Microbiota and Myopericarditis: History
Please note this is an old version of this entry, which may differ significantly from the current revision.
Contributor:

Myopericarditis is an inflammatory heart condition involving the pericardium and myocardium. It can lead to heart failure, dilated cardiomyopathy, arrhythmia and sudden death. Its pathogenesis is mainly mediated by viral infections but also can be induced by bacterial infections, toxic substances and immune mediated disorders. 

  • microbiota
  • myocarditis
  • COVID-19
  • emergency department

1. Introduction: Microbiota and the “Heart–Gut Axis”

The growing interest in the study of the human microbiota has led to the evidence that many organs, that were once supposed to be sterile, also host their resident gut microbial communities. Interestingly, microorganisms residing in different body districts are not compartmentalized but crosstalk, through to the release of endotoxins and metabolites, that can then reach other microbial populations through the bloodstream [1]. The microbiota is the group of microbe populations living in the human body, and it includes bacteria, archaea, and viruses [1]. The gut microbiota is made up of the largest number of microbes, consisting of over one thousand resident microorganisms. Among bacteria, the main phyla are Firmicutes, Proteobacteria, and Bacteroidetes. While obtaining their habitat and nourishment from the host, these microbes protect the host from other pathogens, preventing infections. Indeed, their interaction with the intestinal surface, which constitutes the microbial niche, works as a physical barrier, increases competition for nutrients, helps produce antimicrobial peptides, and modulates immune cell function both in a pro- and anti-inflammatory fashion. All these effects have an impact on the immune system and consequently affect the susceptibility and the clinical course of many diseases.
Gut dysbiosis consists of an imbalance in the composition of the microbiota. It can lead to cardiovascular diseases [2][3]. At the same time, the presence of cardiovascular disorders can be responsible for gut dysbiosis. In fact, when cardiovascular function is impaired, the blood supply of the gut is not sufficient to maintain a health gut barrier, thus promoting a “leaky gut” situation [4].
More specifically, the “gut–heart axis” relies both on metabolism-dependent and metabolism-independent processes. In metabolism-dependent pathways, the gut microbiota acts like an endocrine organ that generates bioactive metabolites, including the trimethylamine/trimethylamine N-oxide (TMAO), short-chain fatty acids (SCFA), and primary and secondary bile acids (BA). In metabolism-independent mechanisms, impaired heart function contributes to splanchnic circulation congestion, bowel wall edema, and altered intestinal barrier, resulting in bacterial translocation, passage of bacterial products in the bloodstream, and subsequent pro-inflammatory state. Besides negatively influencing the function of many other organs, these changes may also worsen the heart function itself, in a vicious circle [2].
There is evidence of the role of the microbiota in atherosclerotic disease, coronary artery disease, and myocardial infarction pathogenesis. In particular, the atherosclerotic plaque contains DNA of the oral and the gut bacteria, and people with unstable plaques present reduced levels of anti-inflammatory peptides producing bacteria in the stool [5]. Moreover, high levels of TMAO have been associated with vulnerable coronary plaque, plaque rupture, and long-term risks of incident cardiovascular events in patients with acute coronary syndrome [6].
In the light of the described evidence, the modulation of microbial gut communities is an emergent topic to offer therapeutic strategies in heart disease. For example, some authors reported that—in animal models—the administration of antibiotics or probiotics reduces the extension of myocardial infarction size [7][8]. In an experimental study conducted on rats with coronary artery disease, the administration of the probiotic Lactobacillus rhamnosus GR-1 for 6 weeks significantly improved the systolic and diastolic function of left ventricle, with benefits postinfarction heart remodeling and heart failure [8]. This probiotic was chosen owing to its ability to modulate the immune system via the gut, thus confirming the strict communication between gut and heart, through immune-mediated mechanisms [8]. In addition, this Lactobacillus was proved to contribute positively to the cardiac metabolism profile, preserving the cardiac cells taurine content [8]. Taurine is an amino acid abundantly expressed in the heart, with a role in heart failure and ventricular function. In the same way, Lactobacillus rhamnosus GR-1 promotes gut health and reduces the concentration of some adipokines as leptin, providing protective effects on cardiac tissue [8].
Similar results were obtained with the use of a probiotic juice composed Lactobacilli (i.e., Lactobacillus Plantarum) and Bifidobacterium (i.e., Bifidobacterium Lactis) that also decreased the levels of leptin achieving the same benefits in terms of myocardial protection [7].
