Lesions of the heart and parenchymatous organs in patients with COVID-19 and other acute respiratory infections

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Based on available literature, this study aimed to critically assess the effect of SARS-CoV-2 and other respiratory viruses on the heart and parenchymatous internal organs, identify their common and distinctive features, assess the frequency of cytokine storm and “post-infection” syndrome, and identify risk factors for severe systemic reaction and damage to internal organs, particularly the heart.

In the databases of MEDLINE/PubMed, eLibrary, Web of Science, CyberLeninka, and Openmedcom.ru, primary information (full-text and abstract databases) in English and Russian was searched using selected keywords from 2003 to 2023.

Acute respiratory viral infection pathogens can cause not only respiratory but also cardinal, gastroenterological, neurological, and other complications.

Acute respiratory viral infections have many similarities in their effects on parenchymal organs. The emergence of new viruses requires in-depth study, and it is important to consider both the distinctive features of the clinical picture of viral infections and the general patterns of influence on internal organs. In the medium term, patients who have COVID-19 may have complex heart damage in the form of a decrease in ventricular ejection fraction, appearance of pericardial effusion, and development of various types of focal myocardial lesions. The combined nature of damage to the heart and parenchymal organs is influenced by background diseases, nature of the course of viral infection, and features of therapy. The features of lesions of parenchymal organs and the heart after acute respiratory viral infection require further study, including their effect on the development of late complications.

Full Text

Introduction

Humanity has repeatedly faced severe pandemics, including the "Spanish flu" pandemic in 1918 caused by the H1N1 strain of influenza A virus, the "Asian flu" in 1957 caused by the H2N2 strain, the "Hong Kong flu" of 1968, the causative agent of which was the H3N2 virus, as well as the pandemic of the "new influenza A virus" 2009-2010 years, again caused by the H1N1 virus [1]. A number of respiratory infectious diseases are also known, the severity of which varies from mild malaise to the development of pneumonia and multiple organ failure. The pandemic of a new coronavirus infection in 2020-2021 caused by SARS-CoV-2 revealed the need to analyze information about the systemic impact of viral infections on the human body in order to identify common patterns of organ and system damage.
Earlier, when studying coronavirus infections, variants of the development of atypical pneumonia and severe acute respiratory syndrome (Severe Acute Respiratory Syndrome SARS in 2002 and Middle East Respiratory Syndrome MERS in 2012 [2] were described.
It seems relevant to compare the pathogenicity of SARS CoV-2 with other respiratory viruses (SARS CoV, MERS-CoV, influenza A H1N1 virus, adenovirus) with respect to the development of organ complications in these diseases, as well as the identification of common factors of unfavorable prognosis. Along with the study of the most typical manifestations of acute respiratory viral infections (ARVI), the analysis of the frequency of occurrence and clinical significance of extrapulmonary lesions is relevant.

Material and methods

This search affected 268 electronic resources in the databases MEDLINE/PubMed, eLibrary, Web of science, Cyberleninca, Оpenmedcom.ru , in English and Russian. Content analysis and search were used, according to the main keywords.
Results and discussion
The SARS CoV-2 pandemic has shown that the ability of the virus to infect several organs and systems depends both on the features of the pathogenesis of SARS and on the reaction of the host organism. ARVI pathogens can cause not only respiratory, but cardiac, gastroenterological, neurological and other complications.
The results of comparing the frequency of lesions of the main parenchymal organs in the most common ARVI are presented in Table 1.Table 1. Lesions of parenchymal organs in acute respiratory viral infections

