PMC:7289100 / 17647-30097 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7289100","sourcedb":"PMC","sourceid":"7289100","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7289100","text":"7 Kawasaki like disease secondary to COVID-19\nKawasaki disease (KD) is a systemic vasculitis that usually affects children less than 5 years old. Soon after the first description by Tomisaku Kawasaki in 1967, it was clear that the disease, although self-limiting, might cause coronary artery aneurism (CAA) in a high percentage of cases [61]. KD is nowadays considered as the first cause of acquired heart disease in children from developed countries [62]. The disease is far more common in eastern countries, and in children of eastern origin living in western countries. For example, the 2010 annual incidence for KD was 222.9 cases/100000 children \u003c5 y/o in Japan, compared to 20/100000 in the USA [63,64]. Since no specific test is available, diagnosis relies on the recognition of the cardinal clinical features and the exclusion of other mimickers. The mainstay of treatment is the administration of intravenous immunoglobulins (IVIG) at 2 g/kg of body weight, as soon as the diagnosis is established, and possibly within 10 days from the onset of fever. IVIG have been demonstrated to reduce the risk of CAA [65]. A subgroup of patients, accounting for nearly 5% of those with KD, has been described to have a very severe disease onset with systolic hypotension or shock (Kawasaki Shock Syndrome-KSS). The shock may be caused by a capillary leak syndrome or by poor perfusion due to inflammatory myocarditis. KSS patients are more likely to be females and to have earlier onset, incomplete presentations, and more severe laboratory abnormalities (lower platelet counts, higher serum CRP levels, hyponatremia, increased transaminases, metabolic acidosis, consumptive coagulopathy, and lower serum albumin levels). Patients with KSS are often resistant to IVIG treatment and have a higher incidence of coronary artery aneurysms, mitral regurgitation, and prolonged myocardial dysfunction [66].\nNorthern Italy was the first European region to be severely hit by the SARS-COV2 epidemic after the original outbreak in China [67]. Although the data on the clinical presentation of COVID-19 in children is still scarce, lower rates of infection and milder forms of disease seem to be typical of this age group [68,69]. Since the end of March 2020, we observed and treated or received information from all over Italy about an abnormally elevated number of critically ill patients with clinical characteristics consistent with Kawasaki Shock Syndrome (KSS). The common features were: “middle-aged” children (6–9 y/o) with a history of persistent high spiking fever in the previous days, abdominal pain, diarrhea, skin rash, and rapidly deteriorating clinical conditions with the onset of shock, without clear signs of dehydration. Other less common features were arthralgia, cough, meningism, conjunctivitis and reddened, cracked lips. Labworks usually showed high inflammatory markers, low lymphocyte count, low sodium, and high troponin and pro-BNP levels. Echocardiography was consistent with myocarditis in the majority of patients instead of classical coronary artery abnormalities. Patients were diagnosed as Kawasaki disease (typical or incomplete) and treated accordingly with IVIG and/or steroids. One patient refractory to such treatments responded successfully to intravenous anakinra. Althoug all the patients had family contacts consistent with COVID-19, serology and nasopharyngeal swabs were inconsistently positive both in the single patients and among all children. To date we are aware of at least 10 cases of KSS possibly related to COVID-19. Given the unprecedented cluster of patients we decided to launch a nationwide alert for pediatricians and start a national registry. Few days after the diagnosis of our first cases, news from all over Europe first, and Eastern USA thereafter, reported on the identification of patients with remarkably the same characteristics we have observed. Some children with a less severe picture, without shock at the onset, but with clinical characteristics of systemic inflammation and some features of KD have also been seen by us and others (personal communications). These observations lead to a variety of nationwide alerts in the respective countries [70,71]. On May 7, 2020, Riphagen et al. published on 8 patients treated at the South Thames Retrieval Service for a severe acute illness similar to KSS [72]. Age at presentation was between 4 and 14 years, 6 out of 8 children were of Afro-Caribbean descent and 5 were boys. All the children had a similar disease onset with persistent fever, skin rash, conjunctivitis, peripheral oedema, and extremity pain. Gastrointestinal symptoms were frequent and severe, all children developed shock requiring ICU admission and vasopressors. Another key feature described in those patients was the cardiac involvement, as testified by very elevated cardiac enzymes, and echo-bright coronary vessels. One patient developed a giant coronary aneurism. Lab works typically showed high C-reactive protein, procalcitonin, ferritin, triglycerides, and D-dimers. All children were treated with IVIG (2 g/kg) and 6 also received aspirin (50 mg/kg). Broncho-alveolar lavage or nasopharyngeal aspirates were negative for SARS-COV-2 in all children; some of the patients had histories of familial contact with the virus. The authors stated that, at the time they were writing their report, another ICU in London managed 20 patients with similar characteristics. As per the Royal College of Pediatrics and Child Health (RCPCH) alert, some of these patients resulted to be positive for SARS-CoV-2 infection, by either nasopharyngeal swab, serology, or both [69]. The New York State Department of Health reported sixty-four cases as of May 5th 2020. For the purpose of this review we will refer to this clinical entity as Pediatric COVID-19 Hyperinflammatory Syndrome (PeCOHS), while the English authorities refers to it as Pediatric inflammatory multisystem syndrome temporally associated with SARS-CoV-2 infection (PIMS-TS).