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Cardiac Function in Pediatric Patients with MIS-C Using Speckle Tracking and Conventional Echocardiography: A Longitudinal, Single-Center Study

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Abstract

Cardiovascular involvement in Multisystem Inflammatory Syndrome in Children (MIS-C), a potential consequence of coronavirus disease-2019 (COVID-19), is common. Conventional transthoracic echocardiography (TTE) provides primary data on the function of the left and right ventricles, while Speckle Tracking Echocardiography (STE) is more sensitive. This study aims to assess longitudinal cardiac function using STE in these patients. This longitudinal study was conducted from late 2021 to early 2022 at Imam Hossein Children’s Hospital, Isfahan. Cardiac function was assessed by STE at the time of diagnosis and again two months later. Demographics, clinical characteristics, ECG interpretations, imaging studies, and serum cardiac marker levels were collected. Thirty-five pediatric patients with a mean age of 5.1 years (range: 4 months to 17 years) were included and prospectively followed. Twenty-nine of them, comprising 14 males (48.3%) and 15 females (51.7%), underwent STE and were compared with 29 healthy age- and sex-matched children. Factors related to adverse events included reduced myocardial function, enlarged left atrium or ventricle, and mitral regurgitation (MR). Patients with comorbidities affecting strain measurements were excluded from the strain analyses. A significant difference was observed between the groups in regional strains in the basal and apical septal and middle lateral regions. Global strain rate (GLS) and strain rates were not significantly different but were still lower than the control group. Twenty percent of patients had abnormal GLS but normal left ventricular ejection fraction (LVEF). All patients exhibited reduced segmental myocardial strain in at least one segment. Four out of 26 recovered patients without comorbidities had abnormal GLS at follow-up, despite normal LVEF. STE proves more useful than conventional echocardiography in patients with MIS-C, revealing subclinical cardiac injury in the acute and post-acute phases.

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References

  1. Ait-Belkacem I, Cartagena García C, Millet-Wallisky E, Izquierdo N, Loosveld M, Arnoux I, Morange P-E, Galland F, Lambert N, Malergue F (2022) SARS-CoV-2 spike protein induces a differential monocyte activation that may contribute to age bias in COVID-19 severity. Sci Rep 12:20824

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hakim MS, Wibawa H, Vujira KA, Puspitarani DA, Supriyati E, Trisnawati I, Iskandar K, Khair RE, Puspadewi Y, Irianingsih SH (2023) Prognostic factors for the outcomes of COVID-19 patients infected with SARS-CoV-2 omicron and delta variants. BMC Med Genom 16:1–9

    Google Scholar 

  3. Ben-Tov A, Lotan R, Gazit S, Chodick G, Perez G, Mizrahi-Reuveni M, Patalon T (2022) Dynamics in COVID-19 symptoms during different waves of the pandemic among children infected with SARS-CoV-2 in the ambulatory setting. Eur J Pediatr 181:3309–3318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bitar RR, Alattas B, Azaz A, Rawat D, Miqdady M (2022) Gastrointestinal manifestations in children with COVID-19 infection: retrospective tertiary center experience. Front Pediatr 10:925520

    Article  PubMed  PubMed Central  Google Scholar 

  5. Saleem H, Rahman J, Aslam N, Murtazaliev S, Khan S (2020) Coronavirus disease 2019 (COVID-19) in children: vulnerable or spared? A systematic review. Cureus 12:e8207

    PubMed  PubMed Central  Google Scholar 

  6. Bigdelian H, Sedighi M, Sabri MR, Dehghan B, Mahdavi C, Ahmadi A, Ghaderian M, Rahimi H, Sadeghizadeh A, Emadoleslami M (2021) Case report: acute intracardiac thrombosis in children with coronavirus disease 2019 (COVID-19). Front Pediatr 9:656720

    Article  PubMed  PubMed Central  Google Scholar 

  7. Shati AA, Mahmood SE, Asseri AA, Alhanshani AA, Alqahtani YA, Ahmad A (2023) SARS-CoV-2 infections and MIS-C among children: a narrative review. Medicine 102:e34475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Varga P, Balajthy A, Biró E, Bíró B, Reiger Z, Szikszay E, Mogyorósy G, Káposzta R, Szabó T (2023) Multicolored MIS-C, a single-centre cohort study. BMC Pediatr 23:1–11