The similarity of the course of the analyzed ARVI is to a certain extent due to the signal proinflammatory cytokine kinetics (IL-1 and IL-6, TNF, etc.). In viral infections (SARS, SARS CoV-2, MERS-CoV, influenza A H1N1 virus), the phenomenon of a "cytokine storm" is possible [32].
In severe acute respiratory viral infections and COVID 19, the role of macrophage activation syndrome (secondary hemophagocytic lymphohistiocytosis) and unregulated release of cytokines and chemokines (cytokine storm) with impaired interleukin production, T-lymphocyte function, depletion of cellular immune response and lymphopenia is undeniable in the alteration of organs and tissues. The development of virus-induced autoimmune reactions is also not excluded. Systemic damage by the virus and cytokine storm of the endothelium (microangiopathy with its damage, less often endotheliitis and vasculitis) and activation of the coagulation cascade in COVID-19 cause hypercoagulation syndrome with thrombosis and thromboembolism [33].
With the above diseases and conditions, cases of borderline and regular myocarditis are also described. Thrombohemorrhagic events, disorders of hemodynamics and water metabolism, damage to the renin-angiotensin-aldosterone system, have also been previously described by scientists with the above pathologies. Several interrelated similar pathogenetic mechanisms are involved in the development of the pathological process, leading to the development of a vicious circle: the cytopathic effect of the "aggressor" on the heart tissue, renal tissue and blood vessels, due to the expression of the APF2 receptor; the formation of a "cytokine storm" and a systemic inflammatory response leading to coagulopathy with the formation of multiple microthrombs, the development of systemic vasculitis of organs and tissues. Severe multisystem forms of COVID-19 and similar diseases, including an expanded "cytokine storm", may play a role in the instability of the coronary plaque. In viral infections, various adhesion factors of the viral agent and factors of its penetration into the organomishen interact (the role of a spike-like protein or an accessory protein, a cascade of Toll-like receptors) [34]. Prior to introduction into the cell, viruses produce microproteases 2A (inhibiting protein synthesis) and affect the protein dystrophin, which contributes to the initial development of cardiomyopathies according to a unique clinical scenario [35].
Damage to organ tissue and cells leads to the release of mitochondrial proteins (n-FP, cardiolipin, etc.) and mitochondrial DNA (mtDNA). These decay products contribute to the formation of damage-associated molecular patterns (DAMPs), which stimulate the innate immune response by activating Toll-like receptors (TLR), NOD-like receptors (NLRP) and the cGAS-STING signaling pathway. As a result, the production of pro-inflammatory cytokines, type I interferons and chemokines increases [36].
Angiotensin is a type 2 converting enzyme (ACE-2), a key cellular receptor for the SARS-CoV-2 virus. One of the recent studies has convincingly shown that pericytes (located in the walls of small blood vessels, including capillaries) of the human heart with high expression of ACE-2 can be targets for SARS-CoV-2. Damage to pericytes during viremia leads to dysfunction of capillary endothelial cells, causing dysfunction of the microcirculatory bed. Since patients with initial cardiovascular pathology, for example, with chronic heart failure, have increased expression of ACE-2 both at the level of matrix RNA and at the level of synthesis of the corresponding protein, when infected with SARS-CoV-2, they have a higher risk of heart damage with the development of a critical condition and death. This may explain the high level of severe outcomes among patients with COVID-19 and concomitant chronic diseases, primarily of the cardiovascular system. This circumstance should be taken into account when choosing treatment tactics in severe patients infected with SARS-CoV-2 [37].
Severe acute respiratory syndrome caused by the new SARS-CoV-2 coronavirus causes changes in various tissues, but the frequency of heart damage, as well as the possible consequences of this process are not exactly known. The latest scientific data with an assessment of the presence of SARS-CoV-2 in myocardial tissues during autopsy in patients who died from a new coronavirus infection COVID-19 show that the presence of SARS-CoV-2 RNA in the myocardium can be observed in 62% of cases, while a high viral load with an index of more than 1000 copies of mcg of RNA can be noted at 41.0%. At the same time, replication of the SARS-CoV-2 virus in the myocardium occurs in 13% of patients with a high viral load of more than 1000 copies of mcg of RNA. It is important to note that cytokines are most actively expressed in the myocardium of patients with the presence of SARS-CoV-2 RNA, and their highest level is naturally observed in patients with a high viral load of more than 1000 copies of mcg of RNA. At the same time, the presence of the virus in the heart tissues may not be associated with increased infiltration of mononuclear cells into the myocardium compared to the group of patients who lack SARS-CoV-2 RNA. The presence of SARS-CoV-2 in cardiac tissue does not necessarily cause an inflammatory reaction corresponding to the clinical definition of myocarditis. However, the long-term consequences of the presence of the virus in the heart tissues require further study [38].
Acute myocardial lesion in the new coronavirus infection COVID-19 is currently described as "acute cardiac injury", determined by an increase in the level of cardiac biomarkers (highly sensitive troponins) in the blood above the 99th percentile of the upper reference limit. This syndrome can develop in 20% of patients and, apparently, affects the prognosis [39-40]. The pathogenesis of acute myocardial injury is not fully understood. The diagnosis is based on clinical data, imaging results using echocardiography and MRI, as well as biomarkers of acute cardiac injury. Determining the cause of heart damage either as a result of myocardial inflammation (myocarditis or myopericarditis) or necrosis is critically important for choosing the right treatment tactics for patients, especially those in the intensive care unit.
Cases of acute heart injury directly related to localization in the myocardium of patients with severe acute respiratory syndrome caused by SARS-CoV-2 are described. In such cases, endomyocardial biopsy may show mild myocardial inflammation and the presence of viral particles in the myocardium, which indicates either the viremic phase of the infectious process or the migration of infected macrophages from the lungs [41].
In patients with acute respiratory viral infections with cardiac manifestations, confirmation of myocarditis using the Dallas criteria is usually not available (inflammatory infiltrates in the myocardium associated with myocyte degeneration and necrosis of non-ischemic origin, with positive immunohistochemical signs in the form of inflammatory infiltrate with ≥14 leukocytes 1 mm2, up to 4 monocytes per mm2 in the presence of CD 3 positive T-lymphocytes ≥7 cells in 1 mm2). The presence of acute myocarditis is evidenced by: the presence of a previous viral infection, proven clinically and laboratory data in combination with three major signs of myocardial damage: the appearance on the ECG of changes in the form of regression of the R wave of zones of violation of local contractility according to EchoCG data and an increase in the level of cardiospecific enzymes, primarily highly sensitive TnT or TnI troponins [42].
In slave S. Shi and co-authors (2020) raised the issue of the frequency and significance of myocardial damage in COVID 19. In this study, conclusions are drawn about myocardial damage to the myocardium within the framework of coronavirus infection, relying mainly on the data of markers of myocardial damage. But it is not described in the category of which clinical diagnosis myocardial damage is attributed to coronavirus infection. Considering that the mechanisms of involvement of the cardiovascular system in COVID 19 may be similar both in acute myocardial injury and in the presence of a history of cardiovascular pathology. In addition to the direct organotropic action of the pathogen, viral particles can activate the host's immune responses through various mechanisms, including the complement cascade through the lectin pathway, triggering an immune response [39]. As a result, locally formed immune complexes can play a role in further activation of the complement system and in strengthening the inflammatory response. There is evidence in the clinical literature indicating that with coronavirus, enterovirus infection, some respiratory diseases (influenza, etc.), in addition to respiratory symptoms, the effect on the cardiovascular system is summed up, which generally worsens the condition and affects the prognosis [43]. It was also found to be associated with increased capillary thrombosis, high lactate dehydrogenase and ferritin content, as well as with a moderate increase in blood clotting time, which resembles thrombotic microangiopathy, similar to that of hantavirus infection and West Nile fever [44].

