Cardiovascular involvement in COVID-19: A review
Main Article Content
Abstract
The COVID-19 pandemic, caused by the SARS-CoV-2 virus, has underscored the significant role of cardiovascular risk factors in determining the severity and outcomes of the disease. Pre-existing conditions such as hypertension, diabetes, obesity, and cardiovascular diseases have emerged as key contributors to increased susceptibility to severe forms of COVID-19, influencing both short-term and long-term health outcomes. This review examines the complex interplay between these risk factors and the virus’s direct impact on the cardiovascular system. Key findings suggest that conditions like hypertension, diabetes, and obesity not only predispose individuals to more severe disease but also exacerbate complications such as myocardial injury, arrhythmias, and heart failure. Furthermore, the long-term cardiovascular effects of COVID-19, including myocarditis and pericarditis, are of growing concern, particularly in patients with pre-existing cardiovascular conditions. The virus’s ability to induce myocardial damage through mechanisms involving ACE2 receptor binding and inflammatory cytokine storms has been well-documented. The pandemic has also highlighted significant cardiovascular complications, including left and right ventricular dysfunction, myocardial injury, and elevated pulmonary arterial pressure, with the right ventricle being particularly affected due to pulmonary damage. Imaging modalities such as echocardiography and cardiac magnetic resonance have proven valuable for diagnosing myocardial injury and complications, although accessibility may be limited in routine clinical practice. Survivors of severe COVID-19, especially those with pre-existing cardiovascular conditions, face an elevated risk of major adverse cardiovascular events for up to two years post-infection. Evaluation of post-COVID patients includes ECGs, laboratory tests, echocardiography, and cardiac MRI, which provide critical insights into myocardial injury and complications. Preventive measures, including vaccination, regular monitoring of cardiovascular health, and lifestyle modifications, play a crucial role in reducing the long-term risk of cardiovascular complications. The role of vaccination in mitigating the risk of severe disease and cardiovascular complications is well-established, despite rare cases of vaccine-related myocarditis. Understanding these interactions is essential for developing targeted management strategies, improving patient outcomes in both acute and long-term COVID-19 effects, and addressing the broader challenges posed by COVID-19’s impact on cardiovascular health.
Keywords:
COVID-19, cardiovascular complications, myocardial injury, hypertension, long-term effects, echocardiography, vaccination
Article Details
How to Cite
OSMANI, Zudi et al.
Cardiovascular involvement in COVID-19: A review.
Medical Research Archives, [S.l.], v. 13, n. 2, feb. 2025.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/6208>. Date accessed: 17 mar. 2025.
doi: https://doi.org/10.18103/mra.v13i2.6208.
Section
Review Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Mehra MR, Desai SS, Kuy S, Henry TD, Patel AN. Cardiovascular disease, drug therapy, and mortality in Covid-19. N Engl J Med. 2020;382:e102. doi: 10.1056/NEJMoa2007621
2. Kemerley A, Gupta A, Thirunavukkarasu M, Maloney M, Burgwardt S, Maulik N. COVID-19 Associated Cardiovascular Disease—Risks, Prevention and Management: Heart at Risk Due to COVID-19. Curr Issues Mol Biol. 2024;46:1904-1920. doi: 10.3390/cimb460301241
3. Chudzik M, Kapusta J. Cardiovascular Complications of COVID-19: Acute and Long-Term Impacts. Springer. 2023:379-400.
4. Bousquet J, Anto JM, Iaccarino G, et al. Is diet partly responsible for differences in COVID-19 death rates between and within countries? Clin Transl Allergy. 2020;10:16. doi: 10.1186/s13601-020-00323-0
5. Li X, Xu S, Yu M, et al. Risk factors for severity and mortality in adult COVID-19 inpatients in Wuhan. J Allergy Clin Immunol. 2020;146(1):110-118. doi: 10.1016/j.jaci.2020.04.006
6. Kamyshnyi A, Krynytska I, Matskevych V, Marushchak M, Lushchak O. Arterial Hypertension as a Risk Comorbidity Associated with COVID-19 Pathology. Int J Hypertens. 2020;2020:8019360. Published 2020 Dec 4. doi:10.1155/2020/8019360
7. Lippi G, Wong J, Henry BM. Hypertension in patients with coronavirus disease 2019 (COVID-19): a pooled analysis. Pol Arch Intern Med. 2020;130(4):304-309. doi:10.20452/pamw.15272
8. South AM, Brady TM, Flynn JT. ACE2 (Angiotensin-Converting Enzyme 2), COVID-19, and ACE inhibitor and ang II (Angiotensin II) receptor blocker use during the pandemic: the pediatric perspective. Hypertension. 2020;76(1):16 -22. doi: 10.1161/HYPERTENSIONAHA.120.15291
9. World Health Organization. Obesity and Overweight (2020). Available at: https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight. Accessed December 15, 2024.
