Skip to main content
Top
Published in: European Journal of Pediatrics 7/2021

01-07-2021 | Shock | Review

Multisystem inflammatory syndrome in children related to COVID-19: a systematic review

Authors: Levi Hoste, Ruben Van Paemel, Filomeen Haerynck

Published in: European Journal of Pediatrics | Issue 7/2021

Login to get access

Abstract

An association between a novel pediatric hyperinflammatory condition and SARS-CoV-2 was recently published and termed pediatric inflammatory multisystem syndrome, temporally associated with SARS-CoV-2 (PIMS-TS) or multisystem inflammatory syndrome (in children) (MIS(-C)). We performed a systematic review and describe the epidemiological, clinical, and prognostic characteristics of 953 PIMS-TS/MIS(-C) cases in 68 records. Additionally, we studied the sensitivity of different case definitions that are currently applied. PIMS-TS/MIS(-C) presents at a median age of 8 years. Epidemiological enrichment for males (58.9%) and ethnic minorities (37.0% Black) is present. Apart from obesity (25.3%), comorbidities are rare. PIMS-TS/MIS(-C) is characterized by fever (99.4%), gastrointestinal (85.6%) and cardiocirculatory manifestations (79.3%), and increased inflammatory biomarkers. Nevertheless, 50.3% present respiratory symptoms as well. Over half of patients (56.3%) present with shock. The majority of the patients (73.3%) need intensive care treatment, including extracorporal membrane oxygenation (ECMO) in 3.8%. Despite severe disease, mortality is rather low (1.9%). Of the currently used case definitions, the WHO definition is preferred, as it is more precise, while encompassing most cases.
Conclusion: PIMS-TS/MIS(-C) is a severe, heterogeneous disease with epidemiological enrichment for males, adolescents, and racial and ethnic minorities. However, mortality rate is low and short-term outcome favorable. Long-term follow-up of chronic complications and additional clinical research to elucidate the underlying pathogenesis is crucial.
What is Known:
• A novel pediatric inflammatory syndrome with multisystem involvement has been described in association with SARS-CoV-2.
• To date, the scattered reporting of cases and use of different case definitions provides insufficient insight in the full clinical spectrum, epidemiological and immunological features, and prognosis.
What is New:
• This systematic review illustrates the heterogeneous spectrum of PIMS-TS/MIS(-C) and its epidemiological enrichment for males, adolescents, and racial and ethnic minorities.
• Despite its severe presentation, overall short-term outcome is good.
• The WHO MIS definition is preferred, as it is more precise, while encompassing most cases.
Appendix
Available only for authorised users
Literature
13.
go back to reference Feldstein LR, Rose EB, Horwitz SM, Collins JP, Newhams MM, Son MBF, Newburger JW, Kleinman LC, Heidemann SM, Martin AA, Singh AR, Li S, Tarquinio KM, Jaggi P, Oster ME, Zackai SP, Gillen J, Ratner AJ, Walsh RF, Fitzgerald JC, Keenaghan MA, Alharash H, Doymaz S, Clouser KN, Giuliano JS Jr, Gupta A, Parker RM, Maddux AB, Havalad V, Ramsingh S, Bukulmez H, Bradford TT, Smith LS, Tenforde MW, Carroll CL, Riggs BJ, Gertz SJ, Daube A, Lansell A, Coronado Munoz A, Hobbs CV, Marohn KL, Halasa NB, Patel MM, Randolph AG, Overcoming COVID-19 Investigators, CDC COVID-19 Response Team (2020) Multisystem inflammatory syndrome in U.S. children and adolescents. N Engl J Med 383:334–346. https://doi.org/10.1056/NEJMoa2021680CrossRefPubMed Feldstein LR, Rose EB, Horwitz SM, Collins JP, Newhams MM, Son MBF, Newburger JW, Kleinman LC, Heidemann SM, Martin AA, Singh AR, Li S, Tarquinio KM, Jaggi P, Oster ME, Zackai SP, Gillen J, Ratner AJ, Walsh RF, Fitzgerald JC, Keenaghan MA, Alharash H, Doymaz S, Clouser KN, Giuliano JS Jr, Gupta A, Parker RM, Maddux AB, Havalad V, Ramsingh S, Bukulmez H, Bradford TT, Smith LS, Tenforde MW, Carroll CL, Riggs BJ, Gertz SJ, Daube A, Lansell A, Coronado Munoz A, Hobbs CV, Marohn KL, Halasa NB, Patel MM, Randolph AG, Overcoming COVID-19 Investigators, CDC COVID-19 Response Team (2020) Multisystem inflammatory syndrome in U.S. children and adolescents. N Engl J Med 383:334–346. https://​doi.​org/​10.​1056/​NEJMoa2021680CrossRefPubMed
14.