The administration of antibiotics in a study conducted on rats with coronary artery disease was demonstrated to have a protective effect on cardiac cells, too [7]. In fact, the treatment with vancomycin reduced the levels of the cytokine leptin with favorable effects on cardiac cells. Moreover, the antibiotic vancomycin given orally with water in these animals was tested to be effective in achieving cardio-protection. The same antibiotic introduced directly into the coronary circulation did not achieve the same result. Authors hypothesize that the intravenous administration did not modulate the gut microbiota, differently from the orally administration that reached the intestine [7][8]. This underlines that there is a link between gut microbiota and cardiovascular disease with the possibility of gut microbiota to have an effect on cardiac protection. Moreover, the protective cardiac effect obtained after two days of oral therapy ended three days after stopping the treatment and more studies are needed to explore this issue [7].

2. Microbiota and COVID-19

In the process of viral invasion, the intestinal microbiota plays a key role, acting as a barrier, interacting directly or indirectly with the virus, and stimulating the innate and adaptive immune responses. Viral infections also have the potential of changing the composition of the gut microbiota [9]. Indeed, during COVID-19, modifications in microbiota composition have been reported [10][11][12][13]. Patients with COVID-19 had a higher number of opportunistic pathogens and depletion of beneficial commensals. On the one hand, the baseline abundance of some pro-inflammatory bacteria such as coprobacilli and Clostridiodes was higher and correlated with a more severe disease course. On the other hand, anti-inflammatory bacteria like Faecalibacterium prausnitzii, Eubacterium rectale and bifidobacteria were underrepresented. Interestingly, some bacteroides (B. dorei, B. thetaiotaomicron, B. massiliensis, and B. ovatus) downregulate the expression of angiotensin-converting enzyme 2 (ACE2), reducing the possibility of virus-entry thus causing a lower SARS-CoV-2 viral load in fecal samples of patients [11][12][13].
Liu et al. studied the effect of fecal microbiota transplantation in 11 patients who recovered from COVID-19 and who had suffered with gastrointestinal symptoms, gut dysbiosis and alteration of their immune status. Fecal microbiota transplantation restored gut microbiota and alleviated gastrointestinal disorders, but also had an impact on the immune system as demonstrated by changes in the peripheral lymphocyte subset [14]. In addition, there was also an increase in Bifidobacterium and Faecalibacterium and restored Actinobacteria and Proteobacteria. The modulation of gut microbiota was also proven to reduce COVID-19 disease severity, with beneficial effects on gastrointestinal symptoms, too [14]. Additionally, other study groups are investigating the effects of gut microbiota modulation during COVID-19 infection. In particular, studies are focusing on the effects of microbiota in modulating the immune system of the host, particularly in terms of progression of cytokine storm. It is well known that gut microbiota strictly interacts with host immune system. Their relationship is complex and dynamic. Factors such as viral infections can modify this balance, triggering inflammatory and immune diseases [12]. However, many studies focusing on the interaction between immunity and microbiota have tried to sequence and characterize the microbiome’s profile and to investigate on gut–microbiota modulators [11][12][13][14]. Another aspect that has been investigated is the role of KB109, a synthetic peptide, that can act as a microbiota modulator. In two trials it is currently being investigated whether or not it could significantly and positively impact microbiota composition, as a positive effect of COVID-19 disease [15][16][17].

3. Inflammatory Cardiomyopathies and COVID-19

The first reports in scientific literature regarding cardiac involvement during SARS-CoV-2 infection go back to the first months of the pandemic outbreak.
Many authors have described cases of patients with COVID-19 and inflammatory cardiomyopathies, mostly myocarditis [18][19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35] but also pericarditis [36][37][38][39][40][41]. In some cases, the cardiac disease was the first manifestation of the viral infection [19][27][37]. In other patients it was a life-threatening early complication, [22][23][29][36][42], or a fatal one [18]. Moreover, it could clinically display after infection recovery [28][30][33][35][43], or some-times remain subclinical, being detected only after cardiac imaging taking place for other reasons [44]. Manifestation could be cardiac tamponade or constrictive pericarditis, overall varying widely.
