Cardiovascular abnormalities of long-COVID syndrome: Pathogenic basis and potential strategy for treatment and rehabilitation

Kainuo Wu, Jonathan Van Name, Lei Xi

Sports Medicine and Health Science ›› 2024, Vol. 6 ›› Issue (3) : 221-231.

Sports Medicine and Health Science All Journals
Sports Medicine and Health Science ›› 2024, Vol. 6 ›› Issue (3) : 221-231. DOI: 10.1016/j.smhs.2024.03.009
Review

Cardiovascular abnormalities of long-COVID syndrome: Pathogenic basis and potential strategy for treatment and rehabilitation

Author information +
History +

Abstract

Cardiac injury and sustained cardiovascular abnormalities in long-COVID syndrome, i.e. post-acute sequelae of coronavirus disease 2019 (COVID-19) have emerged as a debilitating health burden that has posed challenges for management of pre-existing cardiovascular conditions and other associated chronic comorbidities in the most vulnerable group of patients recovered from acute COVID-19. A clear and evidence-based guideline for treating cardiac issues of long-COVID syndrome is still lacking. In this review, we have summarized the common cardiac symptoms reported in the months after acute COVID-19 illness and further evaluated the possible pathogenic factors underlying the pathophysiology process of long-COVID. The mechanistic understanding of how Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) damages the heart and vasculatures is critical in developing targeted therapy and preventive measures for limiting the viral attacks. Despite the currently available therapeutic interventions, a considerable portion of patients recovered from severe COVID-19 have reported a reduced functional reserve due to deconditioning. Therefore, a rigorous and comprehensive cardiac rehabilitation program with individualized exercise protocols would be instrumental for the patients with long-COVID to regain the physical fitness levels comparable to their pre-illness baseline.

Keywords

Long-COVID syndrome / Cardiac rehabilitation / Exercise intolerance / Inflammation / Hypoxia inducible factor 1 / SARS-CoV-2 tropism

Cite this article

Download citation ▾
Kainuo Wu, Jonathan Van Name, Lei Xi. Cardiovascular abnormalities of long-COVID syndrome: Pathogenic basis and potential strategy for treatment and rehabilitation. Sports Medicine and Health Science, 2024, 6(3): 221‒231 https://doi.org/10.1016/j.smhs.2024.03.009
Ethical approval statement
All studies included in this review were ensured to have obtained informed consent from each participant, and that the study was reviewed by the affiliated institution(s) and received approval to implement the study.
Conflict of interest
The authors have no conflicts of interest to disclose.
Authors’ contributions
JRS conceptualized and drafted the manuscript. EEK, MAS, and JLD critically reviewed the manuscript. JMD and PWG reviewed the manuscript. XW conceptualized and critically reviewed the manuscript.