go back to reference Dufort EM, Koumans EH, Chow EJ, Rosenthal EM, Muse A, Rowlands J, Barranco MA, Maxted AM, Rosenberg ES, Easton D, Udo T, Kumar J, Pulver W, Smith L, Hutton B, Blog D, Zucker H, New York State and Centers for Disease Control and Prevention Multisystem Inflammatory Syndrome in Children Investigation Team (2020) Multisystem inflammatory syndrome in children in New York state. N Engl J Med 383:347–358. https://doi.org/10.1056/NEJMoa2021756CrossRefPubMed Dufort EM, Koumans EH, Chow EJ, Rosenthal EM, Muse A, Rowlands J, Barranco MA, Maxted AM, Rosenberg ES, Easton D, Udo T, Kumar J, Pulver W, Smith L, Hutton B, Blog D, Zucker H, New York State and Centers for Disease Control and Prevention Multisystem Inflammatory Syndrome in Children Investigation Team (2020) Multisystem inflammatory syndrome in children in New York state. N Engl J Med 383:347–358. https://​doi.​org/​10.​1056/​NEJMoa2021756CrossRefPubMed
15.
go back to reference Whittaker E, Bamford A, Kenny J, Kaforou M, Jones CE, Shah P, Ramnarayan P, Fraisse A, Miller O, Davies P, Kucera F, Brierley J, McDougall M, Carter M, Tremoulet A, Shimizu C, Herberg J, Burns JC, Lyall H, Levin M, for the PIMS-TS Study Group and EUCLIDS and PERFORM Consortia (2020) Clinical characteristics of 58 children with a pediatric inflammatory multisystem syndrome temporally associated with SARS-CoV-2. JAMA - J Am Med Assoc 324:259–269. https://doi.org/10.1001/jama.2020.10369CrossRef Whittaker E, Bamford A, Kenny J, Kaforou M, Jones CE, Shah P, Ramnarayan P, Fraisse A, Miller O, Davies P, Kucera F, Brierley J, McDougall M, Carter M, Tremoulet A, Shimizu C, Herberg J, Burns JC, Lyall H, Levin M, for the PIMS-TS Study Group and EUCLIDS and PERFORM Consortia (2020) Clinical characteristics of 58 children with a pediatric inflammatory multisystem syndrome temporally associated with SARS-CoV-2. JAMA - J Am Med Assoc 324:259–269. https://​doi.​org/​10.​1001/​jama.​2020.​10369CrossRef
19.
go back to reference World Health Organization (WHO) (2020) Multisystem inflammatory syndrome in children and adolescents with COVID-19. 1–3 World Health Organization (WHO) (2020) Multisystem inflammatory syndrome in children and adolescents with COVID-19. 1–3
22.
go back to reference Sackett DL (1989) Rules of evidence and clinical recommendations on the use of antithrombotic agents. Chest 95:2S–4SCrossRefPubMed Sackett DL (1989) Rules of evidence and clinical recommendations on the use of antithrombotic agents. Chest 95:2S–4SCrossRefPubMed
27.