10. Kalligeros M, Shehadeh F, Mylona EK, et al. Association of Obesity With Disease Severity Among Patients With Coronavirus Disease 2019. Obesity (Silver Spring). 2020;28(7):1200-1204. doi: 10.1002/oby.22859
11. Centers for Disease Control and Prevention. Obesity, Race/Ethnicity, and COVID-19. 2020. Available at: https://www.cdc.gov/obesity/data/obesity-and-covid-19.html. Accessed December 12, 2024.
12. Hendren NS, de Lemos JA, Ayers C, et al. Association of Body Mass Index and Age With Morbidity and Mortality in Patients Hospitalized With COVID-19: Results From the American Heart Association COVID-19 Cardiovascular Disease Registry. Circulation. 2021;143(2):135-144. doi: 10.1161/CIRCULATIONAHA.120.051936
13. Walkey AJ, Kumar VK, Harhay MO, et al. The Viral Infection and Respiratory Illness Universal Study (VIRUS): An International Registry of Coronavirus 2019-Related Critical Illness. Crit Care Explor. 2020;2(4):e0113. doi: 10.1097/CCE.00000 00000000113
14. Zupo R, Castellana F, Sardone R, et al. Preliminary Trajectories in Dietary Behaviors During the COVID-19 Pandemic: A Public Health Call to Action to Face Obesity. Int J Environ Res Public Health. 2020;17(19):7073. doi: 10.3390/ijerp h17197073
15. Gregory JM, Slaughter JC, Duffus SH, et al. COVID-19 Severity Is Tripled in the Diabetes Community: A Prospective Analysis of the Pandemic’s Impact in Type 1 and Type 2 Diabetes. Diabetes Care. 2021;44(2):526-532. doi: 10.2337/dc20-2260
16. Conte C, Cipponeri E, Roden M. Diabetes Mellitus, Energy Metabolism, and COVID-19. Endocr Rev. 2024;45(2):281-308. doi: 10.1210/ endrev/bnad026
17. Zamorano Cuervo N, Grandvaux N. ACE2: Evidence of role as entry receptor for SARS-CoV-2 and implications in comorbidities. eLife. 2020;9: e61390. doi: 10.7554/eLife.61390
18. Roca-Ho H, Riera M, Palau V, et al. Characterization of ACE and ACE2 Expression within Different Organs of the NOD Mouse. Int J Mol Sci. 2017;18(3):563. doi: 10.3390/ijms18030563
19. Valencia I, Lumpuy-Castillo J, Magalhaes G, et al. Mechanisms of endothelial activation, hypercoagulation and thrombosis in COVID-19: a link with diabetes mellitus. Cardiovasc Diabetol. 2024;23:75. doi: 10.1186/s12933-023-02097-8
20. Heshmati HM. Interactions between COVID-19 infection and diabetes. Front Endocrinol (Lausanne). 2024;14:1306290. doi: 10.3389/fendo.2023.1306290
21. Nagar M, Geevarughese NM, Mishra R, et al. Body-mass index COVID-19 severity: A systematic review of systematic reviews. J Fam Med Prim Care. 2022;11(9):5351-5360. doi: 10.4103/jfmpc. jfmpc_396_22
22. Khamidullina Z, Avzaletdinova D, Gareeva D, et al. Long-Term Outcomes of COVID-19 in Hospitalized Type 2 Diabetes Mellitus Patients. Biomedicines. 2024;12(2):467. doi: 10.3390/biome dicines12020467
23. Saran R, Robinson B, Abbott KC, et al. US renal data system 2018 annual data report: epidemiology of kidney disease in the United States. Am J Kidney Dis. 2019;73(3):A7-8. doi: 10.1053/j.ajkd.2019.01.001
24. Cheng Y, Luo R, Wang K, et al. Kidney disease is associated with in-hospital death of patients with COVID-19. Kidney Int. 2020;97:829-838. doi: 10.1016/j.kint.2020.03.005
25. Yang L, Mao B, Liang J, et al. Association between age and clinical characteristics and outcomes of COVID-19. Eur Respir J. 2020;55(5): 2001112. doi: 10.1183/13993003.01112-2020
26. Centers for Disease Control and Prevention. People with Certain Medical Conditions and COVID-19 Risk Factors. 2024. Available online: https://www.cdc.gov/covid/risk-factors/index.html Accessed December 8, 2024.