References

[1]
J.K. Logue, N.M. Franko, D.J. McCulloch, et al.. Sequelae in adults at 6 months after COVID-19 infection. JAMA Netw Open, 4 (2) ( 2021), Article e210830, DOI: 10.1001/jamanetworkopen.2021.0830
[2]
D. Ayoubkhani, K. Khunti, V. Nafilyan, et al.. Post-covid syndrome in individuals admitted to hospital with covid-19: retrospective cohort study. BMJ, 372 ( 2021), Article n693, DOI: 10.1136/bmj.n693
[3]
N. Mumoli, G. Conte, I. Evangelista, M. Cei, A. Mazzone, A. Colombo. Post-COVID or long-COVID: two different conditions or the same?. J Infect Public Health, 14 (10) ( 2021), pp. 1349-1350, DOI: 10.1016/j.jiph.2021.08.019
[4]
M. Lorente-Ros, S. Das, J. Elias, W.H. Frishman, W.S. Aronow. Cardiovascular manifestations of the long COVID syndrome. Cardiol Rev ( 2023 ; April 10), DOI: 10.1097/CRD.0000000000000552
[5]
L. Huang, P. Zhao, D. Tang, et al.. Cardiac involvement in patients recovered from COVID-2019 identified using magnetic resonance imaging. JACC Cardiovasc Imaging, 13 (11) ( 2020), pp. 2330-2339, DOI: 10.1016/j.jcmg.2020.05.004
[6]
M. Letko, A. Marzi, V. Munster. Functional assessment of cell entry and receptor usage for SARS-CoV-2 and other lineage B betacoronaviruses. Nat Microbiol, 5 (4) ( 2020), pp. 562-569, DOI: 10.1038/s41564-020-0688-y
[7]
C. Huang, L. Huang, Y. Wang, et al.. 6-month consequences of COVID-19 in patients discharged from hospital: a cohort study. Lancet, 397 (10270) ( 2021), pp. 220-232, DOI: 10.1016/S0140-6736(20)32656-8
[8]
J. Frija-Masson, M.P. Debray, S. Boussouar, et al.. Residual ground glass opacities three months after COVID-19 pneumonia correlate to alteration of respiratory function: the post COVID M3 study. Respir Med, 184 ( 2021), Article 106435, DOI: 10.1016/j.rmed.2021.106435
[9]
K.J. Myall, B. Mukherjee, A.M. Castanheira, et al.. Persistent post-COVID-19 interstitial lung disease. An observational study of corticosteroid treatment. Ann Am Thorac Soc, 18 (5) ( 2021), pp. 799-806, DOI: 10.1513/AnnalsATS.202008-1002OC
[10]
M. Gorecka, N. Jex, S. Thirunavukarasu, et al.. Cardiovascular magnetic resonance imaging and spectroscopy in clinical long-COVID-19 syndrome: a prospective case-control study. J Cardiovasc Magn Reson, 24 (1) ( 2022), p. 50, DOI: 10.1186/s12968-022-00887-9
[11]
K.L. Quinn, G.Y. Lam, J.F. Walsh, et al.. Cardiovascular considerations in the management of people with suspected long COVID. Can J Cardiol, 39 (6) ( 2023), pp. 741-753, DOI: 10.1016/j.cjca.2023.04.003
[12]
M. Sova, E. Sovova, J. Ozana, et al.. Post-COVID syndrome and cardiorespiratory fitness—26-month experience of single center. Life, 13 (3) ( 2023), p. 684, DOI: 10.3390/life13030684
[13]
I. Szoltysek-Boldys, W. Zielinska-Danch, D. Loboda, et al.. Photoplethysmographic measurement of arterial stiffness in Polish patients with Long-COVID-19 Syndrome—the results of a cross-sectional study. Diagnostics, 12 (12) ( 2022), p. 3189, DOI: 10.3390/diagnostics12123189
[14]
M. Pływaczewska-Jakubowska, M. Chudzik, M. Babicki, J. Kapusta, P. Jankowski. Lifestyle, course of COVID-19, and risk of long-COVID in non-hospitalized patients. Front Med, 9 ( 2022), Article 1036556, DOI: 10.3389/fmed.2022.1036556
[15]
M. Spinicci, L. Graziani, M. Tilli, et al.. Infection with SARS-CoV-2 variants is associated with different long COVID phenotypes. Viruses, 14 (11) ( 2022), p. 2367, DOI: 10.3390/v14112367
[16]
