firmed SARS-CoV-2 infection on viral polymerase chain reaction, and ial online, Figure S1) which was successfully treated with intravenous excluded those who were negative on testing or where coronary (IV) adenosine. The post-conversion ECG showed 2 mm of antero- angiography was not undertaken. Informed consent was obtained lateral ST-elevation without reciprocal depression (Supplementary from patients or their relatives where appropriate. Formal . material online, Figure S2). Initial troponin I was 6283 ng/L (normal Institutional Review Board approval was not required from any par- . . range <40 ng/L). Chest X-ray showed new bilateral airspace opacities ticipating centre. . (Supplementary material online, Figure S3). The on-call interventional Timeline Case presentation cardiologist suspected myopericarditis and deferred immediate angiography. Case 1 The patient became progressively hypotensive and was started on A 61-year-old male presented to the Emergency Department with high-dose norepinephrine and vasopressin with empirical ceftriax- generalized body aches, fever, and worsening cough (Figure 1). He one, azithromycin, and hydroxychloroquine. The patient was given ST-segment elevation in patients presenting with COVID-19 3 Figure 1 Key timepoints during each case illness. Figure 2 Lab activating electrocardiogram, echocardiogram, and coronary angiography findings in Case 1. 4 M. Saririan et al. Figure 3 Histology from left ventricular section taken at post- mortem in Case 1. Video 1 Coronary arteriography cine imaging from Case 1. a loading dose of ticagrelor and IV heparin. The troponin was 7457 ng/L 3 h after the first ECG, and by 12 h had decreased to 5852 ng/L. A transthoracic echocardiogram showed moderate left ventricular systolic dysfunction (Figure 2). The serum troponin con- tinued to fall to 2159 ng/L, and by Day 12, the patient had been weaned from vasopressors. However, his renal function rapidly deteriorated (baseline creatinine 0.89 mg/dL, peak 6.19 mg/dL, nor- mal range 0.84–1.21 mg/dL), such that by Day 13, he was anuric and continuous veno-venous hemofiltration (CVVH) was started. A repeat ECG on Day 15 showed recurrent global ST-elevation pattern (Figure 2). Coronary angiography was undertaken which revealed no luminal stenosis or thrombosis, with preserved TIMI 3 flow in all coronary arteries (Movies 1–3). Left ventriculography revealed mild apical hypokinesis (Supplementary material online, Movie S4). The patient was returned to the intensive care unit (ICU) with a presumptive diagnosis of COVID-19 associated myocarditis, and IV solumedrol and intravenous immunoglobulin (IVIG) were started. His troponin continued to decrease, last measured at 768 ng/L. Video 2 Coronary arteriography cine imaging from Case 1. Despite aggressive supportive measures, the patient became pro- gressively hypotensive and acidotic. His final ECG demonstrated a dramatic shark fin pattern indicative of a diffuse myocardial process (Supplementary material online, Figure S4) and shortly thereafter he went into cardiac arrest (pulseless electrical activity). He was on CVVH with a final potassium recorded at 6.0 mmol/L (normal range 3.5–5 mmol/L). COVID-19 infection was confirmed post-mortem, and an autopsy was performed. Left ventricular sections demon- strated focal eosin uptake indicative of myocardial ischaemia (Figure 3) with no evidence of atherothrombosis or myocarditis. These findings may be in keeping with type 2 myocardial infarction from profound myocardial oxygen supply mismatch in the context of significant refractory hypotension and acidaemia. Case 2 A 59-year-old female with a past medical history of chronic obstruct- ive pulmonary disease and hypertension was brought in by ambu- lance after being found minimally responsive on the ground by neighbours. Her initial observations showed oxygen saturations of 80% on room air with altered mental status. She was intubated on ar- Video 3 Coronary arteriography cine imaging from Case 1. rival to the emergency department. Following intubation, the ECG (Figure 4) revealed ST-segment elevations in V1–V4 and reciprocal ST-segment elevation in patients presenting with COVID-19 5 Figure 4 Lab activating electrocardiogram, computed tomography chest, echocardiogram, and coronary angiography findings in Case 2. ST-depressions in leads II, III, and aVF. Due to concerns about motion abnormality after correction of hypoxaemia, type 2 myocar- COVID-19 and inability to obtain further medical history, computed dial infarction seems a likely aetiology. tomography (CT) of the head, and chest was performed which revealed bilateral lower lung lobe infiltrates and pulmonary oedema . Case 3 with moderate calcification in the mid-left anterior descending artery A 69-year-old female complained of acute onset chest tightness and (Figure 3). Bedside echocardiogram demonstrated reduced left ven- dyspnoea. A 12-lead ECG revealed left bundle branch block which tricular ejection fraction of 40% with antero-apical wall hypokinesis. was known (Supplementary material online, Figure S6). She denied After discussion between the emergency department, cardiology, any recent travel and had no known exposure to SARS-CoV-2. She and ICU teams, a decision was made to perform coronary angiog- . had a previous history of non-ischaemic heart failure with reduced