27. Mousseaux E, Fayol A, Danchin N, et al. Association between coronary artery calcifications and 6-month mortality in hospitalized patients with COVID-19. Diagn Interv Imaging. 2021;102:717-725. doi: 10.1016/j.diii.2021.06.007
28. Angeli F, Marazzato J, Verdecchia P, et al. Joint effect of heart failure and coronary artery disease on the risk of death during hospitalization for COVID-19. Eur J Intern Med. 2021;89:81-86. doi: 10.1016/j.ejim.2021.04.007
29. Hessami A, Shamshirian A, Heydari K, et al. Cardiovascular diseases burden in COVID-19: Systematic review and meta-analysis. Am J Emerg Med. 2021;46:382-391. doi: 10.1016/j.ajem.2020.10.022
30. Wu Z, McGoogan JM. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72314 cases from the Chinese Center for Disease Control and Prevention. JAMA. 2020;323: 1239-1242. doi: 10.1001/jama.2020.2648
31. Shi S, Qin M, Shen B, et al. Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China. JAMA Cardiol. 2020;5:802-810. doi: 10.1001/jamacardio.2020.0950
32. Puntmann VO, Carerj ML, Wieters I, et al. Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19). JAMA Cardiol. 2020;5:1265-1273. doi: 10.1001/jamacard io.2020.3557
33. Xu Z, Shi L, Wang Y, et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med. 2020;8:420-422. doi: 10.1016/S2213-2600(20)30076-X
34. Long B, Brady WJ, Koyfman A, et al. Cardiovascular complications in COVID-19. Am J Emerg Med. 2020;38(7):1504-1507. doi: 10.1016/j. ajem.2020.04.048
35. Sardu, C.; Gambardella, J.; Morelli, M.B.; Wang, X.; Marfella, R.; Santulli, G. Hypertension, Thrombosis, Kidney Failure, and Diabetes: Is COVID-19 an Endothelial Disease? A Comprehensive Evaluation of Clinical and Basic Evidence. J. Clin. Med. 2020, 9, 1417. doi:10.3390/jcm9051417
36. Zhou L, Niu Z, Jiang X, et al. SARS-CoV-2 targets by the pscRNA profiling of ACE2, TMPRSS2 and Furin proteases. iScience. 2020;23:101744. doi: 10.1016/j.isci.2020.101744
37. Bavishi C, Bonow RO, Trivedi V, et al. Acute myocardial injury in patients hospitalized with COVID-19 infection: A review. Prog Cardiovasc Dis. 2020;63:682-689. doi: 10.1016/j.pcad.2020.03.015
38. Smolgovsky S, Ibeh U, Tamayo TP, et al. Adding insult to injury—Inflammation at the heart of cardiac fibrosis. Cell Signal. 2021;77:109828. doi:10.1016/j.cellsig.2020.109828
39. Ackermann M, Verleden SE, Kuehnel M, et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in COVID-19. N Engl J Med. 2020;383:120-128. doi:10.1056/NEJMoa2015432
40. Muus C, Luecken MD, Eraslan G, et al. Single-cell meta-analysis of SARS-CoV-2 entry genes across tissues and demographics. Nat Med. 2021;2 7:546-559. doi.org/10.1038/s41591-020-01227-z
41. Varga Z, Flammer AJ, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet. 2020;395:1417-1418. doi:10.10 16/S0140-6736(20)30937-5
42. Bonow RO, Fonarow GC, O’Gara PT, et al. Association of coronavirus disease 2019 (COVID-19) with myocardial injury and mortality. JAMA Cardiol. 2020;5(7):751-753. doi:10.1001/jamacardi o.2020.1105
43. Moayed MS, Rahimi-Bashar F, Vahedian-Azimi A, et al. Cardiac injury in COVID-19: a systematic review. Adv Exp Med Biol. 2021;1321:325-333. doi:10.1007/978-3-030-59261-5_29
44. Lala A, Johnson KW, Januzzi JL, et al. Prevalence and impact of myocardial injury in patients hospitalized with COVID-19 infection. J Am Coll Cardiol. 2020;76:533-546. doi:10.1016/j.ja cc.2020.06.007
45. Fairweather D, Beetler DJ, Di Florio DN, Musigk N, Heidecker B, Cooper LT Jr. COVID-19, myocarditis and pericarditis. Circ Res. 2023;132:13 02-1319. doi:10.1161/CIRCRESAHA.123.321878
46. Allayee H, et al. COVID-19 is a coronary artery disease risk equivalent and exhibits a genetic interaction with ABO blood type. Arterioscler Thromb Vasc Biol. 2024. doi:10.1161/ATVBAHA. 124.321001
47. Lovell JP, Čiháková D, Gilotra NA. COVID-19 and Myocarditis: Review of Clinical Presentations, Pathogenesis and Management. Heart Int. 2022;16(1):20-27. doi: 10.17925/HI.2022.16.1.20.
