Electrocardiogram in COVID-19 children

There are described various variants of the clinical manifestations of coronavirus infection, reflecting the severity of the course of the disease from mild forms to severe acute respiratory syndrome, the development of a multisystem hyperinflammatory syndrome with a high probability of death. There is an understanding that, along with a viral infection, COVID-19 is a cardiorespiratory disease. With the defeat of the respiratory system, violations of the functioning of the cardiovascular system are often recorded. Heart lesions detected in 17–75% of cases are associated with myocardial damage by the SARS-CoV-2 virus.  An informative and accessible method of examination for COVID-19 in children is electrocardiography (ECG), used in combination with telemedicine technologies. Long-lasting changes in the structure and function of the heart during convalescence require an individual approach to rehabilitation. The review presents the analysis and interpretation of data on ECG changes in COVID-19 children, discusses the patterns of electrophysiological disorders in COVID-19 children and adults.

Conclusion. Effective methods for diagnosing heart lesions in children have not been defined, and the ECG and echocardiography used do not have specific markers for diagnosing cardiac pathology in COVID-19. Therefore, it is necessary to use the available knowledge to optimize the algorithms for the rehabilitation of children in the period of convalescence.

Contribution:
Kozhevnikova O.V. — concept and design of the study;
Blazhievskaya T.O., Rakhimova A.N., Akhmedova E.E., Abashidze E.A. — collection and processing of the material;
Kozhevnikova O.V., Blazhievskaya T.O. — writing the text;
Kozhevnikova O.V. — editing the text.
All co-authors — approval of the final version of the article, responsibility for the integrity of all parts of the article.

Acknowledgment. The study had no sponsorship.

Conflict of interest. The authors declare no conflict of interest.

Received: June 05, 2023
Accepted: June 20, 2023
Published: August 31, 2023

1. Malkova A., Kudlay D., Kudryavtsev I., Starshinova A., Yablonskiy P., Shoenfeld Y. Immunogenetic Predictors of Severe COVID-19. Vaccines (Basel). 2021; 9(3): 211. https://doi.org/10.3390/vaccines9030211

2. Ludvigsson J.F. Systematic review of COVID-19 in children shows milder cases and a better prognosis than adults. Acta Paediatr. 2020; 109(6): 1088–95. https://doi.org/10.1111/apa.15270

3. Vasichkina E., Alekseeva D., Karev V., Podyacheva E., Kudryavtsev I., Glushkova A., et al. Cardiac involvement in children affected by COVID-19: Clinical features and diagnosis. Diagnostics (Basel). 2022; 13(1): 120. https://doi.org/10.3390/diagnostics13010120

4. Kurosaki S., Otani A., Senoo S., Hataya H., Horikoshi Yu. A child with the Omicron variant coronavirus disease 2019 pneumonia complicated with arrhythmia. Pediatr. Int. 2022; 64(1): e15299. https://doi.org/10.1111/ped.15299

5. Rav-Acha M., Orlev A., Itzhaki I., Zimmerman S.F., Fteiha B., Bohm D., et al. Cardiac arrhythmias amongst hospitalised Coronavirus 2019 (COVID-19) patients: Prevalence, characterisation, and clinical algorithm to classify arrhythmic risk. Int. J. Clin. Pract. 2021; 75(4): e13788. https://doi.org/10.1111/ijcp.13788

6. Kochi A.N., Tagliari A.P., Forleo G.B., Fassini G.M., Tondo C. Cardiac and arrhythmic complications in patients with COVID-19. J. Cardiovasc. Electrophysiol. 2020; 31(5): 1003–8. https://doi.org/10.1111/jce.14479

7. Pellegrino R., Chiappini E., Licari A., Galli L., Marseglia G.L. Prevalence and clinical presentation of long COVID in children: a systematic review. Eur. J. Pediatr. 2022; 181(12): 3995–4009. https://doi.org/10.1007/s00431-022-04600-x

8. Pasternack D., Singh R.K., Minocha P.K., Farkas J.S., Ramaswamy P., Better D., et al. Characteristics of cardiac abnormalities in pediatric patients with acute COVID-19. Cureus. 2023; 15(3): e36093. https://doi.org/10.7759/cureus.36093

9. Feldstein L.R., Rose E.B., Horwitz S.M., Collins J.P., Newhams M.M., Son M.B.F., et al. Multisystem inflammatory syndrome in U.S. children and adolescents. N. Engl. J. Med. 2020; 383(4): 334–46. https://doi.org/10.1056/NEJMoa2021680

