COVID-19 Inflammatory With Clinical Features Resembling Kawasaki Disease Robert Spencer, MD,a Ryan C. Closson, MD,a Mark Gorelik, MD,b Alexis D. Boneparth, MD,b Rebecca F. Hough, MD, PhD,c Karen P. Acker, MD,d Usha Krishnan, MDa

We describe 2 patients with coronavirus disease who had multiple clinical abstract features suggestive of Kawasaki disease (KD). Both patients presented with lasting .5 days and were found to have , conjunctival injection, and swollen lips. One patient also had extremity swelling, whereas the other Divisions of aPediatric , bAllergy, , and fi , and cPediatric Critical Care Medicine, developed of the ngers. In both cases, laboratory results were Department of , Columbia University Irving similar to those seen in KD. These patients had highly unusual but similar Medical Center and Morgan Stanley Children’s Hospital, New d features, and both appeared to respond favorably to treatment. It remains York, New York; and Division of Pediatric Infectious Diseases, Department of Pediatrics, Weill Cornell Medicine, unclear whether these patients had true KD or manifestations of coronavirus New York, New York disease that resembled KD. Dr Spencer was the consulting cardiology fellow who evaluated 1 of the 2 patients, and he was the primary author of this case report; Dr Closson was the consulting cardiology fellow who evaluated the As of May 18, 2020, nearly 1.5 million of his and feet developed. other patient, and he contributed references and cases of coronavirus disease (COVID- Two days later, he developed revisions to the manuscript; Dr Gorelik was the fi consulting rheumatology attending who helped 19) have been con rmed in the a polymorphous rash on his torso, manage one of these patients, and he contributed 1 United States. Although ∼2% of cases extremities, and face. The patient references and revisions to the manuscript; Dr are among individuals aged ,18 contacted his primary care physician, Boneparth was the consulting rheumatology years, and the majority of those who recommended supportive care. attending who helped manage these patients, and he patients experience mild symptoms, Three days later, symptoms increased contributed references and revisions to the manuscript; Dr Hough was the critical care our understanding of the wide in severity, and the patient began to attending who primarily managed these patients in spectrum of clinical patterns and have , severe , and the ICU, and she contributed references and spectrum of disease in this population neck stiffness, prompting revisions to the manuscript; Dr Acker was the remains limited.2,3 We report 2 cases presentation to the emergency consulting infectious disease attending who helped of children who tested positive for department. manage these patients, and she contributed revisions to the manuscript; Dr Krishnan was the severe respiratory syndrome On admission, his temperature was precepting attending for Dr Spencer and senior coronavirus 2 (SARS-CoV-2) on 39.3°C, with a rate of 145 beats author, and she conceptualized and contributed reverse transcription polymerase revisions to the manuscript; and all authors per minute and blood pressure of chain reaction (RT-PCR) but approved the final manuscript as submitted and 78/42. He had a respiratory rate of presented with a multisystem agree to be accountable for all aspects of the work. 24 breaths per minute and oxygen inflammatory syndrome that also DOI: https://doi.org/10.1542/peds.2020-1845 saturation of 97% while he was may fulfill diagnostic criteria for Accepted for publication May 26, 2020 breathing ambient air. On examination, Kawasaki disease (KD). he appeared unwell and in moderate Address correspondence to Robert Spencer, MD, Division of Pediatric Cardiology, Morgan Stanley distress with grunting. He had nuchal Children’s Hospital of New York-Presbyterian, rigidity, bilateral bulbar conjunctival PATIENT I Columbia University Irving Medical Center, 3959 injection without exudate, and diffuse Broadway, New York, NY 10032. E-mail: ros9225@ An 11-year-old boy with a history of maculopapular rash (Fig 1). His lips nyp.org febrile had been well until were initially noted to be swollen and 5 days before his presentation, when red, although this was not subsequently To cite: Spencer R, Closson RC, Gorelik M, et al. fever, , , dry observed. He did not have cervical COVID-19 Inflammatory Syndrome With Clinical , emesis, , myalgia, adenopathy, and extremity was Features Resembling Kawasaki Disease. Pediatrics. 2020;146(3):e20201845 bilateral , and swelling not noted.