Z. Lin. More than a key—the pathological roles of SARS-CoV-2 spike protein in COVID-19 related cardiac injury. Sports Med Health Sci., 30 (2023 March), DOI: 10.1016/j.smhs.2023.03.004. Online ahead of print
[17]
M. Hoffmann, H. Kleine-Weber, S. Schroeder, et al.. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell, 181 (2) ( 2020), pp. 271-280.e8, DOI: 10.1016/j.cell.2020.02.052
[18]
A.C. Montezano, Dinh Nguyen, A. Cat, F.J. Rios, R.M. Touyz.Angiotensin II and vascular injury. Curr Hypertens Rep, 16 (6) ( 2014), p. 431, DOI: 10.1007/s11906-014-0431-2
[19]
D. Lindner, A. Fitzek, H. Bräuninger, et al.. Association of cardiac infection with SARS-CoV-2 in confirmed COVID-19 autopsy cases. JAMA Cardiol, 5 (11) ( 2020), p. 1281, DOI: 10.1001/jamacardio.2020.3551
[20]
C. Gemayel, A. Pelliccia, P.D. Thompson. Arrhythmogenic right ventricular cardiomyopathy. J Am Coll Cardiol, 38 (7) ( 2001), pp. 1773-1781, DOI: 10.1016/S0735-1097(01)01654-0
[21]
Y. Xie, E. Xu, B. Bowe, Z. Al-Aly.Long-term cardiovascular outcomes of COVID-19. Nat Med, 28 (3) ( 2022), pp. 583-590, DOI: 10.1038/s41591-022-01689-3
[22]
P.E. Lazzerini, P.L. Capecchi, N. El-Sherif, F. Laghi-Pasini, M. Boutjdir. Emerging arrhythmic risk of autoimmune and inflammatory cardiac channelopathies. J Am Heart Assoc, 7 (22) ( 2018), Article e010595, DOI: 10.1161/JAHA.118.010595
[23]
P.E. Lazzerini, F. Laghi-Pasini, M. Boutjdir, P.L. Capecchi. Cardioimmunology of arrhythmias: the role of autoimmune and inflammatory cardiac channelopathies. Nat Rev Immunol, 19 (1) ( 2019), pp. 63-64, DOI: 10.1038/s41577-018-0098-z
[24]
M. Gyöngyösi, P. Alcaide, F.W. Asselbergs, et al.. Long COVID and the cardiovascular system-elucidating causes and cellular mechanisms in order to develop targeted diagnostic and therapeutic strategies: a joint Scientific Statement of the ESC Working Groups on Cellular Biology of the Heart and Myocardial and Pericardial Diseases. Cardiovasc Res, 119 (2) ( 2023), pp. 336-356, DOI: 10.1093/cvr/cvac115
[25]
C. Edler, A.S. Schröder, M. Aepfelbacher, et al.. Dying with SARS-CoV-2 infection—an autopsy study of the first consecutive 80 cases in Hamburg, Germany. Int J Leg Med, 134 (4) ( 2020), pp. 1275-1284, DOI: 10.1007/s00414-020-02317-w
[26]
M.K. Halushka, R.S. Vander Heide.Myocarditis is rare in COVID-19 autopsies: cardiovascular findings across 277 postmortem examinations. Cardiovasc Pathol, 50 ( 2021), Article 107300, DOI: 10.1016/j.carpath.2020.107300
[27]
T. Chen, J. Song, H. Liu, H. Zheng, C. Chen.Positive Epstein-Barr virus detection in coronavirus disease 2019 (COVID-19) patients. Sci Rep, 11 (1) ( 2021), Article 10902, DOI: 10.1038/s41598-021-90351-y
[28]
B. Chen, B. Julg, S. Mohandas, S.B. Bradfute. Viral persistence, reactivation, and mechanisms of long COVID. Elife, 12 ( 2023), Article e86015, DOI: 10.7554/eLife.86015
[29]
M. Panigada, N. Bottino, P. Tagliabue, et al.. Hypercoagulability of COVID-19 patients in intensive care unit: a report of thromboelastography findings and other parameters of hemostasis. J Thromb Haemostasis, 18 (7) ( 2020), pp. 1738-1742, DOI: 10.1111/jth.14850
[30]
M.Y. Abou-Ismail, A. Diamond, S. Kapoor, Y. Arafah, L. Nayak. The hypercoagulable state in COVID-19: incidence, pathophysiology, and management. Thromb Res, 194 ( 2020), pp. 101-115, DOI: 10.1016/j.thromres.2020.06.029
[31]
Z. Varga, A.J. Flammer, P. Steiger, et al.. Endothelial cell infection and endotheliitis in COVID-19. Lancet, 395 (10234) ( 2020), pp. 1417-1418, DOI: 10.1016/S0140-6736(20)30937-5
[32]