Acute myocardial dysfunction during the early course of COVID-19 has been retrospectively reported in 16–36% of patients [45][46]. While the etiology is unclear, it has been suggested that cardiac damage in COVID-19 could be attributed to stress-induced cardiomyopathy and immunological and microvascular damage [47].
The virus can indeed directly infect cardiac cells, entering in the endothelial blood vessels and activating immune response with endothelitis. Moreover, it can dysregulate hormonal pathways and activate proinflammatory responses with the release of many cytokines and the involvement of neutrophils, macrophages, platelets, and lymphocytes, thus provoking a prothrombotic state and a predisposition for clotting. This can happen both in the cardiac micro- and macro-vessels, with potentially many complications [47].
Moreover, it can dysregulate hormonal pathways and activate proinflammatory responses, with the release of many cytokines and the involvement of neutrophils, macrophages, platelets, and lymphocytes, thus provoking a prothrombotic state and a predisposition for clotting. This can happen in the cardiac micro and macrovessels. There are many different possible consequences, which range from the above discussed myocarditis and pericarditis, but also sudden arrythmias, heart failure and cor pulmonaris, plaque rupture. Another manifestation, closely associated with stress-induced mechanisms, is Takotsubo syndrome [47].
Post-mortem examination of hearts revealed potentially COVID-19-related cardio-vascular histopathologic findings, such as macro or microvascular thrombi, inflammation, and presence of intraluminal megakaryocytes. Even if these manifestations have been reported in almost half of autopsies (47.8%), functionally significant myocarditis was identified in only 2% of all cases [48]. Interestingly, when analyzing myocardial biopsies of patients with myocarditis/myopericarditis, no evidence of intracellular virus was reported [49]. Yet, some authors reported the presence of SARS-CoV-2 mRNA in the endomyocardial biopsies of patients with clinically suspected myocarditis, both testing positive [50] or negative for COVID-19 by nasopharyngeal swab [51]. SARS-CoV-2 particles were found in the cardiac macrophages or in the endothelial cells [52] but not directly in cardiomyocytes; some authors have thus suggested that the cardiovascular damage was caused by overall immune activation, rather than by direct viral induced damage [53].
The above discussed evidence has contributed to identifying and describing the “acute COVID-19 cardiovascular syndrome” (ACoVCS) in adults [54]. Yet, even though it has been identified as a clinical entity, its pathogenesis still remains largely unknown. Molecular mimicry and endothelial dysfunction have been hypothesized, but more studies are needed to confirm these results [49].
Even if our review focuses on adult patients, it is interesting to note that the ACoVCS presents some similarities with the “multisystem inflammatory syndrome in children” (MIS-C) described by Most, that has been reported in children with SARS-CoV-2 infection [54]. At a cardiac level, the MIS-C can present itself with coronary dilatation, which resembles Kawasaki disease [53][54]. Other manifestations can be elevated troponin, cardiogenic shock, and reduced biventricular function. In this study, all children tested negative for SARS-CoV-2 by polymerase chain reaction (PCR) test, but they also had specific IgG antibodies. The authors thus concluded that MIS-C could depend on a post-infectious inflammatory state that occurs several weeks after a primary infection [54].
There is much more evidence on the association between COVID-19 and cardiovascular complications, such as myocarditis, pericarditis, fulminant myocarditis with arrhythmias, as described above, but there is a gap of knowledge in understanding the different pathogenic mechanisms [55]. Fox et al. analyzed myocardial biopsies of COVID-19 patients with myocarditis and found an increased number of CD68 + cells (that indicate monocyte/macrophage lineage), compared to myocarditis which are not associated to COVID-19 infection [56]. Similar observations have been reported by other authors as well [50]. The significance of these data has not been clarified yet and the possible association with prognosis and mortality is unclear. Lethal complications of myocarditis (such as end stage heart failure, cardiogenic shock, etc.) have also been observed in patients with COVID-19 infection [49]. Sawalha et al. noticed that cardiac tamponade was present in 20% of echocardiograms in patients with COVID-19 infection. Moreover, patients who died usually also had a serious acute respiratory distress syndrome as well [57].

This entry is adapted from the peer-reviewed paper 10.3390/biomedicines9091234

References

  1. Cicchinelli, S.; Nuzzo, E.; Piccioni, A.; Candelli, M.; Covino, M.; Ojetti, V.; Ianiro, G.; Cammarota, G. COVID-19 and fecal microbiota transplantation: Limitations and potentialities are two sides of the same coin. Microb. Health Dis. 2021, 3, e444.