48. Castiello T, Georgios P, Finnochiaro G et al. COVID-19 and myocarditis: a systematic review and overview of current challenges. Heart Fail Rev. 2022;27:251–261. doi.org/10.1007/s10741-021-10087-9
49. Oster ME, Shay DK, Su JR, Gee J, Creech CB, Broder KR, et al. Myocarditis Cases Reported After mRNA-Based COVID-19 Vaccination in the US From December 2020 to August 2021. JAMA 2022. 327, 331–340. doi:10.1001/jama.2021.24110
50. Cardiologia. 1957;30:1-8. doi:10.1159/000165631
51. Feery BJ. Adverse reactions after smallpox vaccination. Med J Aust. 1977;2(4):180-183. doi:10.5694/j.1326-5377.1977.tb114544.x
52. Halsell JS, Riddle JR, Atwood JE, et al. Myopericarditis following smallpox vaccination among vaccinia-naive US military personnel. JAMA. 2003;289(24):3283-3289. doi:10.1001/jama .289.24.3283
53. Salah HM, Mehta JL. COVID-19 vaccine and myocarditis. Am J Cardiol. 2021;157:146-148. doi:10.1016/j.amjcard.2021.07.009
54. Barouch DH. COVID-19 vaccines—immunity, variants, boosters. N Engl J Med. 2022;387(11): 1011-1020. doi:10.1056/NEJMra2206573.
55. Haas EJ, Angulo FJ, McLaughlin JM, et al. Impact and effectiveness of mRNA BNT162b2 vaccine against SARS-CoV-2 infections and COVID-19 cases, hospitalisations, and deaths following a nationwide vaccination campaign in Israel: an observational study using national surveillance data. Lancet. 2021;397(10287):1819-1829. doi:10.1016/S0140-6736(21)00947-8
56. Lopez Bernal J, Andrews N, Gower C, et al. Effectiveness of the Pfizer-BioNTech and Oxford-AstraZeneca vaccines on COVID-19 related symptoms, hospital admissions, and mortality in older adults in England: test negative case-control study. BMJ. 2021;373:n1088. doi:10.1136/bmj.n1088
57. Lv G, Yuan J, Xiong X, Li M. Mortality rate and characteristics of deaths following COVID-19 vaccination. Front Med. 2021;8:670370. doi:10.33 89/fmed.2021.670370
58. Carrizales-Sepúlveda EF, Vera-Pineda R, Flores-Ramírez R, et al. Echocardiographic manifestations in COVID-19: a review. Heart Lung Circ. 2021;30 (8):1117-1129. doi:10.1016/j.hlc.2020.12.004
59. Jain SS, Liu Q, Raikhelkar J, et al. Indications for and findings on transthoracic echocardiography in COVID-19. J Am Soc Echocardiogr. 2020;33 (10):1278-1284. doi:10.1016/j.echo.2020.06.009
60. Stöbe S, Richter S, Seige M, Stehr S, Laufs U, Hagendorff A. Echocardiographic characteristics of patients with SARS-CoV-2 infection. Clin Res Cardiol. 2020;109(12):1549-1566. doi:10.1007/s00 392-020-01727-5
61. Barssoum K, Victor V, Salem A, et al. Echocardiography, lung ultrasound, and cardiac magnetic resonance findings in COVID-19: A systematic review. Echocardiography. 2021;38(8):1 365-1404. doi:10.1111/echo.15152
62. Szekely Y, Lichter Y, Taieb P, et al. Spectrum of cardiac manifestations in COVID-19: a systematic echocardiographic study. Circulation. 2020;142(4): 342-353. doi:10.1161/CIRCULATIONAHA.120.047971.
63. Baycan OF, Barman HA, Atici A, et al. Evaluation of biventricular function in patients with COVID-19 using speckle tracking echocardiography. Int J Cardiovasc Imaging. 2021;37:135-144. doi:10.1007/s10554-020-01968-5
64. Knight R, Walker V, Ip S, et al; CVD-COVID-UK/COVID-IMPACT Consortium and the Longitudinal Health and Wellbeing COVID-19 National Core Study. Association of COVID-19 with major arterial and venous thrombotic diseases: a population-wide cohort study of 48 million adults in England and Wales. Circulation. 2022;146:892-906. doi:10.1161/CIRCULATIONAHA.122.060785
65. Bowe B, Xie Y, Al-Aly Z. Postacute sequelae of COVID-19 at 2 years. Nat Med. 2023.29:2347-2357. doi:10.1038/s41591-023-02521-2
66. Writing Committee for the COMEBAC Study Group; Morin L, Savale L, Pham T, Colle R, Figueiredo S, Harrois A, Gasnier M, Lecoq AL, Meyrignac O, Noel N, Baudry E, Bellin MF, Beurnier A, Choucha W, Corruble E, Dortet L, Hardy-Leger I, Radiguer F, Sportouch S, Verny C, Wyplosz B, Zaidan M, Becquemont L, Montani D, Monnet X. Four-Month Clinical Status of a Cohort of Patients After Hospitalization for COVID-19. JAMA. 2021 Apr 20;325(15):1525-1534. doi: 10. 1001/jama.2021.3331. Erratum in: JAMA. 2021 Nov 9;326(18):1874. doi: 10.1001/jama.2021.19113.