S. Nagashima, M.C. Mendes, A.P. Camargo Martins, et al.. Endothelial dysfunction and thrombosis in patients with COVID-19—brief report. Arterioscler Thromb Vasc Biol, 40 (10) ( 2020), pp. 2404-2407, DOI: 10.1161/ATVBAHA.120.314860
[33]
Y.J. Lai, S.H. Liu, S. Manachevakul, T.A. Lee, C.T. Kuo, D. Bello. Biomarkers in long COVID-19: a systematic review. Front Med, 10 ( 2023), Article 1085988, DOI: 10.3389/fmed.2023.1085988
[34]
A.C. Montezano, L.L. Camargo, S. Mary, et al.. SARS-CoV-2 spike protein induces endothelial inflammation via ACE 2 independently of viral replication. Sci Rep, 13 (1) ( 2023), Article 14086, DOI: 10.1038/s41598-023-41115-3
[35]
L.A. Cosimi, C. Kelly, S. Esposito, et al.. Duration of symptoms and association with positive home rapid antigen test results after infection with SARS-CoV-2. JAMA Netw Open, 5 (8) ( 2022), Article e2225331, DOI: 10.1001/jamanetworkopen.2022.25331
[36]
C. Cervia-Hasler, S.C. Brüningk, T. Hoch, et al.. Persistent complement dysregulation with signs of thromboinflammation in active long COVID. Science, 383 (6680) ( 2024), p. eadg7942, DOI: 10.1126/science.adg7942
[37]
F. Bossi, L. Rizzi, R. Bulla, et al.. C 7 is expressed on endothelial cells as a trap for the assembling terminal complement complex and may exert anti-inflammatory function. Blood, 113 (15) ( 2009), pp. 3640-3648, DOI: 10.1182/blood-2008-03-146472
[38]
Y. Su, D. Yuan, D.G. Chen, et al.. Multiple early factors anticipate post-acute COVID-19 sequelae. Cell, 185 (5) ( 2022), pp. 881-895.e20, DOI: 10.1016/j.cell.2022.01.014
[39]
A. Gupta, M.V. Madhavan, K. Sehgal, et al.. Extrapulmonary manifestations of COVID-19. Nat Med, 26 (7) ( 2020), pp. 1017-1032, DOI: 10.1038/s41591-020-0968-3
[40]
W. Wang, C.Y. Wang, S.I. Wang, J.C.C. Wei. Long-term cardiovascular outcomes in COVID-19 survivors among non-vaccinated population: a retrospective cohort study from the TriNetX US collaborative networks. eClinicalMedicine, 53 ( 2022), Article 101619, DOI: 10.1016/j.eclinm.2022.101619
[41]
N. Tang, D. Li, X. Wang, Z. Sun. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemostasis, 18 (4) ( 2020), pp. 844-847, DOI: 10.1111/jth.14768
[42]
Z. Al-Aly, Y. Xie, B. Bowe.High-dimensional characterization of post-acute sequelae of COVID-19. Nature, 594 (7862) ( 2021), pp. 259-264, DOI: 10.1038/s41586-021-03553-9
[43]
D.C. de Menezes, P.D.L. de Lima, I.C. de Lima, et al.. Metabolic profile of patients with long COVID: a cross-sectional study. Nutrients, 15 (5) ( 2023), p. 1197, DOI: 10.3390/nu15051197
[44]
J.J. Frere, B.R. tenOever. Cardiometabolic syndrome — an emergent feature of Long COVID?. Nat Rev Immunol, 22 (7) ( 2022), pp. 399-400, DOI: 10.1038/s41577-022-00739-8
[45]
X. Tang, S. Uhl, T. Zhang, et al.. SARS-CoV-2 infection induces beta cell transdifferentiation. Cell Metabol, 33 (8) ( 2021), pp. 1577-1591.e7, DOI: 10.1016/j.cmet.2021.05.015
[46]
M. Reiterer, M. Rajan, N. Gómez-Banoy, et al.. Hyperglycemia in acute COVID-19 is characterized by insulin resistance and adipose tissue infectivity by SARS-CoV-2. Cell Metabol, 33 (11) ( 2021), pp. 2174-2188.e5, DOI: 10.1016/j.cmet.2021.09.009
[47]
H. Yanai, H. Yoshida.Beneficial effects of adiponectin on glucose and lipid metabolism and atherosclerotic progression: mechanisms and perspectives. Int J Mol Sci, 20 (5) ( 2019), p. 1190, DOI: 10.3390/ijms20051190
[48]
C. Sharma, J. Bayry.High risk of autoimmune diseases after COVID-19. Nat Rev Rheumatol, 19 (7) ( 2023), pp. 399-400, DOI: 10.1038/s41584-023-00964-y