raphy. Moderate diffuse atherosclerotic disease was observed in the . ejection fraction and was on appropriately tailored heart failure ther- left system with no significant luminal obstruction elsewhere (Figure 4 apy including bisoprolol, ramipril, spironolactone, and furosemide. and Supplementary material online, Movies S5 and S6) corresponding Her baseline NYHA class was II, with a dry NT-proBNP of 899 ng/L to the ECG findings. Left ventricular end-diastolic pressure was ele- (normal range <175 ng/L) 4 months previously. An implantable vated at 30 mmHg. cardioverter-defibrillator was placed in 2004, however, given recov- The peak troponin I concentration was elevated at 2390 ng/L. A . . ery in left ventricular function the device was not replaced when it formal echocardiogram on Day 2 of hospitalization revealed normal . . reached end of life in 2018. Other background history was significant left ventricular function with no significant wall motion abnormalities. . for motor neurone disease, diagnosed 4 years previously, and the pa- A repeat ECG demonstrated resolution of the ST-segment elevation . tient required assistance in activities of daily living. and residual T-wave inversion (Supplementary material online, Figure . Initial assessment showed temperature 35.6 C, blood pressure S5). The patient was extubated on Day 3 and tested positive for . 132/85, heart rate 103, oxygen saturations 87% on 4 L via nasal can- COVID-19. The attending clinician suspected myopericarditis. The nula and a respiratory rate of 33. Examination revealed reduced air patient was maintained in isolation for an additional day and as they . entry at both lung bases. Chest X-ray revealed bilateral infiltrates were noted to be back at baseline, they were discharged home with . (Supplementary material online, Figure S7). Blood panel revealed instruction to self-quarantine for a further 14 days. Given the brisk improvement in ECG changes and the resolution of regional wall white cell count of 10.2 and lymphocytes of 4.4. Initial high-sensitivity 6 M. Saririan et al. Figure 5 Lab activating electrocardiogram, echocardiogram, and coronary angiography findings in Case 3. troponin T concentrations were 51 ng/L, rising to 504 ng/L on serial . Discussion testing. NT-proBNP was elevated at 16 857 ng/L. The patient was . This case series describes three patients who developed ST-segment managed as presumed Non ST-segment elevation acute coronary . elevation suspicious for myocardial infarction in the context of syndrome (NSTE-ACS) with decompensated heart failure and load- . COVID-19 infection, who were found to have no angiographic evi- ing dose dual antiplatelets, therapeutic low molecular weight heparin, dence of atherothrombotic type 1 myocardial infarction. In all cases, high-dose IV diuretics, and IV nitrates were administered. On Day 2 type 2 myocardial infarction due to myocardial oxygen supply mis- of admission, a run of rapidly conducted atrial fibrillation was treated . match in the context of critical illness was felt to be the most likely successfully with IV digoxin. . aetiology. In one case, post-mortem examination of myocardial tissue On Day 3 of admission, progressive dyspnoea, chest pain, hypoten- at autopsy demonstrated evidence of ischaemia without thrombosis sion, and oliguria developed and ECG changes were noted with or myocarditis. progressive dynamic concordant ST-elevation in V1–V2 and ST- . Myocardial injury has been described in up to 12% of hospitalized depression in V3–V5 (Figure 5). Bedside transthoracic echocardiog- 3,4 patients with COVID-19, and up to 20% of those requiring inten- raphy revealed impaired left ventricular function which was similar to 4,5 sive care. One study suggested a high prevalence of abnormal find- baseline. The primary percutaneous coronary intervention pathway . ings on cardiac magnetic resonance imaging scans in patients with was activated and the patient emergently transferred. Coronary angi- . 6 . COVID-19 infection. Similarly, a global survey of echocardiography ography was performed via a radial approach, which revealed no ob- findings including 1272 patients with COVID-19 across 69 countries structive atheroma or thrombus (Supplementary material online, found abnormalities in almost half of all patients. However, all find- Movies S7–S9). The presumptive aetiology of her decompensated ings to date are susceptible to selection and reporting bias. heart failure was type 2 myocardial infarction secondary to hypoxia . There are a number of plausible mechanisms for both direct and and hypotension due to critical illness, or myocarditis. On Day 4 of her indirect myocardial injury due to COVID-19. Direct effects may be admission, SARS-CoV-2 swabs returned as positive. Given her history mediated by the SARS-CoV-2 virus harnessing angiotensin- of motor neurone disease and progressive clinical decline, limits of . converting enzyme-2 receptor to gain access into the host cell. . Angiotensin-converting enzyme-2 is expressed within the myocar- treatment were discussed, and comfort measures instituted with help dium and up-regulated in heart disease, and patients with from palliative care colleagues. The patient died on Day 7 of admission. ST-segment elevation in patients presenting with COVID-19 7 cardiovascular disease may therefore be more vulnerable. This