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Specific Immune- Related Manifestations of COVID-19

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Specific Immune- Related Manifestations of COVID-19 REVIEWS Systemic and organ- specific immune- related manifestations of COVID-19 Manuel Ramos- Casals 1,2 ✉ , Pilar Brito- Zerón3 and Xavier Mariette4 Abstract | Immune- related manifestations are increasingly recognized conditions in patients with COVID-19, with around 3,000 cases reported worldwide comprising more than 70 different systemic and organ- specific disorders. Although the inflammation caused by SARS- CoV-2 infection is predominantly centred on the respiratory system, some patients can develop an abnormal inflammatory reaction involving extrapulmonary tissues. The signs and symptoms associated with this excessive immune response are very diverse and can resemble some autoimmune or inflammatory diseases, with the clinical phenotype that is seemingly influenced by epidemiological factors such as age, sex or ethnicity. The severity of the manifestations is also very varied, ranging from benign and self- limiting features to life- threatening systemic syndromes. Little is known about the pathogenesis of these manifestations, and some tend to emerge within the first 2 weeks of SARS- CoV-2 infection, whereas others tend to appear in a late post- infectious stage or even in asymptomatic patients. As the body of evidence comprises predominantly case series and uncontrolled studies, diagnostic and therapeutic decision- making is unsurprisingly often based on the scarcely reported experience and expert opinion. Additional studies are required to learn about the mechanisms involved in the development of these manifestations and apply that knowledge to achieve early diagnosis and the most suitable therapy. In January 2020, a novel coronavirus — severe acute res- manuscripts. This Review compiles the current know- piratory syndrome coronavirus 2 (SARS-CoV-2) — was ledge of immune-related manifestations associated with identified as the aetiological agent for a cluster of pneu- the COVID-19 (both systemic and organ- specific) and 1Department of Autoimmune monia cases initially detected in Wuhan City, China1. focuses principally on specific epidemiological, clin- Diseases, ICMiD, Hospital The disease caused by SARS- CoV-2, COVID-19, has ical and virological aspects that could help specialists Clínic, Barcelona, Spain. a very wide clinical spectrum, ranging from asympto- to identify and manage patients presenting with these 2Department of Medicine, University of Barcelona, matic cases (accounting for a substantial proportion features. Barcelona, Spain. of infections) to development of bilateral pneumonia 3Department of Internal that can progress to respiratory failure and, in some Immune- related systemic manifestations Medicine, Hospital cases, multi-organ failure and death2. Some patients can Some patients with COVID-19 can develop a severe, CIMA- Sanitas, Barcelona, develop a hyperinflammatory response caused by an acute virus- induced lung injury under the umbrella Spain. excessive reaction to the virus, characterized by a highly of acute respiratory distress syndrome (ARDS), a clinical 4Department of impaired interferon type I response associated with a syndrome characterized by acute lung inflammation and Rheumatology, Center for Immunology of Viral persistent blood viral load, with inflammation being increased-permeability pulmonary oedema due to injury 6 Infections and Autoimmune partially driven by the transcription factor NF- κB with to the alveolar capillary barrier . The hyperinflammatory Diseases, Université increased TNF and IL-6 production3. This exacerbated phenotype of ARDS is characterized by elevated con- Paris- Saclay, INSERM, immune- related inflammatory response can promote centrations of pro-inflammatory cytokines, an increased Assistance Publique – the development of extrapulmonary features4, including incidence of shock and adverse clinical outcomes7,8. Hôpitaux de Paris, Hôpital Bicêtre, Le Kremlin- Bicêtre, immune- related manifestations that can mimic a wide Although the mechanisms of COVID-19-induced ARDS 9 Paris, France. variety of systemic and organ-specific inflammatory and are still being elucidated , the term ‘cytokine storm’ ✉e- mail: [email protected] autoimmune diseases (BOx 1), as has been reported in has become synonymous with its pathophysiology, 5 https://doi.org/10.1038/ other viral infections . To date, reports of these man- although some authors have suggested use of this term s41584-021-00608- z ifestations have been scattered among hundreds of is misleading in the context of severe COVID-19 (REF.10). NATURE REVIEWS | RHEUMATOLOGY VOLUME 17 | JUNE 2021 | 315 0123456789();: REVIEWS Key points (92%), cardiovascular (80%), mucocutaneous (74%) and respiratory (70%) symptoms. The clinical presentation • COVID-19 can produce a systemic inflammatory reaction involving extra-pulmonary is severe; around half of the reported cases fulfilled the organs. criteria for defined or incomplete Kawasaki disease and • Immune- related manifestations are increasingly recognized conditions in patients 73% required critical care, with an overall mortality with COVID-19. rate of 1.7% (Supplementary Table 1). MIS- C has some • ~3,000 cases involving >70 different systemic and organ- specific immune- related notable differences from classic Kawasaki disease18–21, disorders have been reported. which predominantly affects children under the age of • The clinical phenotype varies and seems to be influenced by age, sex and/or ethnicity. 