    Article  Google Scholar 

  9. Gawlik AM, Berdej-Szczot E, Chmiel I, Lorek M, Antosz A, Firek-Pędras M, Szydłowski L, Ludwikowska KM, Okarska-Napierała M, Dudek N (2022) A tendency to worse course of multisystem inflammatory syndrome in children with obesity: multiorgan inflammatory syndromes COVID-19 related study. Front Endocrinol 13:934373

    Article  Google Scholar 

  10. Mehrban S, Tahghighi F, Moghadam EA, Ziaee V (2023) Multisystem inflammatory syndrome in children and Kawasaki disease; comparison of their clinical findings and one-year follow-up-a cross-sectional study. Ital J Pediatr 49:90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Minocha PK, Srinivasan R, Babb J, Singh RK, Phoon CK, Better D, Bhatla P (2022) Strain in children with MIS-C and acute COVID-19. Ann Pediatr Cardiol 15:459

    Article  PubMed  Google Scholar 

  12. Abdul Hadi T, Garrison C, Roca T (2023) Atrial fibrillation as a rare complication of multisystem inflammatory syndrome in children (MIS-C): a case report. Cureus 15:e42812

    PubMed  PubMed Central  Google Scholar 

  13. Pamuk U, Gürsu HA, Azak E, Çetin İ (2023) Assessment of myocardial mechanics in acute rheumatic fever using speckle-tracking echocardiography. Anatol J Cardiol 27:592

    Article  PubMed  PubMed Central  Google Scholar 

  14. Mahjoob MP, Parsa SA, Mazarei A, Safi M, Khaheshi I, Esmaeeli S (2017) Rest 2D speckle tracking echocardiography may be a sensitive but nonspecific test for detection of significant coronary artery disease. Acta Bio Medica: Atenei Parmensis 88:457

    Google Scholar 

  15. Dehghan B, Ahmadi A, Sarfarazi Moghadam S, Sabri MR, Ghaderian M, Mahdavi C, Sedighi M, Bigdelian H (2022) Biventricular strain and strain rate impairment shortly after surgical repair of tetralogy of Fallot in children: a case-control study. Health Sci Rep 5:e613

    Article  PubMed  PubMed Central  Google Scholar 

  16. Ghaderian M, Dehghan B, Sabri MR, Ahmadi A, Sadeghi-Lotfabadi A (2020) Evaluation of cardiac function in children after percutaneous closure of atrial septal defect using speckle tracking echocardiography. ARYA Atherosclerosis 16:290

    PubMed  PubMed Central  Google Scholar 

  17. Dehghan B, Sedighi M, Rostampour N, Hashemi E, Hovsepian S, Sabri MR, Ghaderian M, Mahdavi C, Ahmadi A, Esnaashari A (2023) Childhood obesity is associated with subclinical left ventricular dysfunction detected by speckle tracking echocardiography. Clin Pediatr. https://doi.org/10.1177/00099228231201203

    Article  Google Scholar 

  18. Başar EZ, Usta E, Akgün G, Güngör HS, Sönmez HE, Babaoğlu K (2022) Is strain echocardiography a more sensitive indicator of myocardial involvement in patients with multisystem inflammatory syndrome in children (MIS-C) associated with SARS-CoV-2? Cardiol Young 32:1657–1667

    Article  PubMed  Google Scholar 

  19. Sirico D, Basso A, Sabatino J, Reffo E, Cavaliere A, Biffanti R, Cerutti A, Castaldi B, Zulian F, Da Dalt L (2022) Evolution of echocardiographic and cardiac magnetic resonance imaging abnormalities during follow-up in patients with multisystem inflammatory syndrome in children. Eur Heart J-Cardiovasc Imaging 23:1066–1074

    Article  CAS  PubMed  Google Scholar 

  20. Centers for Disease Control and Prevention (2020) Multisystem inflammatory syndrome in children (MIS-C) associated with coronavirus disease 2019 (COVID-19). CDC. https://emergency.cdc.gov/han/2020/han00432.asp. Accessed 8 Sept 2023