SARS, MERS, and SARS CoV-2 viruses are characterized by a significant percentage of the incidence of lung, liver, and kidney damage. However, this lesion increases the reaction of the sympathoadrenal system to the fact of virus intervention, as well as the "cytokine storm" within the framework of the systemic inflammatory response and drug-induced liver damage due to the use of drugs with potential hepatotoxic effects for the treatment of infection.

In general, the incidence of lesions of various organ systems is higher in males over 40 years of age with SARS CoV-2 and over 50 years of age with MERS, suffering from hypertension, oncological diseases and having comorbid pathology. For SARS and H1N1 viruses, among the factors of a more severe course of infection, it is possible to distinguish the female sex and the status of a medical worker (probably due to the high viral load).

 

Figure. The pattern of heart damage according to magnetic resonance imaging with contrast enhancement in patients who underwent COVID-19 in the form of a Venn diagram with the allocation of the most typical clusters of signs. EF — ejection fraction; LV — left ventricle; RV — right ventricle; EC — early contrast; LC — late contrast

 

It should be noted that other viral diseases of the liver, kidneys and gastrointestinal tract contribute to the defeat of internal organs in ARVI. H1N1 viruses and adenoviruses in general are characterized by a lower frequency of internal organ damage with the exception of the lungs, however, they, like other analyzed ARVI, are characterized by a symptom similar in characteristics to LONG Covid – postinfectious asthenic syndrome. Among the risk factors contributing to its occurrence are female gender, persons with a history of anxiety or depression or the use of antidepressants, persons with extensive comorbid pathology [45, 46].