67. Writing Committee; Gluckman TJ, Bhave NM, Allen LA, Chung EH, Spatz ES, Ammirati E, Baggish AL, Bozkurt B, Cornwell WK 3rd, Harmon KG, Kim JH, Lala A, Levine BD, Martinez MW, Onuma O, Phelan D, Puntmann VO, Rajpal S, Taub PR, Verma AK. 2022 ACC Expert Consensus Decision Pathway on Cardiovascular Sequelae of COVID-19 in Adults: Myocarditis and Other Myocardial Involvement, Post-Acute Sequelae of SARS-CoV-2 Infection, and Return to Play: A Report of the American College of Cardiology Solution Set Oversight Committee. J Am Coll Cardiol. 2022 May 3;79(17):1717-1756. doi: 10.1016/j.jacc.2022.02.003
68. Beladiya J, Kumar A, Vasava Y, et al. Safety and efficacy of COVID-19 vaccines: a systematic review and meta-analysis of controlled and randomized clinical trials. Rev Med Virol. 2024; 34(1):e2507. doi:10.1002/rmv.2507
2. Kemerley A, Gupta A, Thirunavukkarasu M, Maloney M, Burgwardt S, Maulik N. COVID-19 Associated Cardiovascular Disease—Risks, Prevention and Management: Heart at Risk Due to COVID-19. Curr Issues Mol Biol. 2024;46:1904-1920. doi: 10.3390/cimb460301241
3. Chudzik M, Kapusta J. Cardiovascular Complications of COVID-19: Acute and Long-Term Impacts. Springer. 2023:379-400.
4. Bousquet J, Anto JM, Iaccarino G, et al. Is diet partly responsible for differences in COVID-19 death rates between and within countries? Clin Transl Allergy. 2020;10:16. doi: 10.1186/s13601-020-00323-0
5. Li X, Xu S, Yu M, et al. Risk factors for severity and mortality in adult COVID-19 inpatients in Wuhan. J Allergy Clin Immunol. 2020;146(1):110-118. doi: 10.1016/j.jaci.2020.04.006
6. Kamyshnyi A, Krynytska I, Matskevych V, Marushchak M, Lushchak O. Arterial Hypertension as a Risk Comorbidity Associated with COVID-19 Pathology. Int J Hypertens. 2020;2020:8019360. Published 2020 Dec 4. doi:10.1155/2020/8019360
7. Lippi G, Wong J, Henry BM. Hypertension in patients with coronavirus disease 2019 (COVID-19): a pooled analysis. Pol Arch Intern Med. 2020;130(4):304-309. doi:10.20452/pamw.15272
8. South AM, Brady TM, Flynn JT. ACE2 (Angiotensin-Converting Enzyme 2), COVID-19, and ACE inhibitor and ang II (Angiotensin II) receptor blocker use during the pandemic: the pediatric perspective. Hypertension. 2020;76(1):16 -22. doi: 10.1161/HYPERTENSIONAHA.120.15291
9. World Health Organization. Obesity and Overweight (2020). Available at: https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight. Accessed December 15, 2024.
10. Kalligeros M, Shehadeh F, Mylona EK, et al. Association of Obesity With Disease Severity Among Patients With Coronavirus Disease 2019. Obesity (Silver Spring). 2020;28(7):1200-1204. doi: 10.1002/oby.22859
11. Centers for Disease Control and Prevention. Obesity, Race/Ethnicity, and COVID-19. 2020. Available at: https://www.cdc.gov/obesity/data/obesity-and-covid-19.html. Accessed December 12, 2024.