go back to reference Rostad CA, Chahroudi A, Mantus G, Lapp SA, Teherani M, Macoy L, Tarquinio KM, Basu RK, Kao C, Linam WM, Zimmerman MG, Shi PY, Menachery VD, Oster ME, Edupuganti S, Anderson EJ, Suthar MS, Wrammert J, Jaggi P (2020) Quantitative SARS-CoV-2 serology in children with multisystem inflammatory syndrome (MIS-C). Pediatrics 146:e2020018242. https://doi.org/10.1542/peds.2020-018242CrossRefPubMed Rostad CA, Chahroudi A, Mantus G, Lapp SA, Teherani M, Macoy L, Tarquinio KM, Basu RK, Kao C, Linam WM, Zimmerman MG, Shi PY, Menachery VD, Oster ME, Edupuganti S, Anderson EJ, Suthar MS, Wrammert J, Jaggi P (2020) Quantitative SARS-CoV-2 serology in children with multisystem inflammatory syndrome (MIS-C). Pediatrics 146:e2020018242. https://​doi.​org/​10.​1542/​peds.​2020-018242CrossRefPubMed
28.
go back to reference Weisberg SP, Connors TJ, Zhu Y, Baldwin MR, Lin WH, Wontakal S, Szabo PA, Wells SB, Dogra P, Gray J, Idzikowski E, Stelitano D, Bovier FT, Davis-Porada J, Matsumoto R, Poon MML, Chait M, Mathieu C, Horvat B, Decimo D, Hudson KE, Zotti FD, Bitan ZC, la Carpia F, Ferrara SA, Mace E, Milner J, Moscona A, Hod E, Porotto M, Farber DL (2021) Distinct antibody responses to SARS-CoV-2 in children and adults across the COVID-19 clinical spectrum. Nat Immunol 22:25–31. https://doi.org/10.1038/s41590-020-00826-9CrossRefPubMed Weisberg SP, Connors TJ, Zhu Y, Baldwin MR, Lin WH, Wontakal S, Szabo PA, Wells SB, Dogra P, Gray J, Idzikowski E, Stelitano D, Bovier FT, Davis-Porada J, Matsumoto R, Poon MML, Chait M, Mathieu C, Horvat B, Decimo D, Hudson KE, Zotti FD, Bitan ZC, la Carpia F, Ferrara SA, Mace E, Milner J, Moscona A, Hod E, Porotto M, Farber DL (2021) Distinct antibody responses to SARS-CoV-2 in children and adults across the COVID-19 clinical spectrum. Nat Immunol 22:25–31. https://​doi.​org/​10.​1038/​s41590-020-00826-9CrossRefPubMed
29.
go back to reference Swann OV, Holden KA, Turtle L, Pollock L, Fairfield CJ, Drake TM, Seth S, Egan C, Hardwick HE, Halpin S, Girvan M, Donohue C, Pritchard M, Patel LB, Ladhani S, Sigfrid L, Sinha IP, Olliaro PL, Nguyen-van-Tam JS, Horby PW, Merson L, Carson G, Dunning J, Openshaw PJM, Baillie JK, Harrison EM, Docherty AB, Semple MG (2020) Clinical characteristics of children and young people admitted to hospital with covid-19 in United Kingdom: prospective multicentre observational cohort study. BMJ 370:m3249. https://doi.org/10.1136/bmj.m3249CrossRefPubMed Swann OV, Holden KA, Turtle L, Pollock L, Fairfield CJ, Drake TM, Seth S, Egan C, Hardwick HE, Halpin S, Girvan M, Donohue C, Pritchard M, Patel LB, Ladhani S, Sigfrid L, Sinha IP, Olliaro PL, Nguyen-van-Tam JS, Horby PW, Merson L, Carson G, Dunning J, Openshaw PJM, Baillie JK, Harrison EM, Docherty AB, Semple MG (2020) Clinical characteristics of children and young people admitted to hospital with covid-19 in United Kingdom: prospective multicentre observational cohort study. BMJ 370:m3249. https://​doi.​org/​10.​1136/​bmj.​m3249CrossRefPubMed
33.