[49]
O. Blagova, N. Varionchik, V. Zaidenov, P. Savina, N. Sarkisova.Anti-heart antibodies levels and their correlation with clinical symptoms and outcomes in patients with confirmed or suspected diagnosis COVID-19. Eur J Immunol, 51 (4) ( 2021), pp. 893-902, DOI: 10.1002/eji.202048930
[50]
B. Raman, D.A. Bluemke, T.F. Lüscher, S. Neubauer. Long COVID: post-acute sequelae of COVID-19 with a cardiovascular focus. Eur Heart J, 43 (11) ( 2022), pp. 1157-1172, DOI: 10.1093/eurheartj/ehac031
[51]
E.Y. Wang, T. Mao, J. Klein, et al.. Diverse functional autoantibodies in patients with COVID-19. Nature, 595 (7866) ( 2021), pp. 283-288, DOI: 10.1038/s41586-021-03631-y
[52]
A. Utrero-Rico, M. Ruiz-Ruigómez, R. Laguna-Goya, et al.. A short corticosteroid course reduces symptoms and immunological alterations underlying long-COVID. Biomedicines, 9 (11) ( 2021), p. 1540, DOI: 10.3390/biomedicines9111540
[53]
D. Radovanovic, M. Rizzi, S. Pini, M. Saad, D.A. Chiumello, P. Santus.Helmet CPAP to treat acute hypoxemic respiratory failure in patients with COVID-19: a management strategy proposal. J Clin Med, 9 (4) ( 2020), p. 1191, DOI: 10.3390/jcm9041191
[54]
M. Jahani, S. Dokaneheifard, K. Mansouri.Hypoxia: a key feature of COVID-19 launching activation of HIF-1 and cytokine storm. J Inflamm, 17 (1) ( 2020), p. 33, DOI: 10.1186/s12950-020-00263-3
[55]
N. Vassilaki, E. Frakolaki. Virus-host interactions under hypoxia. Microb Infect, 19 (3) ( 2017), pp. 193-203, DOI: 10.1016/j.micinf.2016.10.004
[56]
R. Zhang, H. Su, X. Ma, et al.. miRNA let-7b promotes the development of hypoxic pulmonary hypertension by targeting ACE2. Am J Physiol Lung Cell Mol Physiol, 316 (3) ( 2019), pp. L547-L557, DOI: 10.1152/ajplung.00387.2018
[57]
E.V. Fernandez, K.M. Reece, A.M. Ley, et al.. Dual targeting of the androgen receptor and hypoxia-inducible factor 1α pathways synergistically inhibits castration-resistant prostate cancer cells. Mol Pharmacol, 87 (6) ( 2015), pp. 1006-1012, DOI: 10.1124/mol.114.097477
[58]
K. Nishi, T. Oda, S. Takabuchi, et al.. LPS induces hypoxia-inducible factor 1 activation in macrophage-differentiated cells in a reactive oxygen species-dependent manner. Antioxidants Redox Signal, 10 (5) ( 2008), pp. 983-996, DOI: 10.1089/ars.2007.1825
[59]
E.M. Palsson-McDermott, L.A.J. O'Neill. The Warburg effect then and now: from cancer to inflammatory diseases. Bioessays, 35 (11) ( 2013), pp. 965-973, DOI: 10.1002/bies.201300084
[60]
S. Rajasundaram.Adenosine A2A receptor signaling in the immunopathogenesis of experimental autoimmune encephalomyelitis. Front Immunol, 9 ( 2018), p. 402, DOI: 10.3389/fimmu.2018.00402
[61]
S.A. dos Santos, D.R. de Andrade Júnior.HIF-1alpha and infectious diseases: a new frontier for the development of new therapies. Rev Inst Med Trop Sao Paulo, 59 ( 2017), p. e92, DOI: 10.1590/s1678-9946201759092
[62]
G. Li, L. He, E. Zhang, et al.. Overexpression of human papillomavirus (HPV) type 16 oncoproteins promotes angiogenesis via enhancing HIF-1α and VEGF expression in non-small cell lung cancer cells. Cancer Lett, 311 (2) ( 2011), pp. 160-170, DOI: 10.1016/j.canlet.2011.07.012
[63]
A.S. Menezes, S.M. Botelho, L.R. Santos, A.L. Rezende. Acute COVID-19 syndrome predicts severe long COVID-19: an observational study. Cureus, 14 (10) ( 2022), Article e29826, DOI: 10.7759/cureus.29826
[64]
C.M. Terzic, B.J. Medina-Inojosa.Cardiovascular complications of coronavirus disease-2019. Phys Med Rehabil Clin, 34 (3) ( 2023), pp. 551-561, DOI: 10.1016/j.pmr.2023.03.003