  21. Thacker D (2020) Multisystem inflammatory syndrome in children (MIS-C): an emerging immune mediated syndrome in children associated with COVID-19. Dela J Public Health 6:36–39

    Article  PubMed  PubMed Central  Google Scholar 

  22. Matsubara D, Kauffman HL, Wang Y, Calderon-Anyosa R, Nadaraj S, Elias MD, White TJ, Torowicz DL, Yubbu P, Giglia TM (2020) Echocardiographic findings in pediatric multisystem inflammatory syndrome associated with COVID-19 in the United States. J Am Coll Cardiol 76:1947–1961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Balik M, Plasil P, Waldauf P, Pazout J, Fric M, Otahal M, Pachl J (2006) Ultrasound estimation of volume of pleural fluid in mechanically ventilated patients. Intensive Care Med 32:318–321

    Article  CAS  PubMed  Google Scholar 

  24. Mohamed EM (2018) In diagnosis of pleural effusion and pneumothorax in the intensive care unit patients: can chest us replace bedside plain radiography? Egypt J Radiol Nuclear Med 49:346–351

    Article  Google Scholar 

  25. Faqih SA, Noto-Kadou-Kaza B, Abouamrane LM, Mtiou N, El Khayat S, Zamd M, Medkouri G, Benghanem MG, Ramdani B (2016) Pulmonary hypertension: prevalence and risk factors. IJC Heart Vasc 11:87–89

    Article  Google Scholar 

  26. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American society of echocardiography and the European association of cardiovascular imaging. Eur Heart J-Cardiovasc Imaging 16:233–271

    Article  PubMed  Google Scholar 

  27. Levy PT, Machefsky A, Sanchez AA, Patel MD, Rogal S, Fowler S, Yaeger L, Hardi A, Holland MR, Hamvas A, Singh GK (2016) Reference ranges of left ventricular strain measures by two-dimensional speckle-tracking echocardiography in children: a systematic review and meta-analysis. J Am Soc Echocardiogr 29:209-225.e206

    Article  PubMed  Google Scholar 

  28. Levy PT, Sanchez Mejia AA, Machefsky A, Fowler S, Holland MR, Singh GK (2014) Normal ranges of right ventricular systolic and diastolic strain measures in children: a systematic review and meta-analysis. J Am Soc Echocardiogr 27(549–560):e543

    Google Scholar 

  29. Oragui CC (2023) Cardiovascular manifestations of multisystem inflammatory syndrome in children (MIS-C) associated with COVID-19. Cureus. https://doi.org/10.7759/cureus.41950

    Article  PubMed  PubMed Central  Google Scholar 

  30. Sirico D, Basso A, Reffo E, Cavaliere A, Castaldi B, Sabatino J, Meneghel A, Martini G, Da Dalt L, Zulian F (2021) Early echocardiographic and cardiac MRI findings in multisystem inflammatory syndrome in children. J Clin Med 10:3360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. He M, Leone DM, Frye R, Ferdman DJ, Shabanova V, Kosiv KA, Sugeng L, Faherty E, Karnik R (2022) Longitudinal assessment of global and regional left ventricular strain in patients with multisystem inflammatory syndrome in children (MIS-C). Pediatr Cardiol 43:844–854

    Article  PubMed  PubMed Central  Google Scholar 

  32. Yim J, Tsang MYC, Venkataraman A, Balthazaar S, Gin K, Jue J, Nair P, Luong C, Yeung DF, Moss R, Virani SA, McKay J, Williams M, Sayre EC, Abolmaesumi P, Tsang TSM (2023) Cardiac phenotyping of SARS-CoV-2 in British Columbia: a prospective echo study with strain imaging. J Cardiovasc Imaging 31:125–132

    Article  PubMed  PubMed Central  Google Scholar 

  33. Garbin M, Raso I, Piersanti A, Gianolio L, De Silvestri A, Calcaterra V, Corti CG, Nespoli LF, Santacesaria S, Fini G, Dilillo D, Zuccotti G, Mannarino S (2022) Advanced echocardiographic analysis in medium-term follow-up of children with previous multisystem inflammatory syndrome. Children (Basel) 9:917