Downloaded from www.aappublications.org/news by guest on September 29, 2021 PEDIATRICS Volume 146, number 3, September 2020:e20201845 CASE REPORT Pertinent laboratory results on with a 5-day course of intravenous presentation of the patient (patient 1) for cytokine storm to the emergency department are resulting from COVID-19. The summarized in Table 1. They patient’s fever resolved within included a normal 24 hours of receiving IVIg, and his count with neutrophilic noncardiac symptoms have continued predominance and lymphopenia, to improve. A repeat echocardiogram hyponatremia, mild transaminitis did not reveal any further coronary and hypoalbuminemia, elevated abnormalities. inflammatory markers, and elevated N-terminal B-type natriuretic peptide PATENT II (NT-ProBNP). Urinalysis and cerebrospinal fluid (CSF) cell counts, The second patient was a previously which were obtained because of his healthy 7-year-old girl who presented nuchal rigidity and severe headache, with 5 days of fever, sore throat, were unremarkable. Urine, blood, and severe , emesis and CSF cultures were negative for diarrhea, and an . COVID-19 was diagnosed multiforme-like rash on the face, on the basis of RT-PCR for SARS-CoV- FIGURE 1 trunk, and back. Two days earlier, her Rash on the arm of patient 1 (shared with parents took her to a local emergency 2. Electrocardiogram showed normal parental permission). sinus rhythm with nonspecific ST- department, where she tested and T-wave changes. Chest positive for SARS-CoV-2 on RT-PCR. radiography revealed patchy perihilar venous line and an arterial line were On examination, in addition to her opacities in both lungs. He was placed. Although preparations were rash (Fig 2), she was found to have started on antimicrobial therapy, made to intubate for impending conjunctival erythema, cracked lips, including coverage for herpes simplex respiratory failure in the setting of and strawberry . Laboratory virus, toxic syndrome, and shock, he improved, and his results included leukopenia, rickettsial disease, with vancomycin, vasoactive infusions were weaned thrombocytopenia, hyponatremia, ceftriaxone, acyclovir, clindamycin, within hours. Transthoracic mild transaminitis and and doxycycline. He was fluid revealed low- hypoalbuminemia, elevated troponin, resuscitated, and a dopamine infusion normal systolic function of the left and elevated inflammatory markers. was added for hypotension. and a shortening fraction of Because of severe abdominal pain Supplemental oxygen was provided 29% (normal range, 25–45) on concerning for acute appendicitis, through a nasal cannula at a rate of vasoactive support, with moderate abdominal ultrasound and MRI were 2 L per minute. mitral regurgitation and a small both obtained and demonstrated pericardial effusion. The right acute, aggressive colitis, and ileitis. The patient continued to have fever coronary artery was noted to be Shortly after admission, the patient and developed desquamation of his prominent with lack of tapering but developed agitation and confusion fingertips. He soon developed had a z score of 1.4 (normal value, concerning for encephalopathy. On leukocytosis (white blood cell count, ,2.0), whereas the proximal left telemetry, she was noted to have 19 440 per cubic millimeter) and coronary artery appeared normal; no frequent premature ventricular continued to have thrombocytopenia. were evident. contractions. Transthoracic On hospital day 2, his high-sensitivity echocardiography revealed low- troponin T increased to 136 ng/L Given the patient’s persistent normal systolic function of the left (normal value, ,22), whereas NT- and mucocutaneous findings, his ventricle and a shortening fraction of ProBNP rose to 35 137 000 pg/L supportive laboratory data 27%, mild mitral regurgitation, and (normal range, 10 000–242 000). He (leukocytosis with neutrophilic normal . In the continued to have worsening predominance, hyponatremia, context of the previous patient with hypotension and was transitioned hypoalbuminemia, elevated hyperinflammatory syndrome and from dopamine to high-dose inflammatory markers) and his evidence of significant multisystem epinephrine, norepinephrine, and echocardiographic findings (mitral involvement in the setting of COVID- vasopressin infusions. Cefepime was regurgitation and pericardial 19, treatment with intravenous added for increased Gram-negative effusion), there was concern for corticosteroids was initiated, with coverage, and he was given stress- possible KD. He was treated with prompt fever defervescence and dose hydrocortisone. A central intravenous immunoglobulin (IVIg) improvement in her clinical