12. Hendren NS, de Lemos JA, Ayers C, et al. Association of Body Mass Index and Age With Morbidity and Mortality in Patients Hospitalized With COVID-19: Results From the American Heart Association COVID-19 Cardiovascular Disease Registry. Circulation. 2021;143(2):135-144. doi: 10.1161/CIRCULATIONAHA.120.051936
13. Walkey AJ, Kumar VK, Harhay MO, et al. The Viral Infection and Respiratory Illness Universal Study (VIRUS): An International Registry of Coronavirus 2019-Related Critical Illness. Crit Care Explor. 2020;2(4):e0113. doi: 10.1097/CCE.00000 00000000113
14. Zupo R, Castellana F, Sardone R, et al. Preliminary Trajectories in Dietary Behaviors During the COVID-19 Pandemic: A Public Health Call to Action to Face Obesity. Int J Environ Res Public Health. 2020;17(19):7073. doi: 10.3390/ijerp h17197073
15. Gregory JM, Slaughter JC, Duffus SH, et al. COVID-19 Severity Is Tripled in the Diabetes Community: A Prospective Analysis of the Pandemic’s Impact in Type 1 and Type 2 Diabetes. Diabetes Care. 2021;44(2):526-532. doi: 10.2337/dc20-2260
16. Conte C, Cipponeri E, Roden M. Diabetes Mellitus, Energy Metabolism, and COVID-19. Endocr Rev. 2024;45(2):281-308. doi: 10.1210/ endrev/bnad026
17. Zamorano Cuervo N, Grandvaux N. ACE2: Evidence of role as entry receptor for SARS-CoV-2 and implications in comorbidities. eLife. 2020;9: e61390. doi: 10.7554/eLife.61390
18. Roca-Ho H, Riera M, Palau V, et al. Characterization of ACE and ACE2 Expression within Different Organs of the NOD Mouse. Int J Mol Sci. 2017;18(3):563. doi: 10.3390/ijms18030563
19. Valencia I, Lumpuy-Castillo J, Magalhaes G, et al. Mechanisms of endothelial activation, hypercoagulation and thrombosis in COVID-19: a link with diabetes mellitus. Cardiovasc Diabetol. 2024;23:75. doi: 10.1186/s12933-023-02097-8
20. Heshmati HM. Interactions between COVID-19 infection and diabetes. Front Endocrinol (Lausanne). 2024;14:1306290. doi: 10.3389/fendo.2023.1306290
21. Nagar M, Geevarughese NM, Mishra R, et al. Body-mass index COVID-19 severity: A systematic review of systematic reviews. J Fam Med Prim Care. 2022;11(9):5351-5360. doi: 10.4103/jfmpc. jfmpc_396_22
22. Khamidullina Z, Avzaletdinova D, Gareeva D, et al. Long-Term Outcomes of COVID-19 in Hospitalized Type 2 Diabetes Mellitus Patients. Biomedicines. 2024;12(2):467. doi: 10.3390/biome dicines12020467
23. Saran R, Robinson B, Abbott KC, et al. US renal data system 2018 annual data report: epidemiology of kidney disease in the United States. Am J Kidney Dis. 2019;73(3):A7-8. doi: 10.1053/j.ajkd.2019.01.001
24. Cheng Y, Luo R, Wang K, et al. Kidney disease is associated with in-hospital death of patients with COVID-19. Kidney Int. 2020;97:829-838. doi: 10.1016/j.kint.2020.03.005
25. Yang L, Mao B, Liang J, et al. Association between age and clinical characteristics and outcomes of COVID-19. Eur Respir J. 2020;55(5): 2001112. doi: 10.1183/13993003.01112-2020
26. Centers for Disease Control and Prevention. People with Certain Medical Conditions and COVID-19 Risk Factors. 2024. Available online: https://www.cdc.gov/covid/risk-factors/index.html Accessed December 8, 2024.
27. Mousseaux E, Fayol A, Danchin N, et al. Association between coronary artery calcifications and 6-month mortality in hospitalized patients with COVID-19. Diagn Interv Imaging. 2021;102:717-725. doi: 10.1016/j.diii.2021.06.007
28. Angeli F, Marazzato J, Verdecchia P, et al. Joint effect of heart failure and coronary artery disease on the risk of death during hospitalization for COVID-19. Eur J Intern Med. 2021;89:81-86. doi: 10.1016/j.ejim.2021.04.007
29. Hessami A, Shamshirian A, Heydari K, et al. Cardiovascular diseases burden in COVID-19: Systematic review and meta-analysis. Am J Emerg Med. 2021;46:382-391. doi: 10.1016/j.ajem.2020.10.022
30. Wu Z, McGoogan JM. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72314 cases from the Chinese Center for Disease Control and Prevention. JAMA. 2020;323: 1239-1242. doi: 10.1001/jama.2020.2648
31. Shi S, Qin M, Shen B, et al. Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China. JAMA Cardiol. 2020;5:802-810. doi: 10.1001/jamacardio.2020.0950