go back to reference Rodriguez-Gonzalez M, Sanchez-Codez M, Gutierrez-Rosa I, Castellano-Martinez A, Rodriguez-Benitez AR-CP (2020) New onset severe right ventricular failure associated with COVID-19 in a young infant without previous heart disease. Cardiol Young:1–4. https://doi.org/10.1017/S1047951120001857 Rodriguez-Gonzalez M, Sanchez-Codez M, Gutierrez-Rosa I, Castellano-Martinez A, Rodriguez-Benitez AR-CP (2020) New onset severe right ventricular failure associated with COVID-19 in a young infant without previous heart disease. Cardiol Young:1–4. https://​doi.​org/​10.​1017/​S104795112000185​7
35.
go back to reference Dasgupta K, Finch S (2020) A case of pediatric multisystem inflammatory syndrome temporally associated with COVID-19 in South Dakota. S D Med 73:246–251PubMed Dasgupta K, Finch S (2020) A case of pediatric multisystem inflammatory syndrome temporally associated with COVID-19 in South Dakota. S D Med 73:246–251PubMed
41.
go back to reference Balasubramanian S, Nagendran TM, Ramachandran B, Ramanan AV (2020) Hyper-inflammatory syndrome in a child with COVID-19 treated successfully with intravenous immunoglobulin and tocilizumab. Indian Pediatr 57:681–683CrossRefPubMedPubMedCentral Balasubramanian S, Nagendran TM, Ramachandran B, Ramanan AV (2020) Hyper-inflammatory syndrome in a child with COVID-19 treated successfully with intravenous immunoglobulin and tocilizumab. Indian Pediatr 57:681–683CrossRefPubMedPubMedCentral
45.
go back to reference Bahrami A, Vafapour M, Moazzami B, Rezaei N (2020) Hyperinflammatory shock related to COVID-19 in a patient presenting with multisystem inflammatory syndrome in children: first case from Iran. J Paediatr Child Health. https://doi.org/10.1111/jpc.15048 Bahrami A, Vafapour M, Moazzami B, Rezaei N (2020) Hyperinflammatory shock related to COVID-19 in a patient presenting with multisystem inflammatory syndrome in children: first case from Iran. J Paediatr Child Health. https://​doi.​org/​10.​1111/​jpc.​15048
59.
go back to reference Belhadjer Z, Méot M, Bajolle F, Khraiche D, Legendre A, Abakka S, Auriau J, Grimaud M, Oualha M, Beghetti M, Wacker J, Ovaert C, Hascoet S, Selegny M, Malekzadeh-Milani S, Maltret A, Bosser G, Giroux N, Bonnemains L, Bordet J, di Filippo S, Mauran P, Falcon-Eicher S, Thambo JB, Lefort B, Moceri P, Houyel L, Renolleau S, Bonnet D (2020) Acute heart failure in multisystem inflammatory syndrome in children (MIS-C) in the context of global SARS-CoV-2 pandemic. Circulation. 142:429–436. https://doi.org/10.1161/CIRCULATIONAHA.120.048360CrossRefPubMed Belhadjer Z, Méot M, Bajolle F, Khraiche D, Legendre A, Abakka S, Auriau J, Grimaud M, Oualha M, Beghetti M, Wacker J, Ovaert C, Hascoet S, Selegny M, Malekzadeh-Milani S, Maltret A, Bosser G, Giroux N, Bonnemains L, Bordet J, di Filippo S, Mauran P, Falcon-Eicher S, Thambo JB, Lefort B, Moceri P, Houyel L, Renolleau S, Bonnet D (2020) Acute heart failure in multisystem inflammatory syndrome in children (MIS-C) in the context of global SARS-CoV-2 pandemic. Circulation. 142:429–436. https://​doi.​org/​10.​1161/​CIRCULATIONAHA.​120.​048360CrossRefPubMed
61.