[65]
T.J. Gluckman, N.M. Bhave, L.A. Allen, et al.. 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. J Am Coll Cardiol, 79 (17) ( 2022), pp. 1717-1756, DOI: 10.1016/j.jacc.2022.02.003. 2022
[66]
K. Bieksiene, J. Zaveckiene, K. Malakauskas, N. Vaguliene, M. Zemaitis, S. Miliauskas. Post COVID-19 organizing pneumonia: the right time to interfere. Medicina, 57 (3) ( 2021), p. 283, DOI: 10.3390/medicina57030283
[67]
P. Mehta, I.O. Rosas, M. Singer. Understanding post-COVID-19 interstitial lung disease (ILD): a new fibroinflammatory disease entity. Intensive Care Med, 48 (12) ( 2022), pp. 1803-1806, DOI: 10.1007/s00134-022-06877-w
[68]
G.M.C. Rosano, C. Vitale, M. Adamo, M. Metra. Roadmap for the management of heart failure patients during the vulnerable phase after heart failure hospitalizations: how to implement excellence in clinical practice. J Cardiovasc Med, 23 (3) ( 2022), pp. 149-156, DOI: 10.2459/JCM.0000000000001221
[69]
A. Nalbandian, K. Sehgal, A. Gupta, et al.. Post-acute COVID-19 syndrome. Nat Med, 27 (4) ( 2021), pp. 601-615, DOI: 10.1038/s41591-021-01283-z
[70]
B. Bozkurt, R. Kovacs, B. Harrington.Joint HFSA/ACC/AHA Statement addresses concerns Re: using RAAS antagonists in COVID-19. J Card Fail, 26 (5) ( 2020), p. 370, DOI: 10.1016/j.cardfail.2020.04.013
[71]
R.D. Lopes, A.V.S. Macedo, P.G.M. de Barros E Silva, et al.. Effect of discontinuing vs continuing angiotensin-converting enzyme inhibitors and angiotensin II receptor blockers on days alive and out of the hospital in patients admitted with COVID-19. JAMA, 325 (3) ( 2021), p. 254, DOI: 10.1001/jama.2020.25864
[72]
J.R. Rey, J. Caro-Codón, S.O. Rosillo, et al.. Heart failure in COVID-19 patients: prevalence, incidence and prognostic implications. Eur J Heart Fail, 22 (12) ( 2020), pp. 2205-2215, DOI: 10.1002/ejhf.1990
[73]
M. Zuin, G. Rigatelli, V. Battisti, G. Costola, L. Roncon, C. Bilato. Increased risk of acute myocardial infarction after COVID-19 recovery: a systematic review and meta-analysis. Int J Cardiol, 372 ( 2023), pp. 138-143, DOI: 10.1016/j.ijcard.2022.12.032
[74]
R.F. Rinaldo, M. Mondoni, E.M. Parazzini, et al.. Deconditioning as main mechanism of impaired exercise response in COVID-19 survivors. Eur Respir J, 58 (2) ( 2021), Article 2100870, DOI: 10.1183/13993003.00870-2021
[75]
F.A. Gaffney, J.V. Nixon, E.S. Karlsson, W. Campbell, A.B.C. Dowdey, C.G. Blomqvist.Cardiovascular deconditioning produced by 20 hours of bedrest with head-down tilt (-5°) in middle-aged healthy men. Am J Cardiol, 56 (10) ( 1985), pp. 634-638, DOI: 10.1016/0002-9149(85)91025-2
[76]
E.W. Rudofker, H. Parker, W.K. Cornwell. An exercise prescription as a novel management strategy for treatment of long COVID. JACC Case Rep, 4 (20) ( 2022), pp. 1344-1347, DOI: 10.1016/j.jaccas.2022.06.026
[77]
A. Pelliccia, B.J. Maron, A. Spataro, M.A. Proschan, P. Spirito. The upper limit of physiologic cardiac hypertrophy in highly trained elite athletes. N Engl J Med, 324 (5) ( 1991), pp. 295-301, DOI: 10.1056/NEJM199101313240504
[78]
C. Serviente, S.T. Decker, G. Layec. From heart to muscle: pathophysiological mechanisms underlying long-term physical sequelae from SARS-CoV-2 infection. J Appl Physiol, 132 (3) ( 2022), pp. 581-592, DOI: 10.1152/japplphysiol.00734.2021
[79]
T. Fukuda, M. Kurano, K. Fukumura, et al.. Cardiac rehabilitation increases exercise capacity with a reduction of oxidative stress. Korean Circ J, 43 (7) ( 2013), p. 481, DOI: 10.4070/kcj.2013.43.7.481
