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Cardiac echocardiogram findings of severe acute respiratory syndrome coronavirus-2-associated multi-system inflammatory syndrome in children

Part of: Echocardiography

Published online by Cambridge University Press:  05 August 2021

Ashraf S. Harahsheh Open the ORCID record for Ashraf S. Harahsheh [Opens in a new window] ,
Anita Krishnan Open the ORCID record for Anita Krishnan [Opens in a new window] ,
Roberta L. DeBiasi ,
Laura J. Olivieri ,
Christopher Spurney ,
Mary T. Donofrio ,
Russell R. Cross ,
Matthew P. Sharron ,
Lowell H. Frank  and
Charles I. Berul
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Ashraf S. Harahsheh*
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA
Anita Krishnan
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA
Roberta L. DeBiasi
Affiliation:
Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA Microbiology, Immunology and Tropical Medicine, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA Division of Infectious Diseases, Children’s National Hospital, Washington, DC, USA
Laura J. Olivieri
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA
Christopher Spurney
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA
Mary T. Donofrio
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA
Russell R. Cross
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA
Matthew P. Sharron
Affiliation:
Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA Division of Critical Care Medicine, Children’s National Hospital, Washington, DC, USA
Lowell H. Frank
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA
Charles I. Berul
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA
Adam Christopher
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA
Niti Dham
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA
Hemalatha Srinivasalu
Affiliation:
Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA Division of Rheumatology, Children’s National Hospital, Washington, DC, USA
Tova Ronis
Affiliation:
Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA Division of Rheumatology, Children’s National Hospital, Washington, DC, USA
Karen L. Smith
Affiliation:
Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA Division of Hospitalist Medicine, Children’s National Hospital, Washington, DC, USA
Jaclyn N. Kline
Affiliation:
Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA Division of Emergency Medicine, Children’s National Hospital, Washington, DC, USA
Kavita Parikh
Affiliation:
Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA Division of Hospitalist Medicine, Children’s National Hospital, Washington, DC, USA
David Wessel
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA
James E. Bost
Affiliation:
Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA Division of Biostatistics and Study Methodology, Children’s National Hospital, Washington, DC, USA
Sarah Litt
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA
Ashley Austin
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA
Jing Zhang
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA
Craig A. Sable
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC, USA Department of Pediatrics, George Washington University, School of Medicine & Health Sciences, Washington, DC, USA
*
Author for correspondence: Dr A. S. Harahsheh, MD, Department of Pediatrics, George Washington University School of Medicine & Health Sciences; Division of Cardiology, Children’s National Hospital, 111 Michigan Ave, NW, Washington, DC 20010, USA. Tel: +202 476 2020; Fax: +202 476 5700. E-mail: aharahsh@childrensnational.org
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Abstract

Background:

A novel paediatric disease, multi-system inflammatory syndrome in children, has emerged during the 2019 coronavirus disease pandemic.

Objectives:

To describe the short-term evolution of cardiac complications and associated risk factors in patients with multi-system inflammatory syndrome in children.

Methods:

Retrospective single-centre study of confirmed multi-system inflammatory syndrome in children treated from 29 March, 2020 to 1 September, 2020. Cardiac complications during the acute phase were defined as decreased systolic function, coronary artery abnormalities, pericardial effusion, or mitral and/or tricuspid valve regurgitation. Patients with or without cardiac complications were compared with chi-square, Fisher’s exact, and Wilcoxon rank sum.

Results:

Thirty-nine children with median (interquartile range) age 7.8 (3.6–12.7) years were included. Nineteen (49%) patients developed cardiac complications including systolic dysfunction (33%), valvular regurgitation (31%), coronary artery abnormalities (18%), and pericardial effusion (5%). At the time of the most recent follow-up, at a median (interquartile range) of 49 (26–61) days, cardiac complications resolved in 16/19 (84%) patients. Two patients had persistent mild systolic dysfunction and one patient had persistent coronary artery abnormality. Children with cardiac complications were more likely to have higher N-terminal B-type natriuretic peptide (p = 0.01), higher white blood cell count (p = 0.01), higher neutrophil count (p = 0.02), severe lymphopenia (p = 0.05), use of milrinone (p = 0.03), and intensive care requirement (p = 0.04).