  2. Tang, W.W.; Kitai, T.; Hazen, S.L. Gut Microbiota in Cardiovascular Health and Disease. Circ. Res. 2017, 120, 1183–1196.
  3. Wang, Z.; Zhao, Y. Gut microbiota derived metabolites in cardiovascular health and disease. Protein Cell 2018, 9, 416–431.
  4. Hu, X.-F.; Zhang, W.-Y.; Wen, Q.; Chen, W.-J.; Wang, Z.-M.; Chen, J.; Zhu, F.; Liu, K.; Cheng, L.-X.; Yang, J.; et al. Fecal microbiota transplantation alleviates myocardial damage in myocarditis by restoring the microbiota composition. Pharmacol. Res. 2019, 139, 412–421.
  5. Koren, O.; Spor, A.; Felin, J.; Fak, F.; Stombaugh, J.; Tremaroli, V.; Behre, C.J.; Knight, R.; Fagerberg, B.; Ley, R.E.; et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc. Natl. Acad. Sci. USA 2011, 108, 4592–4598.
  6. Li, X.S.; Obeid, S.; Klingenberg, R.; Gencer, B.; Mach, F.; Räber, L.; Windecker, S.; Rodondi, N.; Nanchen, D.; Muller, O.; et al. Gut microbiota-dependent trimethylamine N-oxide in acute coronary syndromes: A prognostic marker for incident cardiovascular events beyond traditional risk factors. Eur. Heart J. 2017, 38, 814–824.
  7. Lam, V.; Su, J.; Koprowski, S.; Hsu, A.; Tweddell, J.S.; Rafiee, P.; Gross, G.J.; Salzman, N.H.; Baker, J.E. Intestinal microbiota determine severity of myocardial infarction in rats. FASEB J. 2012, 26, 1727–1735.
  8. Gan, X.T.; Ettinger, G.; Huang, C.X.; Burton, J.P.; Haist, J.V.; Rajapurohitam, V.; Sidaway, J.E.; Martin, G.; Gloor, G.B.; Swann, J.R.; et al. Probiotic Administration Attenuates Myocardial Hypertrophy and Heart Failure After Myocardial Infarction in the Rat. Circ. Heart Fail. 2014, 7, 491–499.
  9. Yang, M.; Yang, Y.; He, Q.; Zhu, P.; Liu, M.; Xu, J.; Zhao, M. Intestinal Microbiota—A Promising Target for Antiviral Therapy? Front. Immunol. 2021, 12, 676232.
  10. Ma, S.; Zhang, F.; Zhou, F.; Li, H.; Ge, W.; Gan, R.; Nie, H.; Li, B.; Wang, Y.; Wu, M.; et al. Metagenomic analysis reveals oropharyngeal microbiota alterations in patients with COVID-19. Signal Transduct. Target. Ther. 2021, 6, 1–11.
  11. Zuo, T.; Zhang, F.; Lui, G.C.; Yeoh, Y.K.; Li, A.Y.; Zhan, H.; Wan, Y.; Chung, A.C.; Cheung, C.P.; Chen, N.; et al. Alterations in Gut Microbiota of Patients With COVID-19 During Time of Hospitalization. Gastroenterology 2020, 159, 944–955.e8.
  12. Yeoh, Y.K.; Zuo, T.; Lui, G.C.-Y.; Zhang, F.; Liu, Q.; Li, A.Y.; Chung, A.C.; Cheung, C.P.; Tso, E.Y.; Fung, K.S.; et al. Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19. Gut 2021, 70, 698–706.
  13. Zuo, T.; Liu, Q.; Zhang, F.; Lui, G.C.-Y.; Tso, E.Y.; Yeoh, Y.K.; Chen, Z.; Boon, S.S.; Chan, F.K.; Chan, P.K.; et al. Depicting SARS-CoV-2 faecal viral activity in association with gut microbiota composition in patients with COVID-19. Gut 2020, 70, 276–284.
  14. Liu, F.; Ye, S.; Zhu, X.; He, X.; Wang, S.; Li, Y.; Lin, J.; Wang, J.; Lin, Y.; Ren, X.; et al. Gastrointestinal disturbance and effect of fecal microbiota transplantation in discharged COVID-19 patients. J. Med. Case Rep. 2021, 15, 1–9.