go back to reference Toubiana J, Poirault C, Corsia A, Bajolle F, Fourgeaud J, Angoulvant F, Debray A, Basmaci R, Salvador E, Biscardi S, Frange P, Chalumeau M, Casanova JL, Cohen JF, Allali S (2020) Kawasaki-like multisystem inflammatory syndrome in children during the covid-19 pandemic in Paris, France: prospective observational study. BMJ 369:m2094. https://doi.org/10.1136/bmj.m2094CrossRefPubMedPubMedCentral Toubiana J, Poirault C, Corsia A, Bajolle F, Fourgeaud J, Angoulvant F, Debray A, Basmaci R, Salvador E, Biscardi S, Frange P, Chalumeau M, Casanova JL, Cohen JF, Allali S (2020) Kawasaki-like multisystem inflammatory syndrome in children during the covid-19 pandemic in Paris, France: prospective observational study. BMJ 369:m2094. https://​doi.​org/​10.​1136/​bmj.​m2094CrossRefPubMedPubMedCentral
62.
64.
go back to reference Pouletty M, Borocco C, Ouldali N, Caseris M, Basmaci R, Lachaume N, Bensaid P, Pichard S, Kouider H, Morelle G, Craiu I, Pondarre C, Deho A, Maroni A, Oualha M, Amoura Z, Haroche J, Chommeloux J, Bajolle F, Beyler C, Bonacorsi S, Carcelain G, Koné-Paut I, Bader-Meunier B, Faye A, Meinzer U, Galeotti C, Melki I (2020) Paediatric multisystem inflammatory syndrome temporally associated with SARS-CoV-2 mimicking Kawasaki disease (Kawa-COVID-19): A multicentre cohort. Ann Rheum Dis 79:999–1006. https://doi.org/10.1136/annrheumdis-2020-217960CrossRefPubMed Pouletty M, Borocco C, Ouldali N, Caseris M, Basmaci R, Lachaume N, Bensaid P, Pichard S, Kouider H, Morelle G, Craiu I, Pondarre C, Deho A, Maroni A, Oualha M, Amoura Z, Haroche J, Chommeloux J, Bajolle F, Beyler C, Bonacorsi S, Carcelain G, Koné-Paut I, Bader-Meunier B, Faye A, Meinzer U, Galeotti C, Melki I (2020) Paediatric multisystem inflammatory syndrome temporally associated with SARS-CoV-2 mimicking Kawasaki disease (Kawa-COVID-19): A multicentre cohort. Ann Rheum Dis 79:999–1006. https://​doi.​org/​10.​1136/​annrheumdis-2020-217960CrossRefPubMed
65.
go back to reference Ramcharan T, Nolan O, Lai CY et al (2020) Paediatric inflammatory multisystem syndrome: temporally associated with SARS-CoV-2 (PIMS-TS): cardiac features, management and short-term outcomes at a UK tertiary paediatric hospital. Pediatr Cardiol:1–11. https://doi.org/10.1007/s00246-020-02391-2 Ramcharan T, Nolan O, Lai CY et al (2020) Paediatric inflammatory multisystem syndrome: temporally associated with SARS-CoV-2 (PIMS-TS): cardiac features, management and short-term outcomes at a UK tertiary paediatric hospital. Pediatr Cardiol:1–11. https://​doi.​org/​10.​1007/​s00246-020-02391-2
66.