5 years and most prominently in Asian populations, and • The severity of immune- related manifestations of COVID-19 ranges from completely has lower rates of admission to an intensive care unit benign, self- limiting manifestations to systemic, life- threatening syndromes. (ICU) and death than does MIS- C. However, the sys- • Some features tend to appear within the first 2 weeks of SARS- CoV-2 infection, temic phenotype of MIS-C and the specific involvement and others emerge in a late post- infectious stage or even in asymptomatic patients. of some organs, such as the coronary arteries, suggest a close link with Kawasaki disease22 and, in fact, the fre- quency of coronary aneurysms reported in the largest Even the term cytokine storm has been frequently series of children diagnosed with MIS- C (8–23%)17,23–25 interchanged with the term ‘cytokine release syndrome’ is quite similar to that reported in children with classic (CRS)10, which describes an immune- related dysregu- Kawasaki disease (6–17%)18,19. Most cases of MIS- C lation associated with the release of large amounts could be the result of a post- viral immune- related of cytokines that trigger systemic inflammation response. In non- Asian countries with large outbreaks with multi- organ failure and high mortality rates. CRS of SARS- CoV-2 (such as France, Italy, Spain, UK and is one of the most frequent serious adverse effects of USA), most cases of MIS- C were reported in the late chimeric antigen receptor T (CAR-T) cell therapies11 and stages of the first wave of the pandemic17,26 (the reason is characterized by fever, tachycardia, tachypnoea why Asian countries such as China and Japan have not and hypotension, the key symptoms that define sys- reported a similar number of MIS-C cases is unknown27) temic inflammatory response syndrome10. IL-6, a pro- and were diagnosed a mean of 25–45 days after onset inflammatory cytokine, is an important mediator of the of SARS- CoV-2 infection17,28. Accordingly, the rate of acute inflammatory response in ARDS and CRS, and SARS- CoV-2 infection confirmed by serological tests seems to also factor in severe COVID-19, contributing to in children with MIS- C is ~90%, in contrast to only elevated C-reactive protein concentrations, hypercoagu- ~40% positivity using PCR tests (indicating an ongoing lation and hyperferritinaemia12,13. However, serum IL-6 infection) (Supplementary Table 1). The development concentrations reported in patients with COVID-19 are of a Kawasaki disease-like presentation in children pre- substantially lower than those reported in patients with senting with severe COVID-19 cannot be considered CRS, ARDS or sepsis10,14, or even influenza15. Why some unexpected29, in view of the important contribution of patients with severe COVID-19 rapidly enter a state of respiratory viral infections to the aetiopathogenesis multi- organ failure is unknown, but the pathophysiol- of Kawasaki disease30. However, the question of whether ogy of COVID-19- associated ARDS seems to be more MIS- C should be considered a discrete entity or could complex than a simple overproduction of cytokines9. be an aetiologically driven subset of Kawasaki disease The systemic phenotype related to the inflam- is still unresolved31, as the inflammatory response in matory reaction triggered by SARS- CoV-2 infection MIS- C shares several features with Kawasaki disease is very broad and can be reminiscent of that of some but differs with respect to the T cell subsets involved, auto immune or inflammatory diseases. In children, lack of IL-17A- mediated hyperinflammation and levels systemic involvement has a substantial overlap with of biomarkers related to arterial damage32. Kawasaki disease, whereas in adults it seems to be closer Cases of young adults with COVID-19 presenting to haemophagocytic lymphohistiocytosis (HLH), anti- with a classic phenotype of Kawasaki disease have also phospholipid syndrome (APS) or systemic vasculitis been reported33–36; these cases suggest that the Kawasaki (TABle 1, Fig. 1). disease phenotype presented by adults with COVID-19 follows the spectrum of classic Kawasaki disease,
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