10. Valverde I., Singh Y., Sanchez-de-Toledo J., Theocharis P., Chikermane A., Di Filippo S., et al. Acute cardiovascular manifestations in 286 children with multisystem inflammatory syndrome associated with COVID-19 infection in Europe. Circulation. 2021; 143(1): 21–32. https://doi.org/10.1161/circulationaha.120.050065

11. Shehab N., English R.F. Describing our experience with the effects of multisystem inflammatory syndrome in children with COVID-19 on the cardiovascular system. Cardiol. Young. 2023; 1–3. https://doi.org/10.1017/S1047951123000173

12. Kamel S., Raynor A., Zozor S., Lacape G., Brunel V., Nivet-Antoine V., et al. Myocardial injury in coronavirus disease 19 (Covid-19): main pathophysiological mechanisms and clinical utility of cardiac biomarkers. Ann. Biol. Clin. (Paris). 2021; 79(3): 219–31. https://doi.org/10.1684/abc.2021.1642

13. Sandoval Y., Januzzi J.L. Jr., Jaffe A.S. Cardiac troponin for assessment of myocardial injury in COVID-19: JACC review topic of the week. J. Am. Coll. Cardiol. 2020; 76(10): 1244–58. https://doi.org/10.1016/j.jacc.2020.06.068

14. Gartenberg A.J., White T.J., Dang K., Shah M., Paridon S.M., Elias M.D. Assessing the utility of screening electrocardiograms in paediatric patients following COVID-19. Cardiol. Young. 2022; 32(5): 711–7. https://doi.org/10.1017/S1047951121003012

15. Long B., Brady W.J., Bridwell R.E., Ramzy M., Montrief T., Singh M., et al. Electrocardiographic manifestations of COVID-19. Am. J. Emerg. Med. 2021; 41: 96–103. https://doi.org/10.1016/j.ajem.2020.12.060

16. Avcu G., Arslan A., Bal Z.S., Ay O., Levent E., Ozkinay F., et al. Electrocardiographic changes in hospitalised children with COVID-19. Cardiol. Young. 2023; 33(4): 525–31. https://doi.org/10.1017/S1047951123000100

17. Shmueli H., Shah M., Ebinger J.E., Nguyen L.C., Chernomordik F., Flint N., et al. Left ventricular global longitudinal strain in identifying subclinical myocardial dysfunction among patients hospitalized with COVID-19. Int. J. Cardiol. Heart Vasc. 2021; 32: 100719. https://doi.org/10.1016/j.ijcha.2021.100719

18. Wiersinga W.J., Rhodes A., Cheng A.C., Peacock S.J., Prescott H.C. Pathophysiology, transmission, diagnosis, and treatment of coronavirus disease 2019 (COVID-19): A review. JAMA. 2020; 324(8): 782–93. https://doi.org/10.1001/jama.2020.12839

19. Salabei J.K., Asnake Z.T., Ismail Z.H., Charles K., Stanger G.T., Abdullahi A.H., et al. COVID-19 and the cardiovascular system: an update. Am. J. Med. Sci. 2022; 364(2): 139–47. https://doi.org/10.1016/j.amjms.2022.01.022

20. Gordon J.S., Drazner M.H. Biomarkers of cardiac stress and cytokine release syndrome in COVID-19: A review. Curr. Heart Fail Rep. 2021; 18(3): 163–8. https://doi.org/10.1007/s11897-021-00505-2

21. Centurión O.A., Scavenius K.E., García L.B., Torales J.M., Miño L.M. Potential mechanisms of cardiac injury and common pathways of inflammation in patients with COVID-19. Crit. Pathw. Cardiol. 2021; 20(1): 44–52. https://doi.org/10.1097/HPC.0000000000000227

22. Patel T., Kelleman M., West Z., Peter A., Dove M., Butto A., et al. Comparison of multisystem inflammatory syndrome in children-related myocarditis, classic viral myocarditis, and COVID-19 vaccine-related myocarditis in children. J. Am. Heart Assoc. 2022; 11(9): e024393. https://doi.org/10.1161/JAHA.121.024393

23. Ryabykina G.V. ECG changes in COVID-19. Kardiologiya. 2020; 60(8): 16–22. https://doi.org/10.18087/cardio.2020.8.n1192 https://elibrary.ru/hcbqhh (in Russian)