32. Puntmann VO, Carerj ML, Wieters I, et al. Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19). JAMA Cardiol. 2020;5:1265-1273. doi: 10.1001/jamacard io.2020.3557
33. Xu Z, Shi L, Wang Y, et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med. 2020;8:420-422. doi: 10.1016/S2213-2600(20)30076-X
34. Long B, Brady WJ, Koyfman A, et al. Cardiovascular complications in COVID-19. Am J Emerg Med. 2020;38(7):1504-1507. doi: 10.1016/j. ajem.2020.04.048
35. Sardu, C.; Gambardella, J.; Morelli, M.B.; Wang, X.; Marfella, R.; Santulli, G. Hypertension, Thrombosis, Kidney Failure, and Diabetes: Is COVID-19 an Endothelial Disease? A Comprehensive Evaluation of Clinical and Basic Evidence. J. Clin. Med. 2020, 9, 1417. doi:10.3390/jcm9051417
36. Zhou L, Niu Z, Jiang X, et al. SARS-CoV-2 targets by the pscRNA profiling of ACE2, TMPRSS2 and Furin proteases. iScience. 2020;23:101744. doi: 10.1016/j.isci.2020.101744
37. Bavishi C, Bonow RO, Trivedi V, et al. Acute myocardial injury in patients hospitalized with COVID-19 infection: A review. Prog Cardiovasc Dis. 2020;63:682-689. doi: 10.1016/j.pcad.2020.03.015
38. Smolgovsky S, Ibeh U, Tamayo TP, et al. Adding insult to injury—Inflammation at the heart of cardiac fibrosis. Cell Signal. 2021;77:109828. doi:10.1016/j.cellsig.2020.109828
39. Ackermann M, Verleden SE, Kuehnel M, et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in COVID-19. N Engl J Med. 2020;383:120-128. doi:10.1056/NEJMoa2015432
40. Muus C, Luecken MD, Eraslan G, et al. Single-cell meta-analysis of SARS-CoV-2 entry genes across tissues and demographics. Nat Med. 2021;2 7:546-559. doi.org/10.1038/s41591-020-01227-z
41. Varga Z, Flammer AJ, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet. 2020;395:1417-1418. doi:10.10 16/S0140-6736(20)30937-5
42. Bonow RO, Fonarow GC, O’Gara PT, et al. Association of coronavirus disease 2019 (COVID-19) with myocardial injury and mortality. JAMA Cardiol. 2020;5(7):751-753. doi:10.1001/jamacardi o.2020.1105
43. Moayed MS, Rahimi-Bashar F, Vahedian-Azimi A, et al. Cardiac injury in COVID-19: a systematic review. Adv Exp Med Biol. 2021;1321:325-333. doi:10.1007/978-3-030-59261-5_29
44. Lala A, Johnson KW, Januzzi JL, et al. Prevalence and impact of myocardial injury in patients hospitalized with COVID-19 infection. J Am Coll Cardiol. 2020;76:533-546. doi:10.1016/j.ja cc.2020.06.007
45. Fairweather D, Beetler DJ, Di Florio DN, Musigk N, Heidecker B, Cooper LT Jr. COVID-19, myocarditis and pericarditis. Circ Res. 2023;132:13 02-1319. doi:10.1161/CIRCRESAHA.123.321878
46. Allayee H, et al. COVID-19 is a coronary artery disease risk equivalent and exhibits a genetic interaction with ABO blood type. Arterioscler Thromb Vasc Biol. 2024. doi:10.1161/ATVBAHA. 124.321001
47. Lovell JP, Čiháková D, Gilotra NA. COVID-19 and Myocarditis: Review of Clinical Presentations, Pathogenesis and Management. Heart Int. 2022;16(1):20-27. doi: 10.17925/HI.2022.16.1.20.
48. Castiello T, Georgios P, Finnochiaro G et al. COVID-19 and myocarditis: a systematic review and overview of current challenges. Heart Fail Rev. 2022;27:251–261. doi.org/10.1007/s10741-021-10087-9
49. Oster ME, Shay DK, Su JR, Gee J, Creech CB, Broder KR, et al. Myocarditis Cases Reported After mRNA-Based COVID-19 Vaccination in the US From December 2020 to August 2021. JAMA 2022. 327, 331–340. doi:10.1001/jama.2021.24110
50. Cardiologia. 1957;30:1-8. doi:10.1159/000165631
51. Feery BJ. Adverse reactions after smallpox vaccination. Med J Aust. 1977;2(4):180-183. doi:10.5694/j.1326-5377.1977.tb114544.x
52. Halsell JS, Riddle JR, Atwood JE, et al. Myopericarditis following smallpox vaccination among vaccinia-naive US military personnel. JAMA. 2003;289(24):3283-3289. doi:10.1001/jama .289.24.3283
53. Salah HM, Mehta JL. COVID-19 vaccine and myocarditis. Am J Cardiol. 2021;157:146-148. doi:10.1016/j.amjcard.2021.07.009
54. Barouch DH. COVID-19 vaccines—immunity, variants, boosters. N Engl J Med. 2022;387(11): 1011-1020. doi:10.1056/NEJMra2206573.
