Immunomodulating Therapies in Acute Myocarditis and Recurrent/Acute Pericarditis

Enrico Ammirati, Emanuele Bizzi, Giacomo Veronese, Matthieu Groh, Caroline M Van de Heyning, Jukka Lehtonen, Marc Pineton de Chambrun, Alberto Cereda, Chiara Picchi, Lucia Trotta, Javid J Moslehi, Antonio Brucato, Enrico Ammirati, Emanuele Bizzi, Giacomo Veronese, Matthieu Groh, Caroline M Van de Heyning, Jukka Lehtonen, Marc Pineton de Chambrun, Alberto Cereda, Chiara Picchi, Lucia Trotta, Javid J Moslehi, Antonio Brucato

Abstract

The field of inflammatory disease of the heart or "cardio-immunology" is rapidly evolving due to the wider use of non-invasive diagnostic tools able to detect and monitor myocardial inflammation. In acute myocarditis, recent data on the use of immunomodulating therapies have been reported both in the setting of systemic autoimmune disorders and in the setting of isolated forms, especially in patients with specific histology (e.g., eosinophilic myocarditis) or with an arrhythmicburden. A role for immunosuppressive therapies has been also shown in severe cases of coronavirus disease 2019 (COVID-19), a condition that can be associated with cardiac injury and acute myocarditis. Furthermore, ongoing clinical trials are assessing the role of high dosage methylprednisolone in the context of acute myocarditis complicated by heart failure or fulminant presentation or the role of anakinra to treat patients with acute myocarditis excluding patients with hemodynamically unstable conditions. In addition, the explosion of immune-mediated therapies in oncology has introduced new pathophysiological entities, such as immune-checkpoint inhibitor-associated myocarditis and new basic research models to understand the interaction between the cardiac and immune systems. Here we provide a broad overview of evolving areas in cardio-immunology. We summarize the use of new imaging tools in combination with endomyocardial biopsy and laboratory parameters such as high sensitivity troponin to monitor the response to immunomodulating therapies based on recent evidence and clinical experience. Concerning pericarditis, the normal composition of pericardial fluid has been recently elucidated, allowing to assess the actual presence of inflammation; indeed, normal pericardial fluid is rich in nucleated cells, protein, albumin, LDH, at levels consistent with inflammatory exudates in other biological fluids. Importantly, recent findings showed how innate immunity plays a pivotal role in the pathogenesis of recurrent pericarditis with raised C-reactive protein, with inflammasome and IL-1 overproduction as drivers for systemic inflammatory response. In the era of tailored medicine, anti-IL-1 agents such as anakinra and rilonacept have been demonstrated highly effective in patients with recurrent pericarditis associated with an inflammatory phenotype.

Keywords: COVID-19; acute myocarditis; anti-IL-1 therapy; cardiac sarcoidosis; corticosteroids; eosinophilic myocarditis; immunosuppressive therapy; pericarditis.

Conflict of interest statement

EA received a grant from the Italian Ministry of Health (GR-2019-12368506). AB: Institution received funding from Kiniksa Pharmaceuticals, Ltd., as an investigative site; unrestricted research grant from SOBI and ACARPIA; travel and accommodation for advisory committee from SOBI and Kiniksa. JM has served on advisory boards for Bristol Myers Squibb, Pfizer, Takeda, Audentes, Deciphera, Janssen, ImmunoCore, Myovant, Cytokinetics, AstraZeneca, ProteinQure, and Pharmacyclics. JM was supported by the National Institutes of Health (R01HL141466, R01HL155990, and R01HL156021). MG received consulting fees from Astrazeneca and GlaxoSmithKline. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2022 Ammirati, Bizzi, Veronese, Groh, Van de Heyning, Lehtonen, Pineton de Chambrun, Cereda, Picchi, Trotta, Moslehi and Brucato.