In our prospective work, MRI of the heart with contrast enhancement was used as a non-invasive reference method for detecting hidden heart damage, including myocarditis, while the median time interval from the moment of the disease to the MRI was 112.5 [75-151] days. The study was performed on an Optima MR 450 W GE Healthcare tomograph with a field strength of 1.5 T. Data was collected in synchronization mode with an ECG. To assess inflammatory myocardial damage, classical signs of myocarditis (Lake Louise Consensus Criteria) were used: a focal or global increase in the intensity of the MR signal in T2-weighted images (myocardial edema), an increase in the signal from the myocardium in T1-weighted images in the phase of early contrast enhancement (myocardial hyperemia), the presence of areas of late contrast signal enhancement in myocardium (necrosis and/or fibrosis) [47-48].

A complex pattern of heart damage after COVID-19 in the form of a Venn diagram with the selection of the most typical combinations based on tree clustering is shown in Figure 1.Figure 1. The pattern of heart damage according to MRI data with contrast enhancement in patients who underwent COVID-19 in the form of a Venn diagram with the allocation of the most typical clusters of signs. PV – ejection fraction, LV – left ventricle, LV – right ventricle, PK – early contrast, PK – late contrast.

There were no differences between patients with and without focal myocardial lesions by gender, age, type of concomitant pathology, severity of the disease, the current level of CRP, ferritin, highly sensitive troponin I and NT-pro-BNP, as well as the main parameters of ECG and echocardiography. However, in the presence of foci of PK or PK in the myocardium, hydroxychloroquine and tocilizumab were used significantly more often in the acute phase of COVID-19, but antiviral and antibacterial agents were used less often, in addition, this was associated with an increase in end-diastolic (127 ml vs 113.5 ml; p=0.0455) and end-systolic volumes (47.5 ml vs 40 ml; p=0.0205) of LV, which indicated the development of pathological remodeling.

A feature of our work was the inclusion in the study of middle-aged and older patients with a typical premorbid background, regardless of the severity and features of COVID-19 treatment. MRI results showed that postcovid syndrome is often accompanied by latent lesions of the heart of a complex nature, including foci of damage in the myocardium, pericardial effusion, LV and pancreatic dysfunction or a combination thereof. The simultaneous appearance of pancreatic and LV dysfunction, as well as foci of PK and PK, has a certain pattern and reflects the general pathogenesis of these phenomena in COVID-19 [49-53].

The results obtained are consistent with the data of other studies in which foci of myocardial damage after COVID-19 were detected with a frequency of 10-35% and even 49%, while T1 and T2 mapping allows confirming the presence of active myocarditis in 19.4–60% of such cases [54-57]. A feature of myocarditis caused by the SARS-CoV-2 virus is a noticeable macrophage infiltration, however, whether this is important for contrast delay in the myocardium requires separate study [47-50].

Ischemic myocardial injuries after COVID-19 are noted in 17-23%, while it is not clear whether their appearance depends on the severity of infection or is determined by a premorbid background [56-59].

In the recently presented consensus of the American College of Cardiology, it is proposed to use the term "myocardial involvement" or myocardial involvement in the absence of complete criteria for myocarditis, but there are signs of heart damage. This broad concept includes myocardial infarction of type I and II, multisystem inflammatory syndrome, stress cardiomyopathy, cytokine storm, acute pulmonary heart disease, exacerbation of heart failure, the debut of previously hidden heart disease [60].

Conclusion

ARVI have a number of similarities in their effect on parenchymal organs. The emergence of new viruses undoubtedly requires their further in-depth study, but it is important to take into account the similarities of the course of viral infections and their general patterns of influence on internal organs. The combination of the new COVID-19 coronavirus infection with cardiovascular diseases creates additional difficulties in diagnosis, determining priority tactics, changing the routing orders of patients with urgent conditions, and choosing therapy. The situation is complicated by a lack of information, a significant volume of daily, often contradictory, publications on these issues, and the extremely high importance of solving a number of issues for clinical practice.

The relationship of COVID-19 and other viral infections with cardiovascular diseases is determined by the following features:

• Any infectious process can provoke the development of acute and exacerbation of chronic cardiovascular diseases;
• The presence of only cardiovascular diseases is not associated with a higher risk of coronavirus infection, but it is associated with a higher risk of complications when an infection is attached;
• Elderly patients with concomitant conditions are more likely to be infected with SARS-CoV-2, especially in the presence of arterial hypertension, coronary heart disease and diabetes mellitus.

There is a more severe course and high mortality with a combination of acute respiratory viral infections, including COVID-19, and cardiovascular diseases. The mechanisms of this association are still unclear. Apparently, the important circumstances in this context are:

1) a large proportion of elderly and senile people among those with cardiovascular diseases;
2) concomitant disorders of the immune system;
3) elevated levels of ACE-2.