may with significant morbidity and mortality, we believe it is important to lead to endothelial cell and microvascular dysfunction or occlusion. consider these observations in the context of the emerging evidence A recent case report from Bergamo, Italy, described evidence of cor- base. Importantly, we identified but did not include four cases of pos- onary microthrombi at post-mortem in a patient with COVID-19 sible STEMI in patients with clinically suspected COVID-19 as viral who presented with ST-segment elevation without obstructive cor- . PCR swabs were negative for SARS-CoV-2. We would note the sen- onary disease. This is consistent with reports of pulmonary micro- . sitivity for this test is reportedly as low as 70%, and where the clinical vascular thrombosis in patients with COVID-19, and diagnostic suspicion for COVID-19 is high, patients should be retested and iso- criteria for disseminated intravascular coagulation have been lated as appropriate. observed in 71.4% of non-survivors with COVID-19. COVID-19 and infection with other coronaviruses may lead to 13–15 myocarditis. A recent report described lone COVID-19 myo- Conclusion carditis in a patient with no respiratory symptoms, and fulminant Patients with COVID-19 may present with ST-segment elevation sug- COVID-19-induced myocarditis has been described and treated with 13 gestive of myocardial infarction in the absence of atherothrombosis. corticosteroids and human immunoglobulin. In addition, transfusion At present, the true prevalence of STEMI in COVID-19 cannot be of convalescent plasma with an SARS-CoV-2–specific antibody (IgG) . determined and guidelines recommend we continue to approach all in addition to corticosteroid therapy has been described, leading to 16 . patients with ST-elevation with a high index of suspicion for coronary improvement in clinical state in a patient with myocardial injury. . artery occlusion, to minimize delay to diagnosis and maximize treat- These treatments have not demonstrated efficacy in clinical trials. . ment benefit. Although histopathological characteristics of COVID-19 are simi- lar to previously described coronaviruses causing SARS and Middle Eastern respiratory syndrome, pathological cardiac manifestations Lead author biography are poorly described. Whilst interstitial mononuclear inflammatory infiltrates have been observed at post-mortem in a patient with myo- Dr Andrew R. Chapman is a cardial injury during their COVID-19 illness in our case, there was Specialist Registrar and Clinical no evidence of myocarditis nor thrombosis. Lecturer in Cardiology at the Royal It is possible the findings observed at autopsy are simply reflective Infirmary of Edinburgh and University of pathophysiological changes in type 2 myocardial infarction, which of Edinburgh, Scotland, UK. may have occurred due to profound refractory hypotension and acidosis, as is commonly observed in critically unwell patients requir- ing circulatory support. Indeed, all presented cases had clear evi- dence of myocardial oxygen supply or demand imbalance without evidence of atherothrombosis, satisfying the diagnostic criteria for type 2 myocardial infarction as per the Fourth Universal Definition of Myocardial Infarction. In order to fully understand the mechanism of ST-elevation in patients with COVID-19, studies of consecutive patients who have undergone coronary angiography are required. In the largest case 21 Supplementary material series of 18 patients, only 50% underwent coronary angiography. Where invasive coronary angiography is indicated, this should be Supplementary material is available at European Heart Journal - Case undertaken with full personal protective equipment. Non-invasive Reports online. imaging may aid diagnosis. The presence of a regional wall motion ab- Slide sets: A fully edited slide set detailing this case and suitable for normality on echocardiography increases the likelihood of an acute local presentation is available online as Supplementary data. atherothrombotic lesion and may lead clinicians to undertake coron- ary angiography. Conversely, the lack of regional changes may pro- Consent: The authors confirm that written consent for submission vide reassurance and lead to alternative non-invasive imaging and publication of this case series including images and associated methods such as CT coronary angiography or cardiac MRI. text has been obtained from the patients in line with COPE guidance. As STEMI is more common in patients with recent respiratory in- Conflict of interest: none declared. fection, we would reiterate recommendations from the European Society of Cardiology Guidance for the Diagnosis and Management Funding: A.R.C. is supported by a Starter Grant for Clinical of Cardiovascular Disease during the COVID-19 pandemic, to Lecturers from the Academy of Medical Sciences [SGL021\1075]. promptly assess patients with ST-segment elevation in line with exist- There are no other funding declarations. ing treatment protocols and consider urgent coronary angiography where acute coronary syndrome is suspected. 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Journal

European Heart Journal - Case Reports – Oxford University Press

Published: Feb 8, 2021

Keywords: COVID-19; STEMI; Histology; Case series; Case report

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