Downloaded from www.aappublications.org/news by guest on September 29, 2021 2 SPENCER et al TABLE 1 Demographic and Clinical Characteristics and Laboratory Findings Characteristic Patient 1 Patient 2 Age, y 11 7 Sex Male Female Febrile seizures None Kawasaki criteria Fever, mucosal changes, conjunctivitis, Fever, mucosal changes, rash, extremity swelling conjunctivitis, rash Imaging features Patchy perihilar opacities Patchy perihilar opacities Echocardiogram features Low-normal function, moderate mitral Low-normal function, mild regurgitation, small pericardial effusion mitral regurgitation Findings on presentation Days since disease onset 5 5 Disease severity Critical Stable Laboratory findings White blood cell count, per 8100 3990 (↓) mm3 Differential count, per mm3 Total neutrophils 6642 (↑) 2872 (↑) Total lymphocytes 543 (↓) 678 Total monocytes 454 80 (↓) Platelet count, per mm3 116 000 (↓) 69 000 (↓) , g/L 117 128 , g/L 27 (↓)37(↓) Alanine aminotransferase, 118.0 (↑) 52.0 (↑) U/L Aspartate 84.0 (↑) 47.0 (↑) aminotransferase, U/L FIGURE 2 Sodium, mmol/L 126 (↓) 129 (↓) Rash on the back of patient 2 (shared with Potassium, mmol/L 3.6 3.9 parental permission). Creatinine, mg/L 80 74 Creatine kinase, U/L 223.0 (↑) 45.0 ↑ High-sensitivity troponin T, 18.0 61.0 ( ) fl ng/L KD is an acute, systemic in ammatory NT-ProBNP, pg/L 14 587 000 (↑) 6 985 000 (↑) that is predominantly High-sensitivity C-reactive 293.0 (↑) 185.0 (↑) diagnosed in children ,5 years of protein, mg/L age. Affecting medium-sized arteries, ↑ ↑ Sedimentation rate, mm/h 76.0 ( ) 56.0 ( ) with a predilection for coronary Procalcitonin, ng/mL 24.0 (↑) N/A Ferritin, ng/mL 1121.0 (↑) 695.5 (↑) arteries, it is a leading cause of Urinalysis Normal Normal acquired heart disease in the United Urine culture No growth N/A States.12 The etiology of the disease Blood culture No growth No growth remains elusive; however, clinical, CSF culture No growth N/A immunologic, and epidemiological ↑, increased; ↓, decreased; N/A, not applicable. evidence suggests an infectious trigger.13 Although an association of symptoms. Although the diagnosis of clinical presentations and outcomes KD with non–COVID-19 subtypes of KD was considered, IVIg was not associated with the virus remains coronavirus has been suggested, given, because she did not meet poorly understood, particularly in the causality has not been established, diagnostic criteria for incomplete KD, pediatric age group.4,5 Most children and this association was contradicted and the consensus at that time was appear to experience predictable and by subsequent investigations.14–17 that her symptoms were likely due to milder symptoms, such as diarrhea, Although there is no specific test to COVID-19. After a week course of oral fever, and upper respiratory diagnose KD, the diagnosis is made on glucocorticoids was completed, she symptoms, and recover within 1 to the basis of the presence of – had recurrence of rash and, at 2 weeks.6 9 However, uncommon a constellation of signs and present, is once again on clinical presentations have also symptoms.12 glucocorticoids. been reported.2,4,6 For instance, investigators have recently described These patients presented with cases of patients with confirmed or $5 days of fever and were found to DISCUSSION highly suspected COVID-19 who have mucosal changes, rash, and Despite the ongoing global spread of presented with clinical features of conjunctival injection, which are COVID-19, the broad spectrum of KD.10,11 diagnostic criteria for KD