Damage to the cardiovascular system can be diagnosed in 40% of patients who died from COVID-19 infection, while possible mechanisms of adverse outcome may be associated with:

• ACE-2 signaling pathways involved in the cascade of heart damage (decreased expression of ACE-2 and dysregulation of the renin-angiotensin system);
• pathological systemic inflammatory response, which manifests itself as a "cytokine storm" caused by an imbalance in the response of type 1 and type 2 T helper cells, with the development of multiple organ failure and damage to the cardiovascular system;
• respiratory dysfunction and hypoxia (oxidative stress, intracellular acidosis and mitochondrial damage), leading to damage to cardiomyocytes;
• an imbalance between increased metabolic needs and a decrease in cardiac reserve;
• destabilization and rupture of atherosclerotic plaques due to virus-induced inflammation;
• the development of thrombotic complications due to the procoagulant and prothrombogenic effect of systemic inflammation;
• microvascular damage due to hypoperfusion, increased vascular permeability, angiospasm, direct damaging effect of the virus on the endothelium of the coronary arteries.

The combined nature of damage to the heart, as well as other parenchymal organs, is apparently explained by background diseases, as well as the nature of the course of infection and therapy. The features of lesions of the heart and other parenchymal organs of a person after COVID-19 in comparison with other acute respiratory infections require further study, with the identification of common patterns and a risk factor for an unfavorable prognosis.

×

About the authors

Roman A. Khokhlov

Voronezh State Medical University named after N.N. Burdenko; Voronezh Regional Clinical Consulting and Diagnostic Center

Email: visartis@yandex.ru

MD, Dr. Sci. (Med.), Assistant Professor

Russian Federation, 10, st. Studencheskaya, 394036, Voronezh; 5А Lenina Square, Voronezh, 394018

Margarita V. Yarmonova

Voronezh Regional Clinical Consulting and Diagnostic Center

Email: mv.yarmonova@mail.ru
ORCID iD: 0009-0008-1391-1993
SPIN-code: 9646-6858

cardiologist

Russian Federation, 5А Lenina Square, Voronezh, 394018

Lyudmila V. Tribuntseva

Voronezh State Medical University named after N.N. Burdenko

Author for correspondence.
Email: tribunzewa@yandex.ru
ORCID iD: 0000-0002-3617-8578
SPIN-code: 1115-1877