  15. ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US). 2000 Feb 29. Identifier NCT04486482, A Clinical Study to Assess the Physiologic Effects of KB109 in Patients with COVID-19 on Gut Microbiota Structure and Function. 31 August 2020. Available online: https://clinicaltrials.gov/show/NCT04486482 (accessed on 23 July 2021).
  16. ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US). 2000 Feb 29. Identifier NCT04824222, the Impact of Fecal Microbiota Transplantation as an Immunomodulation on the Risk Reduction of COVID-19 Disease Progression with Escalating Cytokine Storm and Inflammatory Parameters. 30 April 2021. Available online: https://clinicaltrials.gov/show/NCT04824222 (accessed on 17 July 2021).
  17. Haran, J.P.; Pinero, J.C.; Zheng, Y.; Palma, N.A.; Wingertzahn, M. Virtualized clinical studies to assess the natural history and impact of gut microbiome modulation in non-hospitalized patients with mild to moderate COVID-19 a randomized, open-label, prospective study with a parallel group study evaluating the physiologic effects of KB109 on gut microbiota structure and function: A structured summary of a study protocol for a randomized controlled study. Trials 2021, 22, 1–5.
  18. Auer, J.; Neuhierl, F.; Hetzmann, Z. COVID-19-related fatal myocarditis in a 42-year-old female patient. Cardiol. J. 2020, 27, 642–643.
  19. Beşler, M.S.; Arslan, H. Acute myocarditis associated with COVID-19 infection. Am. J. Emerg. Med. 2020, 38, 2489.e1–2489.e2.
  20. Lam, M.C.; Villena, A.D.L.F.; Hernández, A.H.; de Yébenes, M.G.; Alemañ, G.B. Cardiac magnetic resonance characterization of COVID-19 myocarditis. Rev. Esp. Cardiol. 2020, 73, 863–864.
  21. De Vita, S.; Ippolito, S.; Caracciolo, M.M.; Barosi, A. Peripartum cardiomyopathy in a COVID-19-infected woman: Differential diagnosis with acute myocarditis—A case report from a Hub Institution during the COVID-19 outbreak. Echocardiography 2020, 37, 1673–1677.
  22. Doyen, D.; Moceri, P.; Ducreux, D.; Dellamonica, J. Myocarditis in a patient with COVID-19: A cause of raised troponin and ECG changes. Lancet 2020, 395, 1516.
  23. Irabien-Ortiz, Á.; Carreras-Mora, J.; Sionis, A.; Pàmies, J.; Montiel, J.; Tauron, M. Fulminant myocarditis due to COVID-19. Rev. Esp. Cardiol. 2020, 73, 503–504.
  24. Jain, A.; Deval, N.; Paul, L. A recovered case of COVID-19 myocarditis treated with IV immunoglobulin. Chest 2020, 158, A281.
  25. Kim, I.-C.; Kim, J.Y.; Kim, H.A.; Han, S. COVID-19-related myocarditis in a 21-year-old female patient. Eur. Heart J. 2020, 41, 1859.
  26. Luetkens, J.A.; Isaak, A.; Zimmer, S.; Nattermann, J.; Sprinkart, A.M.; Boesecke, C.; Rieke, G.J.; Zachoval, C.; Heine, A.; Velten, M.; et al. Diffuse Myocardial Inflammation in COVID-19 Associated Myocarditis Detected by Multiparametric Cardiac Magnetic Resonance Imaging. Circ. Cardiovasc. Imaging 2020, 13, e010897.
  27. Paul, J.-F.; Charles, P.; Richaud, C.; Caussin, C.; Diakov, C. Myocarditis revealing COVID-19 infection in a young patient. Eur. Heart J. Cardiovasc. Imaging 2020, 21, 776.
  28. Spano, G.; Fischer, K.; Maillat, C.; Vicario, G.; Huber, A.T.; Gräni, C. Delayed isolated peri-myocarditis in a Covid-19 patient with respiratory symptoms but without lung involvement. Int. J. Cardiovasc. Imaging 2020, 36, 2279–2280.
  29. Zeng, J.-H.; Liu, Y.-X.; Yuan, J.; Wang, F.-X.; Wu, W.-B.; Li, J.-X.; Wang, L.-F.; Gao, H.; Wang, Y.; Dong, C.-F.; et al. First case of COVID-19 complicated with fulminant myocarditis: A case report and insights. Infection 2020, 48, 773–777.