Conclusion:

Patients with multi-system inflammatory syndrome in children had a high rate of cardiac complications in the acute phase, with associated inflammatory markers. Although cardiac complications resolved in 84% of patients, further long-term studies are needed to assess if the cardiac abnormalities (transient or persistent) are associated with major cardiac events.

Keywords

Paediatric multisystem inflammatory syndrome temporally associated with 2019 coronavirus diseasemulti-system inflammatory syndrome in children2019 coronavirus disease pandemicpaediatric cardiologymyocarditiscoronary artery

Information

Type
Original Article
Information
Cardiology in the Young , Volume 32 , Issue 5 , May 2022 , pp. 718 - 726
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Copyright
© The Author(s), 2021. Published by Cambridge University Press

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Footnotes

†

The online version of this article has been updated since original publication. A notice detailing the changes has also been published.

References

Harahsheh, AS, Selekman, RE, Simpson, JN, et al. Children’s hospital ambulatory response to the 2019 novel coronavirus disease (COVID-19) pandemic. J Ambul Care Manag 2021; 44: 184–196.CrossRefGoogle Scholar
Harahsheh, AS, Dahdah, N, Newburger, JW, et al. Missed or delayed diagnosis of Kawasaki disease during the 2019 novel coronavirus disease (COVID-19) pandemic. J Pediatr 2020; 222: 261–262.CrossRefGoogle ScholarPubMed
Loke, YH, Berul, CI, Harahsheh, AS. Multisystem inflammatory syndrome in children: is there a linkage to Kawasaki disease? Trends Cardiovasc Med 2020; 30: 389–396.CrossRefGoogle Scholar
Clark, BC, Sanchez-de-Toledo, J, Bautista-Rodriguez, C, et al. Cardiac abnormalities seen in pediatric patients during the SARS-CoV2 pandemic: an international experience. J Am Heart Assoc 2020; 9: e018007.CrossRefGoogle Scholar
Abdel-Haq, N, Asmar, BI, Deza Leon, MP, et al. SARS-CoV-2-associated multisystem inflammatory syndrome in children: clinical manifestations and the role of infliximab treatment. Eur J Pediatr 2021; 180: 1581–1591.CrossRefGoogle ScholarPubMed
Elias, MD, McCrindle, BW, Larios, G, et al. Management of multisystem inflammatory syndrome in children associated with COVID-19: a survey from the international Kawasaki disease registry. CJC Open 2020; 2: 632–640.CrossRefGoogle ScholarPubMed
Sperotto, F, Friedman, KG, Son, MBF, VanderPluym, CJ, Newburger, JW, Dionne, A. Cardiac manifestations in SARS-CoV-2-associated multisystem inflammatory syndrome in children: a comprehensive review and proposed clinical approach. Eur J Pediatr 2021; 180: 307–322.CrossRefGoogle ScholarPubMed
Alsaied, T, Tremoulet, AH, Burns, JC, et al. Review of cardiac involvement in multisystem inflammatory syndrome in children. Circulation 2021; 143: 78–88.CrossRefGoogle ScholarPubMed
Harahsheh, AS, Dahdah, N, Newburger, JW, et al. Reply. J Pediatr 2020; 224: 184.e1–185.e1.CrossRefGoogle ScholarPubMed
Royal College of Paediatric and Child Health. Paediatric multisystem inflammatory syndrome temporally associated with COVID-19. 2020. Retrieved May 10, 2020, from https://www.rcpch.ac.uk/sites/default/files/2020-05/COVID-19-Paediatricmultisystem-%20inflammatory%20syndrome-20200501.pd Google Scholar
Jonat, B, Gorelik, M, Boneparth, A, et al. Multisystem inflammatory syndrome in children associated with coronavirus disease 2019 in a children’s hospital in New York City: patient characteristics and an institutional protocol for evaluation, management, and follow-up. Pediatr Crit Care Med 2021; 22: e178–e191.CrossRefGoogle Scholar
Whittaker, E, Bamford, A, Kenny, J, et al. Clinical characteristics of 58 children with a pediatric inflammatory multisystem syndrome temporally associated with SARS-CoV-2. JAMA 2020; 324: 259–269.CrossRefGoogle ScholarPubMed