55. Haas EJ, Angulo FJ, McLaughlin JM, et al. Impact and effectiveness of mRNA BNT162b2 vaccine against SARS-CoV-2 infections and COVID-19 cases, hospitalisations, and deaths following a nationwide vaccination campaign in Israel: an observational study using national surveillance data. Lancet. 2021;397(10287):1819-1829. doi:10.1016/S0140-6736(21)00947-8
56. Lopez Bernal J, Andrews N, Gower C, et al. Effectiveness of the Pfizer-BioNTech and Oxford-AstraZeneca vaccines on COVID-19 related symptoms, hospital admissions, and mortality in older adults in England: test negative case-control study. BMJ. 2021;373:n1088. doi:10.1136/bmj.n1088
57. Lv G, Yuan J, Xiong X, Li M. Mortality rate and characteristics of deaths following COVID-19 vaccination. Front Med. 2021;8:670370. doi:10.33 89/fmed.2021.670370
58. Carrizales-Sepúlveda EF, Vera-Pineda R, Flores-Ramírez R, et al. Echocardiographic manifestations in COVID-19: a review. Heart Lung Circ. 2021;30 (8):1117-1129. doi:10.1016/j.hlc.2020.12.004
59. Jain SS, Liu Q, Raikhelkar J, et al. Indications for and findings on transthoracic echocardiography in COVID-19. J Am Soc Echocardiogr. 2020;33 (10):1278-1284. doi:10.1016/j.echo.2020.06.009
60. Stöbe S, Richter S, Seige M, Stehr S, Laufs U, Hagendorff A. Echocardiographic characteristics of patients with SARS-CoV-2 infection. Clin Res Cardiol. 2020;109(12):1549-1566. doi:10.1007/s00 392-020-01727-5
61. Barssoum K, Victor V, Salem A, et al. Echocardiography, lung ultrasound, and cardiac magnetic resonance findings in COVID-19: A systematic review. Echocardiography. 2021;38(8):1 365-1404. doi:10.1111/echo.15152
62. Szekely Y, Lichter Y, Taieb P, et al. Spectrum of cardiac manifestations in COVID-19: a systematic echocardiographic study. Circulation. 2020;142(4): 342-353. doi:10.1161/CIRCULATIONAHA.120.047971.
63. Baycan OF, Barman HA, Atici A, et al. Evaluation of biventricular function in patients with COVID-19 using speckle tracking echocardiography. Int J Cardiovasc Imaging. 2021;37:135-144. doi:10.1007/s10554-020-01968-5
64. Knight R, Walker V, Ip S, et al; CVD-COVID-UK/COVID-IMPACT Consortium and the Longitudinal Health and Wellbeing COVID-19 National Core Study. Association of COVID-19 with major arterial and venous thrombotic diseases: a population-wide cohort study of 48 million adults in England and Wales. Circulation. 2022;146:892-906. doi:10.1161/CIRCULATIONAHA.122.060785
65. Bowe B, Xie Y, Al-Aly Z. Postacute sequelae of COVID-19 at 2 years. Nat Med. 2023.29:2347-2357. doi:10.1038/s41591-023-02521-2
66. Writing Committee for the COMEBAC Study Group; Morin L, Savale L, Pham T, Colle R, Figueiredo S, Harrois A, Gasnier M, Lecoq AL, Meyrignac O, Noel N, Baudry E, Bellin MF, Beurnier A, Choucha W, Corruble E, Dortet L, Hardy-Leger I, Radiguer F, Sportouch S, Verny C, Wyplosz B, Zaidan M, Becquemont L, Montani D, Monnet X. Four-Month Clinical Status of a Cohort of Patients After Hospitalization for COVID-19. JAMA. 2021 Apr 20;325(15):1525-1534. doi: 10. 1001/jama.2021.3331. Erratum in: JAMA. 2021 Nov 9;326(18):1874. doi: 10.1001/jama.2021.19113.
67. Writing Committee; Gluckman TJ, Bhave NM, Allen LA, Chung EH, Spatz ES, Ammirati E, Baggish AL, Bozkurt B, Cornwell WK 3rd, Harmon KG, Kim JH, Lala A, Levine BD, Martinez MW, Onuma O, Phelan D, Puntmann VO, Rajpal S, Taub PR, Verma AK. 2022 ACC Expert Consensus Decision Pathway on Cardiovascular Sequelae of COVID-19 in Adults: Myocarditis and Other Myocardial Involvement, Post-Acute Sequelae of SARS-CoV-2 Infection, and Return to Play: A Report of the American College of Cardiology Solution Set Oversight Committee. J Am Coll Cardiol. 2022 May 3;79(17):1717-1756. doi: 10.1016/j.jacc.2022.02.003
68. Beladiya J, Kumar A, Vasava Y, et al. Safety and efficacy of COVID-19 vaccines: a systematic review and meta-analysis of controlled and randomized clinical trials. Rev Med Virol. 2024; 34(1):e2507. doi:10.1002/rmv.2507