MD, Cand. Sci. (Med.), Associate Professor

Russian Federation, 10, st. Studencheskaya, 394036, Voronezh

References

  1. Abdelrahman Z, Li M, Wang X. Comparative review of SARS-CoV-2, SARS-CoV, MERS-CoV, and influenza A respiratory viruses. Front Immunol. 2020;11:552909. doi: 10.3389/fimmu.2020.552909
  2. The WHO MERS-CoV Research Group. State of knowledge and data gaps of Middle East Respiratory Syndrome Coronavirus (MERS-CoV) in humans. PLoS Curr. 2013;5:ecurrents.outbreaks.0bf719e352e7478f8ad85fa30127ddb8. doi: 10.1371/currents.outbreaks.0bf719e352e7478f8ad85fa30127ddb8
  3. Stadler K, Masignani V, Eickmann M, et al. SARS--beginning to understand a new virus. Nat Rev Microbiol. 2003;1(3):209–218. doi: 10.1038/nrmicro775
  4. Yin Y, Wunderink RG. MERS, SARS and other coronaviruses as causes of pneumonia. Respirology. 2018;23(2):130–137. doi: 10.1111/resp.13196
  5. Peiris JS, Yuen KY, Osterhaus AD, Stöhr K. The severe acute respiratory syndrome. N Engl J Med. 2003;349(25):2431–2441. doi: 10.1056/NEJMra032498
  6. Drapkina OM, Maev IV, Bakulin IG, et al. Interim guidelines: Diseases of the digestive organs in the context of a new coronavirus infection pandemic (COVID-19). Profilakticheskaya Meditsina. 2020;23(3-2):120–152. (In Russ.) doi: 10.17116/profmed202023032120
  7. de Wit E, van Doremalen N, Falzarano D, Munster VJ. SARS and MERS: recent insights into emerging coronaviruses. Nat Rev Microbiol. 2016;14(8):523–534. doi: 10.1038/nrmicro.2016.81
  8. Kandeel M, Ibrahim A, Fayez M, Al-Nazawi M. From SARS and MERS CoVs to SARS-CoV-2: Moving toward more biased codon usage in viral structural and nonstructural genes. J Med Virol. 2020;92(6):660–666. doi: 10.1002/jmv.25754
  9. Satija N, Lal SK. The molecular biology of SARS coronavirus. Ann N Y Acad Sci. 2007;1102(1):26–38. doi: 10.1196/annals.1408.002
  10. Giacalone M, Scheier E, Shavit I. Multisystem inflammatory syndrome in children (MIS-C): a mini-review. Int J Emerg Med. 2021;14(1):50. doi: 10.1186/s12245-021-00373-6
  11. Al-Omari A, Rabaan AA, Salih S, et al. MERS coronavirus outbreak: Implications for emerging viral infections. Diagn Microbiol Infect Dis. 2019;93(3):265–285. doi: 10.1016/j.diagmicrobio.2018.10.011
  12. Mackay IM, Arden KE. MERS coronavirus: diagnostics, epidemiology and transmission. Virol J. 2015;12:222. doi: 10.1186/s12985-015-0439-5
  13. Petrosillo N, Viceconte G, Ergonul O, et al. COVID-19, SARS and MERS: are they closely related? Clin Microbiol Infect. 2020;26(6):729–734. doi: 10.1016/j.cmi.2020.03.026
  14. Ye Q, Wang B, Mao J. The pathogenesis and treatment of the ‘Cytokine Storm’ in COVID-19. J Infect. 2020;80(6):607–613. doi: 10.1016/j.jinf.2020.03.037
  15. Letko M, Munster V. Functional assessment of cell entry and receptor usage for lineage B β-coronaviruses, including 2019-nCoV. bioRxiv. 2020:2020.01.22.915660. doi: 10.1101/2020.01.22.915660
  16. Siripanthong B, Nazarian S, Muser D, et al. Recognizing COVID-19-related myocarditis: The possible pathophysiology and proposed guideline for diagnosis and management. Heart Rhythm. 2020;17(9):1463–1471. doi: 10.1016/j.hrthm.2020.05.001
  17. Holshue ML, DeBolt C, Lindquist S, et al. First case of 2019 novel coronavirus in the United States. N Engl J Med. 2020;382(10):929–936. doi: 10.1056/NEJMoa2001191
  18. Bazhukhina IV, Klimova NV, Gaus AA, Petrova NN. The role of perfusion computed tomography as a predictor of pancreatic necrosis in acute pancreatitis. Radiology – Practice. 2022;(3):11–23. (In Russ.) doi: 10.52560/2713-0118-2022-3-11-23
  19. Platonova TA, Golubkova AA, Sklyar MS, et al. Clinical and laboratory aspects of gastrointestinal tract damage in СOVID-19. Medical almanac. 2021;(4(69)):34–41. (In Russ.)
  20. Lei P, Zhang L, Han P, et al. Liver injury in patients with COVID-19: clinical profiles, CT findings, the correlation of the severity with liver injury. Hepatol Int. 2020;14(5):733–742. doi: 10.1007/s12072-020-10087-1
  21. Liu Q, Shi Y, Cai J, et al. Pathological changes in the lungs and lymphatic organs of 12 COVID-19 autopsy cases. Natl Sci Rev. 2020;7(12):1868–1878. doi: 10.1093/nsr/nwaa247