[80]
J.J. Manson, C. Crooks, M. Naja, et al.. COVID-19-associated hyperinflammation and escalation of patient care: a retrospective longitudinal cohort study. Lancet Rheumatol, 2 (10) ( 2020), pp. e594-e602, DOI: 10.1016/S2665-9913(20)30275-7
[81]
L. Cavigli, C. Fusi, M. Focardi, et al.. Post-acute sequelae of COVID-19: the potential role of exercise therapy in treating patients and athletes returning to play. J Clin Med, 12 (1) ( 2022), p. 288, DOI: 10.3390/jcm12010288
[82]
F. D'Ascenzi, S. Castelletti, P.E. Adami, et al.. Cardiac screening prior to return to play after SARS-CoV-2 infection: focus on the child and adolescent athlete: a clinical consensus statement of the task force for childhood health of the European association of preventive Cardiology. Eur J Prev Cardiol, 29 (16) ( 2022), pp. 2120-2124, DOI: 10.1093/eurjpc/zwac180
[83]
A. Mohr, L. Dannerbeck, T.J. Lange, et al.. Cardiopulmonary exercise pattern in patients with persistent dyspnoea after recovery from COVID-19. Multidiscip Respir Med, 16 (1) ( 2021), p. 732, DOI: 10.4081/mrm.2021.732
[84]
Y. Gao, R. Chen, Q. Geng, et al.. Cardiopulmonary exercise testing might be helpful for interpretation of impaired pulmonary function in recovered COVID-19 patients. Eur Respir J, 57 (1) ( 2021), Article 2004265, DOI: 10.1183/13993003.04265-2020
[85]
I. Singh, P. Joseph, P.M. Heerdt, et al.. Persistent exertional intolerance after COVID-19. Chest, 161 (1) ( 2022), pp. 54-63, DOI: 10.1016/j.chest.2021.08.010
[86]
H.E. Davis, L. McCorkell, J.M. Vogel, E.J. Topol.Author Correction: long COVID: major findings, mechanisms and recommendations. Nat Rev Microbiol, 21 (6) ( 2023), p. 408, DOI: 10.1038/s41579-023-00896-0
[87]
M. Parotto, S.N. Myatra, D. Munblit, A. Elhazmi, O.T. Ranzani, M.S. Herridge.Recovery after prolonged ICU treatment in patients with COVID-19. Lancet Respir Med, 9 (8) ( 2021), pp. 812-814, DOI: 10.1016/S2213-2600(21)00318-0
[88]
F. Besnier, B. Bérubé, J. Malo, et al.. Cardiopulmonary rehabilitation in long-COVID-19 patients with persistent breathlessness and fatigue: the COVID-Rehab Study. Int J Environ Res Publ Health, 19 (7) ( 2022), p. 4133, DOI: 10.3390/ijerph19074133
[89]
J.C. Sánchez-García, A. Reinoso-Cobo, B. Piqueras-Sola, et al.. Long COVID and physical therapy: a systematic review. Diseases, 11 (4) ( 2023), p. 163, DOI: 10.3390/diseases11040163
[90]
D.V. Pouliopoulou, J.C. Macdermid, E. Saunders, et al.. Rehabilitation interventions for physical capacity and quality of life in adults with post-COVID-19 condition. JAMA Netw Open, 6 (9) ( 2023), Article e2333838, DOI: 10.1001/jamanetworkopen.2023.33838
[91]
T. del Corral, R. Fabero-Garrido, G. Plaza-Manzano, C. Fernández-de-las-Peñas, M. Navarro-Santana, I. López-de-Uralde-Villanueva.Home-based respiratory muscle training on quality of life and exercise tolerance in long-term post-COVID-19: randomized controlled trial. Ann Phys Rehabil Med, 66 (1) ( 2023), Article 101709, DOI: 10.1016/j.rehab.2022.101709
[92]
J. Shang, G. Ye, K. Shi, et al.. Structural basis of receptor recognition by SARS-CoV-2. Nature, 581 (7807) ( 2020), pp. 221-224, DOI: 10.1038/s41586-020-2179-y
[93]
S. Yokota, T. Miyamae, Y. Kuroiwa, K. Nishioka.Novel Coronavirus Disease 2019 (COVID-19) and cytokine storms for more effective treatments from an inflammatory pathophysiology. J Clin Med, 10 (4) ( 2021), p. 801, DOI: 10.3390/jcm10040801