Bautista-Rodriguez, C, Sanchez-de-Toledo, J, Clark, BC, et al. Multisystem inflammatory syndrome in children: an international survey. Pediatrics 2021; 147: e2020024554.CrossRefGoogle Scholar
Valverde, I, Singh, Y, Sanchez-de-Toledo, J, et al. Acute cardiovascular manifestations in 286 children with multisystem inflammatory syndrome associated with COVID-19 infection in Europe. Circulation 2021; 143: 21–32.CrossRefGoogle ScholarPubMed
Kaushik, S, Aydin, SI, Derespina, KR, et al. Multisystem inflammatory syndrome in children associated with severe acute respiratory syndrome coronavirus 2 infection (MIS-C): a multi-institutional study from New York City. J Pediatr 2020; 224: 24–29.CrossRefGoogle ScholarPubMed
Dufort, EM, Koumans, EH, Chow, EJ, et al. Multisystem inflammatory syndrome in children in New York State. N Engl J Med 2020; 383: 347–358.CrossRefGoogle ScholarPubMed
Godfred-Cato, S, Bryant, B, Leung, J, et al. COVID-19-associated multisystem inflammatory syndrome in children – United States, March–July 2020. MMWR Morb Mortal Wkly Rep 2020; 69: 1074–1080.CrossRefGoogle ScholarPubMed
DeBiasi, RL, Song, X, Delaney, M, et al. Severe coronavirus disease-2019 in children and young adults in the Washington, DC, metropolitan region. J Pediatr 2020; 223: 199.e1–203.e1.CrossRefGoogle Scholar
Multisystem Inflammatory Syndrome in Children (MIS-C). Associated with Coronavirus Disease 2019 (COVID-19). 2020. Retrieved May 15, 2020, from https://emergency.cdc.gov/han/2020/han00432.asp.Google Scholar
Li, Y, Yu, Y, Chen, S, Liao, Y, Du, J. Corticosteroids and intravenous immunoglobulin in pediatric myocarditis: a meta-analysis. Front Pediatr 2019; 7: 342.CrossRefGoogle ScholarPubMed
Caldeira, D, Lopes, LR, Vaz-Carneiro, A, Costa, J. Cochrane corner: corticosteroids for viral myocarditis. Rev Port Cardiol 2015; 34: 65–67.CrossRefGoogle ScholarPubMed
World Health Organization. Clinical Management of COVID-19: Interim Guidance, 2020. Retrieved June 15, 2021, from https://apps.who.int/iris/bitstream/handle/10665/332196/WHO-2019-nCoV-clinical-2020.5-eng.pdf.Google Scholar
van Paassen, J, Vos, JS, Hoekstra, EM, Neumann, KMI, Boot, PC, Arbous, SM. Corticosteroid use in COVID-19 patients: a systematic review and meta-analysis on clinical outcomes. Crit Care 2020; 24: 696.CrossRefGoogle ScholarPubMed
DeBiasi, R, Harahsheh, A, Srinivasalu, H, et al. Multisystem inflammatory syndrome of children: sub-phenotypes, risk factors, biomarkers, cytokine profiling and viral sequencing. J Pediatr 2021; 25: S0022-3476(21)00518-7. doi: 10.1016/j.jpeds.2021.06.002.CrossRefGoogle Scholar
Maniscalco, V, Abu-Rumeileh, S, Mastrolia, MV, et al. The off-label use of anakinra in pediatric systemic autoinflammatory diseases. Ther Adv Musculoskelet Dis 2020; 12: 1759720X20959575. doi: 10.1177/1759720X20959575.CrossRefGoogle ScholarPubMed
Kantor, PF, Lougheed, J, Dancea, A, et al. Presentation, diagnosis, and medical management of heart failure in children: Canadian cardiovascular society guidelines. Can J Cardiol 2013; 29: 1535–1552.CrossRefGoogle ScholarPubMed
Margossian, R, Schwartz, ML, Prakash, A, et al. Comparison of echocardiographic and cardiac magnetic resonance imaging measurements of functional single ventricular volumes, mass, and ejection fraction (from the Pediatric Heart Network Fontan Cross-Sectional Study). Am J Cardiol 2009; 104: 419–428.CrossRefGoogle Scholar
McCrindle, BW, Rowley, AH, Newburger, JW, et al. Diagnosis, treatment, and long-term management of Kawasaki disease: a scientific statement for health professionals from the American Heart Association. Circulation 2017; 135: e927–e999.CrossRefGoogle ScholarPubMed