24. Thakkar S., Arora S., Kumar A., Jaswaney R., Faisaluddin M., Ammad Ud Din M., et al. A systematic review of the cardiovascular manifestations and outcomes in the setting of Coronavirus-19 disease. Clin. Med. Insights Cardiology. 2020; 14: 1179546820977196. https://doi.org/10.1177/1179546820977196

25. Minocha P.K., Phoon C.K.L., Verma S., Singh R.K. Cardiac findings in pediatric patients with multisystem inflammatory syndrome in children associated with COVID-19. Clin. Pediatr. (Phila). 2021; 60(2): 119–26. https://doi.org/10.1177/0009922820961771

26. Kochi A.N., Tagliari A.P., Forleo G.B., Fassini G.M., Tondo C. Cardiac and arrhythmic complications in patients with COVID-19. J. Cardiovasc. Electrophysiol. 2020; 31(5): 1003–8. https://doi.org/10.1111/jce.14479

27. Rav-Acha M., Orlev A., Itzhaki I., Zimmerman S.F., Fteiha B., Bohm D., et al. Cardiac arrhythmias amongst hospitalised Coronavirus 2019 (COVID-19) patients: Prevalence, characterisation, and clinical algorithm to classify arrhythmic risk. Int. J. Clin. Pract. 2021; 75(4): e13788. https://doi.org/10.1111/ijcp.13788

28. Kozhevnikova O.V., Smirnov I.E. Risk factors for cardiovascular pathology in children: the properties of blood vessels and atherosclerosis. Rossiyskiy pediatricheskiy zhurnal. 2015; 18(4): 36–42. https://elibrary.ru/umbikd (in Russian)

29. Heching H.J., Goya A., Harvey B., Malloy-Walton L., Follansbee C., Mcintosh A., et al. Electrocardiographic changes in non-hospitalised children with COVID-19. Cardiol. Young. 2022; 32(12): 1910–6. https://doi.org/10.1017/S1047951121005138

30. Gartenberg A.J., White T.J., Dang K., Shah M., Paridon S.M., Elias M.D. Assessing the utility of screening electrocardiograms in paediatric patients following COVID-19. Cardiol. Young. 2022; 32(5): 711–7. https://doi.org/10.1017/S1047951121003012

31. Musin T.I., Bagmanova Z.A., Pavlov V.N., Gumerov R.M., Tyurin A.V., Talipova Kh.M., et al. Osborn wave in a patient with COVID-19: a case report. Rossiyskiy kardiologicheskiy zhurnal. 2021; 26(S1): 68–73. https://doi.org/10.15829/1560-4071-2021-4254 https://elibrary.ru/vjzzva (in Russian)

32. Joshi K., Kaplan D., Bakar A., Jennings J.F., Hayes D.A., Mahajan S., et al. Cardiac dysfunction and shock in pediatric patients with COVID-19. JACC Case Res. 2020; 2(9): 1267–70. https://doi.org/10.1016/j.jaccas.2020.05.082

33. Sirico D., Di Chiara C., Costenaro P., Bonfante F., Cozzani S., Plebani M., et al. Left ventricular longitudinal strain alterations in asymptomatic or mildly symptomatic paediatric patients with SARS-CoV-2 infection. Eur. Heart J. Cardiovasc. Imaging. 2022; 23(8): 1083–9. https://doi.org/10.1093/ehjci/jeab127

34. Shrestha L.B., Foster C., Rawlinson W., Tedla N., Bull R.A. Evolution of the SARS-CoV-2 omicron variants BA.1 to BA.5: Implications for immune escape and transmission. Rev. Med. Virol. 2022; 32(5): e2381. https://doi.org/10.1002/rmv.2381

35. Rodriguez-Gonzalez M., Castellano-Martinez A., Cascales-Poyatos H.M., Perez-Reviriego A.A. Cardiovascular impact of COVID-19 with a focus on children: A systematic review. World J. Clin. Cases. 2020; 8(21): 5250–83. https://doi.org/10.12998/wjcc.v8.i21.5250

36. Cantarutti N., Battista V., Adorisio R., Cicenia M., Campanello C., Listo E., et al. Cardiac manifestations in children with SARS-COV-2 infection: 1-year pediatric multicenter experience. Children. 2021; 8(8): 717. https://doi.org/10.3390/children8080717