\nVerdoni et al. published the first Italian experience on 10 patients admitted to their hospital for Kawasaki-like disease from February 18th to April 20th, 2020 (during the peak of COVID19 epidemic in Italy). Very nicely, the authors compared these children (group 2) to the historical cohort of KD patients seen in the last 5 years (group 1, 19 patients). Half of the children in group 2 presented with classic KD, while half were diagnosed as incomplete KD. Half of the patients showed hypotension and signs of hypoperfusion at onset, and were interpreted as KSS, and half had signs of myocarditis at echocardiogram. Pro-BNP was above normal values in all the patients. Half of the patients satisfied the PRINTO laboratory criteria for Macrophage Activation Syndrome (MAS) [73]. Two patients developed CAAs. Patients in group 2 displayed older age, a higher frequency of gastrointestinal and respiratory symptoms, meningeal signs, myocarditis, shock syndrome, and MAS criteria as compared with group 1. Nasopharyngeal swab for SARS-CoV-2 was positive in 2 patients only, 8 patients had positive IgG while 3 patients had positive IgM (all of whom were positive also for IgG) for SARS-CoV-2. All patients from group 2 were treated with IVIG and steroids, with good clinical outcome [74].\nThe occurrence of such cases with a stereotyped clinical picture, which is rarely seen in children, during the peak of SARS-CoV2 infection in highly epidemic areas, points to a causative link. One hypothesis is that these children were suffering from actual KD triggered by the SARS-CoV-2 virus. Indeed, a microbial etiology has been long advocated as a possible cause for KD. Many viruses (HHV-6, Epstein Barr virus, Cytomegalovirus, Coronavirus other than SARS-CoV-2, Parvovirus B19 etc.) but also bacterial infections (such as staphylococci, streptococci, Bartonella, and Yersinia) have been linked to KD. Interestingly enough, a case of classic KD has been recently reported in a 6 months-old child who tested positive for SARS-CoV-2, although this could be just coincidental [75]. The clinical and laboratory characteristics of the patients recently described are strikingly similar to the KSS typical picture, except for the older age, male predominance and relatively low frequency of coronary artery aneurysms [65]. Given these differences, it can be speculated that this COVID-19 Hyperinflammatory Syndrome is indeed a systemic vasculitis peculiar of the pediatric age and caused by SARS-CoV-2 infection.\nHow SARS-CoV-2 infection may cause a hyperinflammatory syndrome? At this point we can only formulate hypotheses, based on the clinical picture of the observed patients and using other diseases with overlapping manifestations, such as KD and Toxic Shock Syndrome (TSS), as models. The delay between the pandemic peak of COVID-19 and the occurrence of this hyperinflammatory syndrome in children does not point to a direct effect of the infection, but rather towards an immune-mediated disease. This seems to be confirmed also by the observation of Verdoni et al. that the majority of their patients had positive SARS-CoV-2 IgG, but negative IgM and swabs. Staphylococcal or Streptococcal TSS are the result of T cells induction by superantigens TSST-1, enterotoxins B or C (staphylococci), or pyrogenic exotoxin A or B (streptococci). Superantigens can stimulate clonal T cell proliferation and this leads to the production of massive amounts of pro-inflammatory cytokines, as IL-1, IL-6, and IFN-γ in a so-called cytokine storm [76]. There is a body of evidence suggesting that KD may be caused by a superantigen response, and recent data demonstrated that KSS is characterized by a massive pro-inflammatory cytokine release that differentiate those patients from the “regular” KD patients [77]. This cytokine storm could be the underlying mechanism leading to the clinical picture similar of that of TSS, KSS, and PeCOHS.\nOther possible mechanisms by which SARS-CoV-2 could induce a hyperinflammatory syndrome are: i) the autoantibodies formation through “molecular mimicry”, as in Acute Rheumatic Fever (although this mechanism would not justify the occurrence of shock); ii) a vascular damage secondary to the deposition of immune-complexes as in acute serum sickness; iii) an antibody-dependent enhancement (ADE) with IgG immune complexes that enhance virus infection in Fc-receptor-bearing cells. Intriguingly, this phenomenon is the cause of Dengue vascular permeability syndrome, which, again, shares some similarities with PeCOHS [78]. ADE were demonstrated in SARS-CoV infection years ago, mediated by antibodies directed to the envelope spike proteins [79].\nChildren with SARS-CoV-2 infection usually have a benign course [67]. Differently from what we usually see in Kawasaki Disease, which has a predilection for asian countries, PeCOHS has not been described so far in those countries, suggesting that both the genetic predisposition of the host and differences in the viral genome may play a role in this disease.\nTo our knowledge, the majority of patients with PeCOHS respond to a variable combination of steroids and IVIG. The discussion about the immunomodulatory effects of both steroids and IVIG is beyond the scope of this review, but it is interesting to highlight that one of the many effects of IVIG is the down modulation of superantigens [80]. Of note, IVIG is the therapy of choice in the capillary leak syndrome, whose main features are similar to KSS and PeCOHS [81]. Finally, the efficacy of anti-IL-1 treatment as “rescue therapy” for cases resistant to IVIG+steroids points out the relevance of this pro-inflammatory cytokine in the hyperinflammatory state, similar to what already shown in adults with COVID-19 and hyperinflammation [82].\nIn conclusion, although SARS-CoV-2 infection appears to occur as a oligo-symptomatic form in the majority of children, there is mounting evidence that it can cause a systemic hyperinflammatory syndrome that mimics KSS, but has some peculiar features. The role of host and virus genetics and the exact immune mechanisms leading to the disease are far from been understood, and case collection would help us in better characterization of the clinical phenotype. As light has been shed on the interaction between SARS-CoV-2 and the immune system, we will gain hints also at Kawasaki Disease pathogenesis, almost 50 years from its first description by Tomisaku 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