78.
go back to reference Davies P, Evans C, Kanthimathinathan HK, Lillie J, Brierley J, Waters G, Johnson M, Griffiths B, du Pré P, Mohammad Z, Deep A, Playfor S, Singh D, Inwald D, Jardine M, Ross O, Shetty N, Worrall M, Sinha R, Koul A, Whittaker E, Vyas H, Scholefield BR, Ramnarayan P (2020) Intensive care admissions of children with paediatric inflammatory multisystem syndrome temporally associated with SARS-CoV-2 (PIMS-TS) in the UK: a multicentre observational study. Lancet Child Adolesc Health 4:669–677. https://doi.org/10.1016/S2352-4642(20)30215-7CrossRefPubMedPubMedCentral Davies P, Evans C, Kanthimathinathan HK, Lillie J, Brierley J, Waters G, Johnson M, Griffiths B, du Pré P, Mohammad Z, Deep A, Playfor S, Singh D, Inwald D, Jardine M, Ross O, Shetty N, Worrall M, Sinha R, Koul A, Whittaker E, Vyas H, Scholefield BR, Ramnarayan P (2020) Intensive care admissions of children with paediatric inflammatory multisystem syndrome temporally associated with SARS-CoV-2 (PIMS-TS) in the UK: a multicentre observational study. Lancet Child Adolesc Health 4:669–677. https://​doi.​org/​10.​1016/​S2352-4642(20)30215-7CrossRefPubMedPubMedCentral
81.
go back to reference Lee PY, Day-Lewis M, Henderson LA, Friedman KG, Lo J, Roberts JE, Lo MS, Platt CD, Chou J, Hoyt KJ, Baker AL, Banzon TM, Chang MH, Cohen E, de Ferranti SD, Dionne A, Habiballah S, Halyabar O, Hausmann JS, Hazen MM, Janssen E, Meidan E, Nelson RW, Nguyen AA, Sundel RP, Dedeoglu F, Nigrovic PA, Newburger JW, Son MBF (2020) Distinct clinical and immunological features of SARS-COV-2-induced multisystem inflammatory syndrome in children. J Clin Invest 130:5942–5950. https://doi.org/10.1172/JCI141113CrossRefPubMedPubMedCentral Lee PY, Day-Lewis M, Henderson LA, Friedman KG, Lo J, Roberts JE, Lo MS, Platt CD, Chou J, Hoyt KJ, Baker AL, Banzon TM, Chang MH, Cohen E, de Ferranti SD, Dionne A, Habiballah S, Halyabar O, Hausmann JS, Hazen MM, Janssen E, Meidan E, Nelson RW, Nguyen AA, Sundel RP, Dedeoglu F, Nigrovic PA, Newburger JW, Son MBF (2020) Distinct clinical and immunological features of SARS-COV-2-induced multisystem inflammatory syndrome in children. J Clin Invest 130:5942–5950. https://​doi.​org/​10.​1172/​JCI141113CrossRefPubMedPubMedCentral
82.
go back to reference Moraleda C, Serna-Pascual M, Soriano-Arandes A, Simó S, Epalza C, Santos M, Grasa C, Rodríguez M, Soto B, Gallego N, Ruiz Y, Urretavizcaya-Martínez M, Pareja M, Sanz-Santaeufemia FJ, Fumadó V, Lanaspa M, Jordan I, Prieto L, Belda S, Toral-Vázquez B, Rincón E, Gil-Villanueva N, Méndez-Echevarría A, Castillo-Serrano A, Rivière JG, Soler-Palacín P, Rojo P, Tagarro A, EPICO-AEP Working Group (2020) Multi-inflammatory syndrome in children related to SARS-CoV-2 in Spain. Clin Infect Dis. https://doi.org/10.1093/cid/ciaa1042 Moraleda C, Serna-Pascual M, Soriano-Arandes A, Simó S, Epalza C, Santos M, Grasa C, Rodríguez M, Soto B, Gallego N, Ruiz Y, Urretavizcaya-Martínez M, Pareja M, Sanz-Santaeufemia FJ, Fumadó V, Lanaspa M, Jordan I, Prieto L, Belda S, Toral-Vázquez B, Rincón E, Gil-Villanueva N, Méndez-Echevarría A, Castillo-Serrano A, Rivière JG, Soler-Palacín P, Rojo P, Tagarro A, EPICO-AEP Working Group (2020) Multi-inflammatory syndrome in children related to SARS-CoV-2 in Spain. Clin Infect Dis. https://​doi.​org/​10.​1093/​cid/​ciaa1042
83.