  30. Bajaj, R.; Sinclair, H.C.; Patel, K.; Low, B.; Pericao, A.; Manisty, C.; Guttmann, O.; Zemrak, F.; Miller, O.; Longhi, P.; et al. Delayed-onset myocarditis following COVID-19. Lancet Respir. Med. 2021, 9, e32–e34.
  31. Dahl, E.H.; Mosevoll, K.A.; Cramariuc, D.; Vedeler, C.A.; Blomberg, B. COVID-19 myocarditis and postinfection Bell’s palsy. BMJ Case Rep. 2021, 14, e240095.
  32. Laganà, N.; Cei, M.; Evangelista, I.; Cerutti, S.; Colombo, A.; Conte, L.; Mormina, E.; Rotiroti, G.; Versace, A.G.; Porta, C.; et al. Suspected myocarditis in patients with COVID-19. Medicine 2021, 100, e24552.
  33. Martínez, A.O.; González-Razo, V.T.; Navarro-Sánchez, V.; Meiriño, C.A.S.; Ahumada-Ayala, M. SARS-CoV-2-Related Subacute Thyroiditis, Myocarditis, and Hepatitis After Full Resolution of COVID-19 Serum Markers. Am. J. Case Rep. 2021, 22, e932321.
  34. Sheikh, A.B.; Javed, N.; Sheikh, A.A.E.; Upadhyay, S.; Shekhar, R. Diabetes Insipidus and Concomitant Myocarditis: A Late Sequelae of COVID-19 Infection. J. Investig. Med. High Impact Case Rep. 2021, 9, 2324709621999954.
  35. Volis, I.; Livneh, I.; Hussein, K.; Raz-Pasteur, A. COVID-19-Associated Suspected Myocarditis as the Etiology for Recurrent and Protracted Fever in an Otherwise Healthy Adult. Am. J. Med. Sci. 2021, 361, 522–525.
  36. Hua, A.; O’Gallagher, K.; Sado, D.; Byrne, J. Life-threatening cardiac tamponade complicating myo-pericarditis in COVID-19. Eur. Heart J. 2020, 41, 2130.
  37. Kumar, R.; Kumar, J.; Daly, C.; Edroos, S.A. Acute pericarditis as a primary presentation of COVID-19. BMJ Case Rep. 2020, 13, e237617.
  38. Ortiz-Martínez, Y.; Cabeza-Ruiz, L.D.; Vásquez-Lozano, S.H.; Villamil-Gómez, W.E.; Rodriguez-Morales, A.J. Pericarditis in a young internal medicine resident with COVID-19 in Colombia. Travel. Med. Infect. Dis. 2020, 37, 101863.
  39. Tung-Chen, Y. Acute pericarditis due to COVID-19 infection: An underdiagnosed disease? Med. Clín. 2020, 155, 44–45.
  40. Pérez, J.S.; Girbal, L.A.; Caravaca-Fontán, F.; Polanco, N.; Prieto, Á.S.; Andrés, A. Pericarditis secondary to COVID-19 infection in a kidney transplant recipient. Nefrología 2021, 41, 349–352.
  41. Beckerman, J.K.; Alarfaj, M.; Tracy, C.M.; Faiwiszewski, A.D.; Choi, A.D. Coronavirus disease 2019 (COVID-19)-associated constrictive pericarditis. BMJ Case Rep. 2021, 14, e242018.
  42. Salamanca, J.; Díez-Villanueva, P.; Martínez, P.; Cecconi, A.; de Marcos, B.G.; Reyes, G.; Salas, C.; Segovia, J.; Jiménez-Borreguero, L.J.; Alfonso, F. COVID-19 “Fulminant Myocarditis” Successfully Treated with Temporary Mechanical Circulatory Support. JACC Cardiovasc. Imaging 2020, 13, 2457–2459.
  43. Sardari, A.; Tabarsi, P.; Borhany, H.; Mohiaddin, R.; Houshmand, G. Myocarditis detected after COVID-19 recovery. Eur. Heart J. Cardiovasc. Imaging 2021, 22, 131–132.