Olivieri, L, Arling, B, Friberg, M, Sable, C. Coronary artery z score regression equations and calculators derived from a large heterogeneous population of children undergoing echocardiography. J Am Soc Echocardiogr 2009; 22: 159–164.CrossRefGoogle Scholar
Teitel, DF, Newburger, JW, Sutton, N, et al. Development and utility of quality metrics for ambulatory pediatric cardiology in Kawasaki disease. Clin Pediatr 2020; 59: 245–251.CrossRefGoogle ScholarPubMed
Lopez, L, Colan, SD, Frommelt, PC, et al. Recommendations for quantification methods during the performance of a pediatric echocardiogram: a report from the pediatric measurements writing group of the American Society of Echocardiography Pediatric and Congenital Heart Disease Council. J Am Soc Echocardiogr 2010; 23: 465–495.CrossRefGoogle ScholarPubMed
Zoghbi, WA, Adams, D, Bonow, RO, et al. Recommendations for noninvasive evaluation of native valvular regurgitation: a report from the American Society of Echocardiography developed in collaboration with the society for cardiovascular magnetic resonance. J Am Soc Echocardiogr 2017; 30: 303–371.CrossRefGoogle ScholarPubMed
Belhadjer, Z, Meot, M, Bajolle, F, et al. Acute heart failure in multisystem inflammatory syndrome in children in the context of global SARS-CoV-2 pandemic. Circulation 2020; 142: 429–436.CrossRefGoogle ScholarPubMed
Matsubara, D, Kauffman, HL, Wang, Y, et al. Echocardiographic findings in pediatric multisystem inflammatory syndrome associated with COVID-19 in the United States. J Am Coll Cardiol 2020; 76: 1947–1961.CrossRefGoogle ScholarPubMed
Feldstein, LR, Tenforde, MW, Friedman, KG, et al. Characteristics and outcomes of us children and adolescents with multisystem inflammatory syndrome in children (MIS-C) compared with severe acute COVID-19. JAMA 2021; 325: 1074–1087.CrossRefGoogle ScholarPubMed
Shulman, ST. Pediatric coronavirus disease-2019-associated multisystem inflammatory syndrome. J Pediatric Infect Dis Soc 2020; 9: 285–286.CrossRefGoogle ScholarPubMed
Lamrani, L, Manlhiot, C, Elias, MD, et al. Kawasaki disease shock syndrome versus classical Kawasaki disease, a meta-analysis and comparison with SARS-CoV-2 multisystem inflammatory syndrome. Can J Cardiol 2021: S0828-282X(21)00290-7. doi: 10.1016/j.cjca.2021.05.014.CrossRefGoogle Scholar
Nakamura, Y, Yashiro, M, Uehara, R, et al. Epidemiologic features of Kawasaki disease in Japan: results of the 2007–2008 nationwide survey. J Epidemiol 2010; 20: 302–307.CrossRefGoogle ScholarPubMed
Holman, RC, Belay, ED, Christensen, KY, Folkema, AM, Steiner, CA, Schonberger, LB. Hospitalizations for Kawasaki syndrome among children in the United States, 1997–2007. Pediatr Infect Dis J 2010; 29: 483–488.CrossRefGoogle ScholarPubMed
Sugimoto, M, Manabe, H, Nakau, K, et al. The role of N-terminal pro-B-type natriuretic peptide in the diagnosis of congestive heart failure in children. Correlation with the heart failure score and comparison with B-type natriuretic peptide. Circ J 2010; 74: 998–1005.CrossRefGoogle Scholar
Cuinet, J, Garbagnati, A, Rusca, M, et al. Cardiogenic shock elicits acute inflammation, delayed eosinophilia, and depletion of immune cells in most severe cases. Sci Rep 2020; 10: 7639.CrossRefGoogle ScholarPubMed
Roeleveld, PP, de Klerk, JCA. The perspective of the intensivist on inotropes and postoperative care following pediatric heart surgery: an international survey and systematic review of the literature. World J Pediatr Congenit Heart Surg 2018; 9: 10–21.CrossRefGoogle ScholarPubMed
Hoffman, TM, Wernovsky, G, Atz, AM, et al. Efficacy and safety of milrinone in preventing low cardiac output syndrome in infants and children after corrective surgery for congenital heart disease. Circulation 2003; 107: 996–1002.CrossRefGoogle ScholarPubMed