    PubMed  Google Scholar 

  34. Sabatino J, Di Chiara C, Di Candia A, Sirico D, Donà D, Fumanelli J, Basso A, Pogacnik P, Cuppini E, Romano LR, Castaldi B, Reffo E, Cerutti A, Biffanti R, Cozzani S, Giaquinto C, Di Salvo G (2022) Mid- and long-term atrio-ventricular functional changes in children after recovery from COVID-19. J Clin Med 12:186

    Article  PubMed  PubMed Central  Google Scholar 

  35. Avrusin IS, Abramova NN, Belozerov KE, Kondratiev GV, Bregel LV, Efremova OS, Vilnits AA, Konstantinova JE, Isupova EA, Kornishina TL, Masalova VV, Felker EY, Kalashnikova OV, Chasnyk VG, Aleksandrovich YS, Kostik MM (2023) Determination of risk factors for severe life-threatening course of multisystem inflammatory syndrome associated with COVID-19 in children. Children (Basel) 10:1366

    PubMed  Google Scholar 

  36. Rodriguez-Gonzalez M, Castellano-Martinez A, Cascales-Poyatos HM, Perez-Reviriego AA (2020) Cardiovascular impact of COVID-19 with a focus on children: a systematic review. World J Clin Cases 8:5250–5283

    Article  PubMed  PubMed Central  Google Scholar 

  37. Rogo T, Mathur K, Purswani M (2020) Systemic inflammation with cardiac involvement in pediatric patients with evidence of covid-19 in a community hospital in the Bronx, New York. J Pediatric Infect Dis Soc 9:502–503

    Article  CAS  PubMed  Google Scholar 

  38. Jiang L, Tang K, Levin M, Irfan O, Morris SK, Wilson K, Klein JD, Bhutta ZA (2020) COVID-19 and multisystem inflammatory syndrome in children and adolescents. Lancet Infect Dis 20:e276–e288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Rahmati M, Keshvari M, Mirnasuri S, Yon DK, Lee SW, Il Shin J, Smith L (2022) The global impact of COVID-19 pandemic on the incidence of pediatric new-onset type 1 diabetes and ketoacidosis: a systematic review and meta-analysis. J Med Virol 94:5112–5127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Yang JK, Lin SS, Ji XJ, Guo LM (2010) Binding of SARS coronavirus to its receptor damages islets and causes acute diabetes. Acta Diabetol 47:193–199

    Article  CAS  PubMed  Google Scholar 

  41. Boddu SK, Aurangabadkar G, Kuchay MS (2020) New onset diabetes, type 1 diabetes and COVID-19. Diabetes Metab Syndr 14:2211–2217

    Article  PubMed  PubMed Central  Google Scholar 

  42. Kendall EK, Olaker VR, Kaelber DC, Xu R, Davis PB (2022) Association of SARS-CoV-2 infection with new-onset type 1 diabetes among pediatric patients from 2020 to 2021. JAMA Netw Open 5:e2233014

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank the Vice Chancellor for Research of Isfahan University of Medical Sciences and Cardiovascular Research Institute affiliated to this university for supporting this research. We thank Dr. Rojin Chegini for her assistance in data analysis.

Funding

This article was funded by Isfahan University of Medical Sciences, Grant No. 3400305.

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Authors and Affiliations

  1. Pediatric Cardiovascular Research Center, Cardiovascular Research Institute, Isfahan University of Medical Sciences, Isfahan, Iran

    Mohammad Reza Sabri, Alireza Ahmadi, Mahdieh Saviz, Mehdi Ghaderian, Bahar Dehghan, Chehreh Mahdavi, Davood Ramezani Nezhad, Hamid Rahimi & Zahra Pourmoghaddas

  2. Infectious Diseases and Tropical Medicine Research Center, Isfahan University of Medical Sciences, Isfahan, Iran

    Naseroldin Mostafavi

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  1. Mohammad Reza Sabri
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Correspondence to Mahdieh Saviz.

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Sabri, M.R., Ahmadi, A., Saviz, M. et al. Cardiac Function in Pediatric Patients with MIS-C Using Speckle Tracking and Conventional Echocardiography: A Longitudinal, Single-Center Study. Pediatr Cardiol (2024). https://doi.org/10.1007/s00246-024-03432-w

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