37. Ozenen G., Kara A., Kiymet A., Boncuoglu E., Sahinkaya S., Cem E., et al. The evaluation of Troponin I levels and myocarditis in children with COVID-19: A pediatric single-center experience. Pediatr. Cardiol. 2023; 44(4): 873–81. https://doi.org/10.1007/s00246-022-03017-5

38. Kozhevnikova O.V., Abashidze E.A., Fisenko A.P., Akhmedova E.E., Logacheva O.S., Balabanov A.C., et al. Features of electrocardiogram in school-age children with COVID-19. Rossiyskiy pediatricheskiy zhurnal. 2021; 24(6): 372–80. https://doi.org/10.46563/1560-9561-2021-24-6-372-380 https://elibrary.ru/aedgmh (in Russian)

39. Lara D., Young T., Del Toro K., Chan V., Ianiro C., Hunt K., et al. Acute fulminant myocarditis in a pediatric patient with COVID-19 Infection. Pediatrics. 2020; 146(2): e20201509. https://doi.org/10.1542/peds.2020-1509

40. Yasuhara J., Watanabe K., Takagi H., Sumitomo N., Kuno T. COVID-19 and multisystem inflammatory syndrome in children: A systematic review and meta-analysis. Pediatric. Pulmonol. 2021; 56(5): 837–48. https://doi.org/10.1002/ppul.25245

41. Kelle S., Bucciarelli-Ducci C., Judd R.M., Kwong R.Y., Simonetti O., Plein S., et al. Society for cardiovascular magnetic resonance (SCMR) recommended CMR protocols for scanning patients with active or convalescent phase COVID-19 infection. J. Cardiovasc. Magn. Reson. 2020; 22(1): 61. https://doi.org/10.1186/s12968-020-00656-6

42. Petersen S.E., Friedrich M.G., Leiner T., Elias M.D., Ferreira V.M., Fenski M., et al. Cardiovascular magnetic resonance for patients with COVID-19. JACC Cardiovasc. Imaging. 2022; 15(4): 685–99. https://doi.org/10.1016/j.jcmg.2021.08.021

43. Cau R., Bassareo P., Saba L. Cardiac involvement in COVID-19-assessment with echocardiography and cardiac magnetic resonance imaging. SN Compr. Clin. Med. 2020; 2(7): 845–51. https://doi.org/10.1007/s42399-020-00344-7

44. Marrone A.C., Morrow G., Kelleman M.S., Lipinski J., Border W., Sachdeva R. Impact of the COVID pandemic on quality measures in a pediatric echocardiography lab. Prog. Pediatr. Cardiol. 2022; 67: 101549. https://doi.org/10.1016/j.ppedcard.2022.101549

45. Das B.B., Akam-Venkata J., Abdulkarim M., Hussain T. Parametric mapping cardiac magnetic resonance imaging for the diagnosis of myocarditis in children in the era of COVID-19 and MIS-C. Children (Basel). 2022; 9(7): 1061. https://doi.org/10.3390/children9071061

46. Peck D., Beaton A., Nunes M.C., Ollberding N., Hays A., Hiremath P., et al. Early triage echocardiography to predict outcomes in patients admitted with COVID-19: a multicenter study. Echocardiography. 2023; 40(5): 388–96. https://doi.org/10.1111/echo.15567

47. Hamedi K.R., Loftus G., Traylor L., Goodwin R., Arce S. Comparison of COVID-19 vaccine-associated myocarditis and viral myocarditis pathology. Vaccines (Basel). 2023; 11(2): 362. https://doi.org/10.3390/vaccines11020362

48. Carda S., Invernizzi M., Bavikatte G., Bensmaïl D., Bianchi F., Deltombe T., et al. The role of physical and rehabilitation medicine in the COVID-19 pandemic: the clinician’s view. Ann. Phys. Rehabil. Med. 2020; 63(6): 554–6. https://doi.org/10.1016/j.rehab.2020.04.001

49. Khan F., Amatya B. Medical rehabilitation in pandemics: towards a new perspective. J. Rehabil. Med. 2020; 52(4): jrm00043. https://doi.org/10.2340/16501977-2676

50. Madjid M., Safavi-Naeini P., Solomon S.D., Vardeny O. Potential effects of coronaviruses on the cardiovascular system: A Review. JAMA Cardiol. 2020; 5(7): 831–40. https://doi.org/10.1001/jamacardio.2020.1286