go back to reference Diorio C, Henrickson SE, Vella LA, McNerney KO, Chase J, Burudpakdee C, Lee JH, Jasen C, Balamuth F, Barrett DM, Banwell BL, Bernt KM, Blatz AM, Chiotos K, Fisher BT, Fitzgerald JC, Gerber JS, Gollomp K, Gray C, Grupp SA, Harris RM, Kilbaugh TJ, John ARO, Lambert M, Liebling EJ, Paessler ME, Petrosa W, Phillips C, Reilly AF, Romberg ND, Seif A, Sesok-Pizzini DA, Sullivan KE, Vardaro J, Behrens EM, Teachey DT, Bassiri H (2020) Multisystem inflammatory syndrome in children and COVID-19 are distinct presentations of SARS-CoV-2. J Clin Invest 130:5967–5975. https://doi.org/10.1172/JCI140970CrossRefPubMedPubMedCentral Diorio C, Henrickson SE, Vella LA, McNerney KO, Chase J, Burudpakdee C, Lee JH, Jasen C, Balamuth F, Barrett DM, Banwell BL, Bernt KM, Blatz AM, Chiotos K, Fisher BT, Fitzgerald JC, Gerber JS, Gollomp K, Gray C, Grupp SA, Harris RM, Kilbaugh TJ, John ARO, Lambert M, Liebling EJ, Paessler ME, Petrosa W, Phillips C, Reilly AF, Romberg ND, Seif A, Sesok-Pizzini DA, Sullivan KE, Vardaro J, Behrens EM, Teachey DT, Bassiri H (2020) Multisystem inflammatory syndrome in children and COVID-19 are distinct presentations of SARS-CoV-2. J Clin Invest 130:5967–5975. https://​doi.​org/​10.​1172/​JCI140970CrossRefPubMedPubMedCentral
85.
go back to reference Dhanalakshmi K, Balasubramanian S, Madhusudan M et al (2020) Epidemiological and clinical profile of pediatric inflammatory multisystem syndrome - temporally associated with SARS-CoV-2 (PIMS-TS) in Indian children. Indian Pediatr 57:1010–1014CrossRefPubMedPubMedCentral Dhanalakshmi K, Balasubramanian S, Madhusudan M et al (2020) Epidemiological and clinical profile of pediatric inflammatory multisystem syndrome - temporally associated with SARS-CoV-2 (PIMS-TS) in Indian children. Indian Pediatr 57:1010–1014CrossRefPubMedPubMedCentral
86.
go back to reference Capone CA, Subramony A, Sweberg T, Schneider J, Shah S, Rubin L, Schleien C, Northwell Health COVID-19 Research Consortium, Epstein S, Johnson JC, Kessel A, Misra N, Mitchell E, Palumbo N, Rajan S, Rocker J, Williamson K, Davidson KW (2020) Characteristics, cardiac involvement, and outcomes of multisystem inflammatory disease of childhood (MIS-C) associated with SARS-CoV-2 infection. J Pediatr 224:141–145. https://doi.org/10.1016/j.jpeds.2020.06.044CrossRefPubMedPubMedCentral Capone CA, Subramony A, Sweberg T, Schneider J, Shah S, Rubin L, Schleien C, Northwell Health COVID-19 Research Consortium, Epstein S, Johnson JC, Kessel A, Misra N, Mitchell E, Palumbo N, Rajan S, Rocker J, Williamson K, Davidson KW (2020) Characteristics, cardiac involvement, and outcomes of multisystem inflammatory disease of childhood (MIS-C) associated with SARS-CoV-2 infection. J Pediatr 224:141–145. https://​doi.​org/​10.​1016/​j.​jpeds.​2020.​06.​044CrossRefPubMedPubMedCentral
88.