Figures

Figure 1
Figure 1
Immunosuppressive treatment strategies used for fulminant myocarditis or complicated acute myocarditis not supported by evidence from clinical trials but based on published case reports/series. i.v., intravenous; d, day; IVIG, intravenous immunoglobulin; h, hour; SLE, systemic lupus erythematosus; APS, antiphospholipid syndrome; ICI, immune checkpoint inhibitor; pts, patients; ATG, anti-thymocyte globulin; wk, week; CyA, cyclosporine; mo, month; EGPA, eosinophilic granulomatosis with polyangiitis; ANCA, antineutrophil cytoplasmatic antibodies; DRESS, drug reaction with eosinophilia asn dystemic symptoms; HES, hypereosinophilic syndrome; s.c., subcutaneous. Adapted from Ammirati et al. (1).
Figure 2
Figure 2
Ongoing trials in the setting of acute myocarditis evaluating the use of immunosuppressive drugs. PI, principal investigator; AM, acute myocarditis; HF, heart failure; LVEF, left ventricular ejection fraction; LVEDD, left ventricular end-diastolic diameter; iv, intravenous; d, days; HTx, heart transplant; LVAD, left ventricular assist device; t-MCS, temporary-mechanical circulatory support; VA, ventricular arrhythmias; AVB, atrioventricular block; MV, mechanical ventilation; sc, subcutaneous.
Figure 3
Figure 3
Etiological workup and immunosuppressive treatment strategies used for eosinophilic myocarditis. TTE, transthoracic echocardiography; CMRI, cardiac magnetic resonance; LVEF, left ventricular ejection fraction; ANCA, antineutrophil cytoplasmic antibodies; PCR, polymerase chain reaction; LDH, lactate dehydrogenase; HHV6, human herpes virus 6; CT, computed tomography; d, day; mo, month; AEC, absolute eosinophil count; HES, hypereosinophilic syndrome.
Figure 4
Figure 4
Immunosuppressive treatment strategies used for cardiac sarcoidosis based on clinical and imaging-based monitoring. FDG-PET, fluorodeoxyglucose positron emission tomography; VT/VF, ventricular tachycardia/ventricular fibrillation; LV, left ventricular ejection fraction; TnT, troponin.
Figure 5
Figure 5
Representative patient with acute myocarditis in whom immunosuppression was guided by FDG-PET and cardiac magnetic resonance imaging (CMRI). A 49-year-old woman with a previous history of ANA positive pericarditis presented with acute myocarditis. On CMRI she presented a transmural lesion in the anterior wall as demonstrated by late gadolinium enhancement (LGE, highlighted with asterisks) and increased T2 signal (normal value (A). Left ventricular ejection fraction (LVEF) remain preserved, but a ventricular arrhythmic burden was observed on telemetry monitoring with frequent premature ventricular complexes (PVC) and non-sustained ventricular tachycardia (NSVT) (B). An FDG-PET showed 3 focal areas of uptake in the heart with increased standardized uptake values (SUV), and an uptake in hilar nodes raising the suspect for cardiac sarcoidosis (C). A septal endomyocardial biopsy (EMB) from the right ventricle was non-diagnostic for myocarditis or cardiac sarcoidosis (D). Peak high sensitivity troponin T (hs-tnT) levels was 2,342 ng/L. After initial pulsed methylprednisolone, prednisone was started in combination with methotrexate (MTX) and later shift to mycophenolate mofetil (MMF) and colchicine plus bisoprolol with normalization of troponin levels, and no signs of residual inflammation on FDG-PET (C), and a reduction of PVC burden. Accordingly, CMRI showed a reduction of T2 signal while LGE remains suggesting an area of residual fibrosis (E).
Figure 6
Figure 6
The inflammasome-mediated inflammatory cascade and the location of the effect of currently available drugs for recurrent pericarditis. Non-specific triggers such as structural damage or microbial agents may interact with specific receptors such as NLR and TLR and thus activate the inflammasome. This naturally occurs, but a genetic background may alter the inflammasome response and consequently generate a pathologic response with a sustained inflammatory state. NSAIDs perform their effect directly on inflammasome activation. Azathioprine and corticosteroids carry out their effect mainly on B and T lymphocytes. While Anakinra and Rilonacept directly inhibit IL-1 effects, both colchicine and corticosteroids perform their action on other inflammatory mediators released after inflammasome activation. Furthermore, colchicine also exerts an inhibitory effect on inflammasome activation. PAMPs, pathogen-associated molecular patterns; DAMPs, damage-associated molecular patterns; TLR, toll-like receptor; NLR, NOD-like Receptor; NSAIDs, non-steroidal antiinflammatory drugs.
Figure 7
Figure 7
Immunosuppressive treatment strategies used for acute and recurrent pericarditis. In brackets are reported recommendation and level of evidence based on guidelines. NSAIDs, non-steroidal anti-inflammatory drugs; h, hours; d, day; PO, per os; IV, intravenous; CCS, corticosteroids; IVIG, intravenous immunoglobulin; SC, subcutaneous. Adapted from Adler et al. (210).
Figure 8
Figure 8
Representative patient with pericarditis and resolution of the pericardial inflammation on sequential CMRI scans. Four-chamber late gadolinium enhancement (LGE) PSIR cardiac MRI images of a 35-year-old male patient who presented with recurrent idiopathic pericarditis under NSAIDs and colchicine. (A) At presentation, there was diffuse pericardial thickening and LGE, and presence of pericardial effusion. High-dose corticosteroids (prednisolone 40 mg once daily) with taper schedule and azathioprine were initiated. (B) Re-evaluation after 3 months showed regression of pericardial LGE and disappearance of pericardial effusion. This allowed to further decrease the dose of steroids. (C) Follow-up cardiac MRI 5-months later showed near resolution of pericardial LGE. A low dose of steroids (prednisolone 4 mg once daily) was maintained. (D) Control after 1 year showed a normal pericardium without LGE. Image courtesy of Bernard Paelinck (Antwerp University Hospital).

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