Downloaded from www.aappublications.org/news by guest on September 29, 2021 PEDIATRICS Volume 146, number 3, September 2020 3 (Supplemental Fig 3). They also both develop coronary artery aneurysms, her follow-up echocardiogram had gastrointestinal involvement, which are the major cause of 2 weeks after discharge. which has occasionally been morbidity and mortality in KD.25,26 It remains unclear if these patients described in patients with KD.18 One Both patients had low-normal left had true KD with coincidental SARS- patient also had extremity swelling, ventricle contractility and valvar CoV-2 infection, SARS-CoV-2 whereas the other developed regurgitation. These findings were infection triggering KD, or an desquamation of the fingers. In both consistent with , which independent multisystem cases, the patients exhibited histologic evidence suggests is inflammatory syndrome related to laboratory results consistent with universal in KD.12 The presence of SARS-CoV-2 infection. It is possible KD, such as hyponatremia, a pericardial effusion in one of our that indeed these patients hypoalbuminemia, transaminitis, and patients also indicated demonstrate a novel infectious or elevated inflammatory markers. resulting from his disease. Neither postinfectious syndrome of COVID- Given these findings, concern for KD patient’s echocardiogram revealed 19 with a similar underlying was reasonable. However, some of the coronary artery ectasia or . mechanism of disease to KD, patients’ laboratory and clinical Although these findings may be especially given the lack of findings were not characteristic of absent at presentation, they can be pulmonary symptoms during KD. Notably, our first patient observed within the first 2 to 3 weeks disease development. As a result, presented with severe headache, after fever onset in KD, after which their risk of developing coronary confusion, and nuchal rigidity, their development is unlikely.27 It is artery aneurysms remains prompting a for CSF also worth noting that ∼25% of unknown. Thus, it is important to fluid collection. This is atypical for patients with KD develop coronary consider the potential for cardiac patients with KD. The second patient artery abnormalities.28,29 sequelae in these patients, and to had acute and severe ileitis and colitis manage them accordingly. At the and altered mental status. These Selecting the most appropriate same time, recognizing differences findings are also not classically treatment strategies for these in clinical and laboratory reported in KD. Although one patient patients was not straightforward. presentation will allow us to quickly developed leukocytosis, the other For the first patient, initial primary and appropriately treat patients. presented with leukopenia, which is focuswastomanagehisshock Because patients with COVID-19 uncharacteristic of the disease.12 Both syndrome, which is observed in 7% have a wide variety of clinical patients had thrombocytopenia of patients with KD and can be presentations overlapping with throughout their hospital courses, misdiagnosed as bacterial sepsis or multiple disease processes, which is rare beyond the acute phase .30,31 Given his including KD and toxic shock of KD and could suggest increased constellation of symptoms syndrome, treatment must be disease severity (including shock) consistent with KD and the severity tailored to patients on an individual and higher risk of coronary artery of his illness, he was treated with level on the basis of discussions aneurysms, or which could suggest an IVIg and corticosteroids. This – between the infectious disease, alternative diagnosis.12,19 22 treatment led to immediate rheumatology, cardiology, and, if Additionally, thrombocytopenia is resolution of his fever and applicable, critical care teams. associated with acute SARS-CoV-2 improvement of his clinical status. infection and inflammatory disease.23 Notably, IVIg has been administered Finally, it is also noteworthy to recall Although NT-ProBNP can be elevated with success for acute myocarditis that patients with KD can develop in patients with KD, particularly those during the acute pandemic period of a Kawasaki shock syndrome.30 The who are resistant to IVIg, both COVID-19 in China.32 Our second existence of this syndrome, and the patients had elevations outside of the patient was given a course of overlap of cytokine expression in KD normal range typically observed with corticosteroids that similarly led to shock syndrome with COVID-19 and the disease.24 Moreover, neither significant improvement in her inflammatory response, could add to patient had sterile , which is symptoms, although she later had our understanding of both KD and a common finding in patients recurrence of her rash, which could COVID-19 inflammatory features on with KD.12 be due to immunologic phenomena a more fundamental, mechanistic relatedtoSARS-CoV-2infectionor level.33,34 Our patients were older than the could suggest persistent majority of patients diagnosed with inflammation from an acute CONCLUSIONS KD. Studies have shown that children inflammatory illness. Importantly, .5 years of age are more likely to this patient was not noted to have We describe 2 young patients with have delayed diagnosis and to any coronary artery abnormality on COVID-19 who had features

Downloaded from www.aappublications.org/news by guest on September 29, 2021 4 SPENCER et al suggestive of KD. Our patients had presentation of SARS-CoV-2 ABBREVIATIONS highly unusual but similar features, infection. andbothappearedtorespondto COVID-19: coronavirus disease treatment. We expect there are CSF: cerebrospinal fluid ACKNOWLEDGMENTS more patients with both classic KD IVIg: intravenous immunoglobulin features and coincident COVID-19 We are grateful to the patients and KD: Kawasaki disease as well as a potential novel their families for agreeing to be NT-ProBNP: N-terminal B-type COVID-19 inflammatory syndrome included in this article; to Drs Joshua natriuretic peptide that resembles KD. Better Milner, Eva Cheung, and Kara RT-PCR: reverse transcription characterization of these 2 Margolis for their contributions to the polymerase chain will be important for care of these patients and for their reaction formulating appropriate diagnostic review of this article; as well as to Dr SARS-CoV-2: severe acute and therapeutic guidelines. Further Julie Glickstein for her limitless respiratory syndrome research is needed to better energy and commitment to her coronavirus 2 understand this unique clinical pediatric cardiology fellows.

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright © 2020 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose. FUNDING: No external funding. POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

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Downloaded from www.aappublications.org/news by guest on September 29, 2021 COVID-19 Inflammatory Syndrome With Clinical Features Resembling Kawasaki Disease Robert Spencer, Ryan C. Closson, Mark Gorelik, Alexis D. Boneparth, Rebecca F. Hough, Karen P. Acker and Usha Krishnan Pediatrics 2020;146; DOI: 10.1542/peds.2020-1845 originally published online August 25, 2020;

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