  44. Ng, M.-Y.; Ferreira, V.M.; Leung, S.T.; Lee, J.C.Y.; Fong, A.H.-T.; Liu, R.W.T.; Chan, J.W.M.; Wu, A.K.L.; Lung, K.-C.; Crean, A.M.; et al. Patients recovered from COVID-19 show ongoing subclinical myocarditis as revealed by cardiac magnetic resonance imaging. JACC Cardiovasc. Imaging 2020, 13, 2476–2478.
  45. Lala, A.; Richter, F.; Zhao, S.; Somani, S.; Van Vleck, T.; Vaid, A.; Chaudhry, F.; De Freitas, J.K.; Fayad, Z.A.; Pinney, S.P.; et al. Prevalence and Impact of Myocardial Injury in Patients Hospitalized with COVID-19 Infection. J. Am. Coll. Cardiol. 2020, 76, 533–546.
  46. Wei, J.-F.; Huang, F.-Y.; Xiong, T.-Y.; Liu, Q.; Chen, H.; Wang, H.; Huang, H.; Luo, Y.-C.; Zhou, X.; Liu, Z.-Y.; et al. Acute myocardial injury is common in patients with COVID-19 and impairs their prognosis. Heart 2020, 106, 1154–1159.
  47. Topol, E.J. COVID-19 can affect the heart. Science 2020, 370, 408–409.
  48. Halushka, M.K.; Heide, R.S.V. Myocarditis is rare in COVID-19 autopsies: Cardiovascular findings across 277 postmortem examinations. Cardiovasc. Pathol. 2021, 50, 107300.
  49. Mele, D.; Flamigni, F.; Rapezzi, C.; Ferrari, R. Myocarditis in COVID-19 patients: Current problems. Intern. Emerg. Med. 2021, 16, 1123–1129.
  50. Bearse, M.; Hung, Y.P.; Krauson, A.J.; Bonanno, L.; Boyraz, B.; Harris, C.K.; Helland, T.L.; Hilburn, C.F.; Hutchison, B.; Jobbagy, S.; et al. Factors associated with myocardial SARS-CoV-2 infection, myocarditis, and cardiac inflammation in patients with COVID-19. Mod. Pathol. 2021, 34, 1345–1357.
  51. Wenzel, P.; Kopp, S.; Göbel, S.; Jansen, T.; Geyer, M.; Hahn, F.; Kreitner, K.-F.; Escher, F.; Schultheiss, H.-P.; Münzel, T. Evidence of SARS-CoV-2 mRNA in endomyocardial biopsies of patients with clinically suspected myocarditis tested negative for COVID-19 in nasopharyngeal swab. Cardiovasc. Res. 2020, 116, 1661–1663.
  52. Farshidfar, F.; Koleini, N.; Ardehali, H. Cardiovascular complications of COVID-19. JCI Insight 2021, 6, 148980.
  53. Mehta, P.; McAuley, D.F.; Brown, M.; Sanchez, E.; Tattersall, R.S.; Manson, J.J.; HLH Across Speciality Collaboration. COVID-19: Consider cytokine storm syndromes and immunosuppression. Lancet 2020, 395, 1033–1034.
  54. Most, Z.M.; Hendren, N.; Drazner, M.H.; Perl, T.M. Striking Similarities of Multisystem Inflammatory Syndrome in Children and a Myocarditis-Like Syndrome in Adults: Overlapping Manifestations of COVID-19. Circulation 2021, 143, 4–6.
  55. Tschöpe, C.; Ammirati, E.; Bozkurt, B.; Caforio, A.L.P.; Cooper, L.T.; Felix, S.B.; Hare, J.M.; Heidecker, B.; Heymans, S.; Hübner, N.; et al. Myocarditis and inflammatory cardiomyopathy: Current evidence and future directions. Nat. Rev. Cardiol. 2021, 18, 169–193.
  56. Fox, S.E.; Akmatbekov, A.; Harbert, J.L.; Li, G.; Brown, J.Q.; Heide, R.S.V. Pulmonary and cardiac pathology in African American patients with COVID-19: An autopsy series from New Orleans. Lancet Respir. Med. 2020, 8, 681–686.
  57. Sawalha, K.; Abozenah, M.; Kadado, A.J.; Battisha, A.; Al-Akchar, M.; Salerno, C.; Hernandez-Montfort, J.; Islam, A.M. Systematic Review of COVID-19 Related Myocarditis: Insights on Management and Outcome. Cardiovasc. Revasc. Med. 2021, 23, 107–113.
More
Video Production Service