[94]
RECOVERY Collaborative Group. Tocilizumab in patients admitted to hospital with COVID-19 (RECOVERY): a randomised, controlled, open-label, platform trial. Lancet, 397 (10285) ( 2021), pp. 1637-1645, DOI: 10.1016/S0140-6736(21)00676-0
[95]
G.N. Masoud, W. Li. HIF-1α pathway: role, regulation and intervention for cancer therapy. Acta Pharm Sin B, 5 (5) ( 2015), pp. 378-389, DOI: 10.1016/j.apsb.2015.05.007
[96]
D. Tekin, A.D. Dursun, L. Xi. Hypoxia inducible factor 1 (HIF-1) and cardioprotection. Acta Pharmacol Sin, 31 (9) ( 2010), pp. 1085-1094, DOI: 10.1038/aps.2010.132
[97]
Z.O. Serebrovska, E.Y. Chong, T.V. Serebrovska, L.V. Tumanovska, L. Xi. Hypoxia, HIF-1α and COVID-19: from pathogenic factors to potential therapeutic targets. Acta Pharmacol Sin, 41 (12) ( 2020), pp. 1539-1546, DOI: 10.1038/s41401-020-00554-8
[98]
T.V. Serebrovskaya, L. Xi. Intermittent hypoxia training as non-pharmacologic therapy for cardiovascular diseases: practical analysis on methods and equipment. Exp Biol Med, 241 (15) ( 2016), pp. 1708-1723, DOI: 10.1177/1535370216657614
[99]
Y. Wang, H. Kang, X. Liu, Z. Tong. Combination of RT-qPCR testing and clinical features for diagnosis of COVID-19 facilitates management of SARS-CoV-2 outbreak. J Med Virol, 92 (6) ( 2020), pp. 538-539, DOI: 10.1002/jmv.25721
[100]
I. Gostimskaya. CRISPR-Cas9: a history of its discovery and ethical considerations of its use in genome editing. Biochemistry, 87 (8) ( 2022), pp. 777-788, DOI: 10.1134/S0006297922080090
[101]
C.A. Freije, C. Myhrvold, C.K. Boehm, et al.. Programmable inhibition and detection of RNA viruses using Cas13. Mol Cell, 76 (5) ( 2019), pp. 826-837.e11, DOI: 10.1016/j.molcel.2019.09.013
[102]
B. Berber, C. Aydin, F. Kocabas, et al.. Gene editing and RNAi approaches for COVID-19 diagnostics and therapeutics. Gene Ther, 28 (6) ( 2021), pp. 290-305, DOI: 10.1038/s41434-020-00209-7
[103]
D.H. Kim, J.J. Rossi. RNAi mechanisms and applications. Biotechniques, 44 (5) ( 2008), pp. 613-616, DOI: 10.2144/000112792
[104]
E. Olmastroni, F. Galimberti, E. Tragni, A.L. Catapano, M. Casula.Impact of COVID-19 pandemic on adherence to chronic therapies: a systematic review. Int J Environ Res Publ Health, 20 (5) ( 2023), p. 3825, DOI: 10.3390/ijerph20053825
[105]
C. Roche, A. Fisher, D. Fancourt, A. Burton.Exploring barriers and facilitators to physical activity during the COVID-19 pandemic: a qualitative study. Int J Environ Res Publ Health, 19 (15) ( 2022), p. 9169, DOI: 10.3390/ijerph19159169
[106]
K. Bouabida, B. Lebouché, M.P. Pomey. Telehealth and COVID-19 pandemic: an overview of the telehealth use, advantages, challenges, and opportunities during COVID-19 pandemic. Healthcare, 10 (11) ( 2022), p. 2293, DOI: 10.3390/healthcare10112293
[107]
B. Mandal, N. Porto, D.E. Kiss, S.H. Cho, L.S. Head. Health insurance coverage during the COVID-19 pandemic: the role of Medicaid expansion. J Consum Aff, 57 (1) ( 2023), pp. 296-319, DOI: 10.1111/joca.12500
[108]
D.M. Resurrección, E. Motrico, M. Rubio-Valera, J.A. Mora-Pardo, P. Moreno-Peral. Reasons for dropout from cardiac rehabilitation programs in women: a qualitative study. PLoS One, 13 (7) ( 2018), Article e0200636, DOI: 10.1371/journal.pone.0200636
[109]
H.J. Chuang, C.W. Lin, M.Y. Hsiao, T.G. Wang, H.W. Liang.Long COVID and rehabilitation. J Formos Med Assoc, 123 ( 2024), pp. S61-S69, DOI: 10.1016/j. jfma.2023.03.022

Accesses

Citations

14

Altmetric

Detail

Sections
Recommended

/