go back to reference Gupta A, Madhavan MV, Sehgal K, Nair N, Mahajan S, Sehrawat TS, Bikdeli B, Ahluwalia N, Ausiello JC, Wan EY, Freedberg DE, Kirtane AJ, Parikh SA, Maurer MS, Nordvig AS, Accili D, Bathon JM, Mohan S, Bauer KA, Leon MB, Krumholz HM, Uriel N, Mehra MR, Elkind MSV, Stone GW, Schwartz A, Ho DD, Bilezikian JP, Landry DW (2020) Extrapulmonary manifestations of COVID-19. Nat Med 26:1017–1032. https://doi.org/10.1038/s41591-020-0968-3CrossRefPubMed Gupta A, Madhavan MV, Sehgal K, Nair N, Mahajan S, Sehrawat TS, Bikdeli B, Ahluwalia N, Ausiello JC, Wan EY, Freedberg DE, Kirtane AJ, Parikh SA, Maurer MS, Nordvig AS, Accili D, Bathon JM, Mohan S, Bauer KA, Leon MB, Krumholz HM, Uriel N, Mehra MR, Elkind MSV, Stone GW, Schwartz A, Ho DD, Bilezikian JP, Landry DW (2020) Extrapulmonary manifestations of COVID-19. Nat Med 26:1017–1032. https://​doi.​org/​10.​1038/​s41591-020-0968-3CrossRefPubMed
102.
go back to reference Poissy J, Goutay J, Caplan M, Parmentier E, Duburcq T, Lassalle F, Jeanpierre E, Rauch A, Labreuche J, Susen S, Cousin N, Durand A, el Kalioubie A, Favory R, Girardie P, Houard M, Jaillette E, Jourdain M, Ledoux G, Mathieu D, Moreau AS, Niles C, Nseir S, Onimus T, Préau S, Robriquet L, Rouzé A, Simonnet A, Six S, Toussaint A, Dupont A, Bauters A, Zawadzki C, Paris C, Trillot N, Wibaut B, Hochart A, Marichez C, Dalibard V, Vanderziepe S, Bourgeois L, Gaul A, Jospin A, Stepina N, Pradines B, Tournoys A, Brousseau T, Rémy M, Hutt A (2020) Pulmonary embolism in patients with COVID-19: awareness of an increased prevalence. Circulation 142:184–186CrossRefPubMed Poissy J, Goutay J, Caplan M, Parmentier E, Duburcq T, Lassalle F, Jeanpierre E, Rauch A, Labreuche J, Susen S, Cousin N, Durand A, el Kalioubie A, Favory R, Girardie P, Houard M, Jaillette E, Jourdain M, Ledoux G, Mathieu D, Moreau AS, Niles C, Nseir S, Onimus T, Préau S, Robriquet L, Rouzé A, Simonnet A, Six S, Toussaint A, Dupont A, Bauters A, Zawadzki C, Paris C, Trillot N, Wibaut B, Hochart A, Marichez C, Dalibard V, Vanderziepe S, Bourgeois L, Gaul A, Jospin A, Stepina N, Pradines B, Tournoys A, Brousseau T, Rémy M, Hutt A (2020) Pulmonary embolism in patients with COVID-19: awareness of an increased prevalence. Circulation 142:184–186CrossRefPubMed
Metadata
Title
Multisystem inflammatory syndrome in children related to COVID-19: a systematic review
Authors
Levi Hoste
Ruben Van Paemel
Filomeen Haerynck
Publication date
01-07-2021
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Pediatrics / Issue 7/2021
Print ISSN: 0340-6199
Electronic ISSN: 1432-1076
DOI
https://doi.org/10.1007/s00431-021-03993-5

Other articles of this Issue 7/2021

European Journal of Pediatrics 7/2021 Go to the issue