  22. Chen YT, Shao SC, Hsu CK, et al. Incidence of acute kidney injury in COVID-19 infection: a systematic review and meta-analysis. Crit Care. 2020;24(1):346. doi: 10.1186/s13054-020-03009-y
  23. Townsend L, Dyer AH, Jones K, et al. Persistent fatigue following SARS-CoV-2 infection is common and independent of severity of initial infection. PLoS One. 2020;15(11):e0240784. doi: 10.1371/journal.pone.0240784
  24. Yong SJ. Long COVID or post-COVID-19 syndrome: putative pathophysiology, risk factors, and treatments. Infect Dis (Lond). 2021;53(10):737–754. doi: 10.1080/23744235.2021.1924397
  25. Zhang L, Zhang X, Ma Q, et al. Transcriptomics and proteomics in the study of H1N1 2009. Genomics Proteomics Bioinformatics. 2010;8(3):139–144. doi: 10.1016/S1672-0229(10)60016-2
  26. Harish MM, Ruhatiya RS. Influenza H1N1 infection in immunocompromised host: a concise review. Lung India. 2019;36(4):330–336. doi: 10.4103/lungindia.lungindia_464_18
  27. Michaelis M, Doerr HW, Cinatl J Jr. An influenza A H1N1 virus revival — pandemic H1N1/09 virus. Infection. 2009;37(5):381–389. doi: 10.1007/s15010-009-9181-5
  28. Komine-Aizawa S, Suzaki A, Trinh QD, et al. H1N1/09 influenza A virus infection of immortalized first trimester human trophoblast cell lines. Am J Reprod Immunol. 2012;68(3):226–232. doi: 10.1111/j.1600-0897.2012.01172.x
  29. Mjid M, Cherif J, Toujani S, et al. Infuenzae A (H1N1): about 189 cases. Tunis Med. 2014;92(12):748–751. (In French)
  30. Golokhvastova NO. Peculiarities of present-day morbidity of influenza A (H1N1 swl). Klin Med (Mosk). 2012;90(6):18–25. (In Russ.)
  31. Bearman GM, Shankaran S, Elam K. Treatment of severe cases of pandemic (H1N1) 2009 influenza: review of antivirals and adjuvant therapy. Recent Pat Antiinfect Drug Discov. 2010;5(2):152–156. doi: 10.2174/157489110791233513
  32. Kelley N, Jeltema D, Duan Y, et al. The NLRP3 inflammasome: an overview of mechanisms of activation and regulation. Int J Mol Sci. 2019;20(13):3328. doi: 10.3390/ijms2013328
  33. Zayratyants OV, Samsonova MV, Cherniaev AL, et al. COVID-19 pathology: experience of 2000 autopsies. Russian Journal of Forensic Medicine. 2020;6(4):10–23. (In Russ.) doi: 10.19048/fm340
  34. Rodriguez-Morales AJ, Cardona-Ospina JA, Gutiérrez-Ocampo E, et al. Clinical, laboratory and imaging features of COVID-19: A systematic review and meta-analysis. Travel Med Infect Dis. 2020;34:101623. doi: 10.1016/j.tmaid.2020.101623
  35. Rudroff T, Fietsam AC, Deters JR, et al. Post-COVID-19 fatigue: potential contributing factors. Brain Sci. 2020;10(12):1012. doi: 10.3390/brainsci10121012
  36. Mohanty A, Tiwari-Pandey R, Pandey NR. Mitochondria: the indispensable players in innate immunity and guardians of the inflammatory response. J Cell Commun Signal. 2019;13(3):303–318. doi: 10.1007/s12079-019-00507-9
  37. Mehandru S, Merad M. Pathological sequelae of long-haul COVID. Nat Immunol. 2022;23(2):194–202. doi: 10.1038/s41590-021-01104-y
  38. Delabranche X, Helms J, Meziani F. Immunohaemostasis: a new view on haemostasis during sepsis. Ann Intensive Care. 2017;7(1):117. doi: 10.1186/s13613-017-0339-5
  39. Cao B, Wang Y, Wen D, et al. A trial of lopinavir-ritonavir in adults hospitalized with severe COVID-19. N Engl J Med. 2020;382(19):1787–1799. doi: 10.1056/NEJMoa2001282
  40. Zhang C, Wu Z, Li JW, et al. The cytokine release syndrome (CRS) of severe COVID-19 and Interleukin-6 receptor (IL-6R) antagonist tocilizumab may be the key to reduce the mortality. Int J Antimicrob Agents. 2020;55(5):105954. doi: 10.1016/j.ijantimicag.2020.105954
  41. Xu X, Han M, Li T, et al. Effective treatment of severe COVID-19 patients with tocilizumab. Proc Natl Acad Sci USA. 2020;117(20):10970–10975. doi: 10.1073/pnas.2005615117
  42. Kostiuk SA, Simirski VV, Gorbich YL, et al. Cytokine storm at COVID-19. Mezhdunarodnye obzory: klinicheskaya praktika i zdorov’e. 2021;(1):41–52. (In Russ.)
  43. Jose RJ, Manuel A. COVID-19 cytokine storm: the interplay between inflammation and coagulation. Lancet Respir Med. 2020;8(6):e46–e47. doi: 10.1016/S2213-2600(20)30216-2
  44. Amirov NB, Davletshina EhI, Vasil’eva AG, Fatykhov RG. Postcovid syndrome: multisystem “deficits”. The Bulletin of Contemporary Clinical Medicine. 2021;14(6):94–104. (In Russ.) doi: 10.20969/VSKM.2021.14(6).94-104
  45. Nguyen JL, Yang W, Ito K, et al. Seasonal influenza infections and cardiovascular disease mortality. JAMA Cardiol. 2016;1(3):274–281. doi: 10.1001/jamacardio.2016.0433
  46. Campbell CM, Kahwash R. Will complement inhibition be the new target in treating COVID-19 related systemic thrombosis? Circulation. 2020;141(22):1739–1741. doi: 10.1161/CIRCULATIONAHA.120.047419
  47. Carod-Artal FJ. Post-COVID-19 syndrome: epidemiology, diagnostic criteria and pathogenic mechanisms involved. Rev Neurol. 2021;72(11):384–396. doi: 10.33588/rn.7211.2021230
  48. Tulu TW, Wan TK, Chan CL, et al. Machine learning-based prediction of COVID-19 mortality using immunological and metabolic biomarkers. BMC Digit Health. 2023;1(1):6. doi: 10.1186/s44247-022-00001-0
  49. 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(7):802–810. doi: 10.1001/jamacardio.2020.0950
  50. Gluckman TJ, Bhave NM, Allen LA, et al. 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;79:1717–1756. doi: 10.1016/j.jacc.2022.02.003
  51. Khokhlov RA, Yarmonova MV, Tribuntseva LV, Prozorova GG. Features of myocardial injuries in patients with postcovid syndrome. Nauchno-meditsinskii vestnik Tsentral’nogo Chernozem’ya. 2022;(88):43–50. (In Russ.)
  52. Petersen SE, Khanji MY, Plein S, et al. European Association of Cardiovascular Imaging expert consensus paper: a comprehensive review of cardiovascular magnetic resonance normal values of cardiac chamber size and aortic root in adults and recommendations for grading severity. Eur Heart J Cardiovasc Imaging. 2019;20(12):1321–1331. doi: 10.1093/ehjci/jez232
  53. Basso C, Leone O, Rizzo S, et al. Pathological features of COVID-19-associated myocardial injury: a multicentre cardiovascular pathology study. Eur Heart J. 2020;41(39):3827–3835. doi: 10.1093/eurheartj/ehaa664
  54. Kogan EA, Berezovskiy YS, Blagova OV, et al. Miocarditis in patients with COVID-19 confirmed by immunohistochemical. Kardiologiia. 2020;60(7):4–10. (In Russ.) doi: 10.18087/cardio.2020.7.n1209
  55. Hendren NS, Drazner MH, Bozkurt B, Cooper LT Jr. Description and proposed management of the acute COVID-19 cardiovascular syndrome. Circulation. 2020;141(23):1903–1914. doi: 10.1161/CIRCULATIONAHA.120.047349
  56. Peretto G, Villatore A, Rizzo S, et al. The spectrum of COVID-19-associated myocarditis: a patient-tailored multidisciplinary approach. J Clin Med. 2021;10(9):1974. doi: 10.3390/jcm10091974
  57. Blagova OV, Kogan EA, Lutokhina YA, et al. Subacute and chronic post-covid myoendocarditis: clinical presentation, role of coronavirus persistence and autoimmune mechanisms. Kardiologiia. 2021;61(6):11–27. doi: 10.18087/cardio.2021.6.n1659
  58. Huang L, Zhao P, Tang D, et al. cardiac involvement in patients recovered from COVID-2019 identified using magnetic resonance imaging. JACC Cardiovasc Imaging. 2020;13(11):2330–2339. doi: 10.1016/j.jcmg.2020.05.004
  59. Hamming I, Timens W, Bulthuis ML, et al. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol. 2004;203(2):631–637. doi: 10.1002/path.1570
  60. Khokhlov L, Khokhlov R, Lipovka S, et al. Cardiac injury described by contrast-enhanced cardiac magnetic resonance imaging in patients recovered from COVID-19. J Am Coll Cardiol. 2022;79(9):2100. doi: 10.1016/S0735-1097(22)03091-1

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Figure. The pattern of heart damage according to magnetic resonance imaging with contrast enhancement in patients who underwent COVID-19 in the form of a Venn diagram with the allocation of the most typical clusters of signs. EF — ejection fraction; LV — left ventricle; RV — right ventricle; EC — early contrast; LC — late contrast

Download (236KB)
Indexing metadata

Copyright (c) 2023 Eco-Vector


СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 70763 от 21.08.2017 г.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies