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Abstract

Enteroviruses are a common cause of seasonal childhood infections. The vast majority of enterovirus infections are mild and self-limiting, although neonates can sometimes develop severe disease. Myocarditis is a rare complication of enterovirus infection. Between June 2022 and April 2023, twenty cases of severe neonatal enteroviral myocarditis caused by coxsackie B viruses were reported in the United Kingdom. Sixteen required critical care support and two died. Enterovirus PCR on whole blood was the most sensitive diagnostic test. We describe the initial public health investigation into this cluster and aim to raise awareness among paediatricians, laboratories and public health specialists.

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/content/10.2807/1560-7917.ES.2023.28.39.2300313
2023-09-28
2024-11-22
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2023.28.39.2300313
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References

  1. Sandoni M, Ciardo L, Tamburini C, Boncompagni A, Rossi C, Guidotti I, et al. Enteroviral infections in the first three months of life. Pathogens. 2022;11(1):60.  https://doi.org/10.3390/pathogens11010060  PMID: 35056008 
  2. United Kingdom Acute Flaccid Paralysis (AFP) Task Force. An increase in reports of acute flaccid paralysis (AFP) in the United Kingdom, 1 January 2018-21 January 2019: early findings. Euro Surveill. 2019;24(6):1900093. PMID: 30755296 
  3. Broberg EK, Simone B, Jansa J, EU/EEA Member State contributors. Upsurge in echovirus 30 detections in five EU/EEA countries, April to September, 2018. Euro Surveill. 2018;23(44):1800537.  https://doi.org/10.2807/1560-7917.ES.2018.23.44.1800537  PMID: 30401013 
  4. Grapin M, Mirand A, Pinquier D, Basset A, Bendavid M, Bisseux M, et al. Severe and fatal neonatal infections linked to a new variant of echovirus 11, France, July 2022 to April 2023. Euro Surveill. 2023;28(22):2300253.  https://doi.org/10.2807/1560-7917.ES.2023.28.22.2300253  PMID: 37261730 
  5. Chuang Y-Y, Huang Y-C. Enteroviral infection in neonates. J Microbiol Immunol Infect. 2019;52(6):851-7.  https://doi.org/10.1016/j.jmii.2019.08.018  PMID: 31607572 
  6. Ramachandra G, Shields L, Brown K, Ramnarayan P. The challenges of prompt identification and resuscitation in children with acute fulminant myocarditis: case series and review of the literature. J Paediatr Child Health. 2010;46(10):579-82.  https://doi.org/10.1111/j.1440-1754.2010.01799.x  PMID: 20626579 
  7. Freund MW, Kleinveld G, Krediet TG, van Loon AM, Verboon-Maciolek MA. Prognosis for neonates with enterovirus myocarditis. Arch Dis Child Fetal Neonatal Ed. 2010;95(3):F206-12.  https://doi.org/10.1136/adc.2009.165183  PMID: 20444813 
  8. Madden K, Thiagarajan RR, Rycus PT, Rajagopal SK. Survival of neonates with enteroviral myocarditis requiring extracorporeal membrane oxygenation. Pediatr Crit Care Med. 2011;12(3):314-8.  https://doi.org/10.1097/PCC.0b013e3181e8b44b  PMID: 20625340 
  9. Zhang M, Wang H, Tang J, He Y, Xiong T, Li W, et al. Clinical characteristics of severe neonatal enterovirus infection: a systematic review. BMC Pediatr. 2021;21(1):127.  https://doi.org/10.1186/s12887-021-02599-y  PMID: 33722228 
  10. Lugo D, Krogstad P. Enteroviruses in the early 21st century: new manifestations and challenges. Curr Opin Pediatr. 2016;28(1):107-13.  https://doi.org/10.1097/MOP.0000000000000303  PMID: 26709690 
  11. Ng KF, Gibb J, Struik S, Davis PJ, Muir P, Gillett C, et al. , Neonatal Enteroviral Myocarditis Consortium. Remember the heart: neonatal myocarditis. Arch Dis Child. 2023;108(5):417-9.  https://doi.org/10.1136/archdischild-2023-325316  PMID: 36854579 
  12. National Health Service Digital (NHS Digital). Hospital Episode Statistics (HES). Leeds: NHS Digital. [Accessed: 25 May 2023]. Available from: https://digital.nhs.uk/data-and-information/data-tools-and-services/data-services/hospital-episode-statistics
  13. World Health Organization (WHO). International Statistical Classification of Diseases and Related Health Problems 10th Revision (ICD-10 Version:2019). Geneva: WHO; 2019. Available from: https://icd.who.int/browse10/2019/en
  14. Corless CE, Guiver M, Borrow R, Edwards-Jones V, Fox AJ, Kaczmarski EB, et al. Development and evaluation of a ‘real-time’ RT-PCR for the detection of enterovirus and parechovirus RNA in CSF and throat swab samples. J Med Virol. 2002;67(4):555-62.  https://doi.org/10.1002/jmv.10138  PMID: 12116004 
  15. Nix WA, Oberste MS, Pallansch MA. Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol. 2006;44(8):2698-704.  https://doi.org/10.1128/JCM.00542-06  PMID: 16891480 
  16. National Center for Biotechnology Information (NCBI). Basic Local Alignment Search Tool (BLAST). Bethesda (MD): NCBI. [Accessed: 25 May 2023]. Available from: https://blast.ncbi.nlm.nih.gov/Blast.cgi
  17. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772-80.  https://doi.org/10.1093/molbev/mst010  PMID: 23329690 
  18. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Teeling E, editor. Mol Biol Evol. 2020;37(5):1530-4.
  19. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One. 2010;5(3):e9490.  https://doi.org/10.1371/journal.pone.0009490  PMID: 20224823 
  20. Office for National Statistics (ONS). Population estimates for the UK, England, Wales, Scotland and Northern Ireland: mid-2021. Newport: ONS. [Accessed: 23 Jun 2023]. Available from: https://www.ons.gov.uk/peoplepopulationandcommunity/populationandmigration/populationestimates/bulletins/annualmidyearpopulationestimates/mid2021#population-of-england-and-wales
  21. Kadambari S, Braccio S, Ribeiro S, Allen DJ, Pebody R, Brown D, et al. Enterovirus and parechovirus meningitis in infants younger than 90 days old in the UK and Republic of Ireland: a British Paediatric Surveillance Unit study. Arch Dis Child. 2019;104(6):552-7.  https://doi.org/10.1136/archdischild-2018-315643  PMID: 30530486 
  22. Chow EJ, Uyeki TM, Chu HY. The effects of the COVID-19 pandemic on community respiratory virus activity. Nat Rev Microbiol. 2023;21(3):195-210. PMID: 36253478 
  23. Cottrell S, Moore C, Perry M, Hilvers E, Williams C, Shankar AG. Prospective enterovirus D68 (EV-D68) surveillance from September 2015 to November 2018 indicates a current wave of activity in Wales. Euro Surveill. 2018;23(46):1800578.  https://doi.org/10.2807/1560-7917.ES.2018.23.46.1800578  PMID: 30458915 
  24. World Health Organization (WHO). Myocarditis - United Kingdom of Great Britain and Northern Ireland. Geneva: WHO. 17 May 2023. Available from: https://www.who.int/emergencies/disease-outbreak-news/item/2023-DON465
  25. UK Health Security Agency (UKHSA). Neonatal enteroviral myocarditis (NEM). London: UKHSA. 18 May 2023. Available from: https://www.gov.uk/government/collections/neonatal-enteroviral-myocarditis-nem
  26. de Graaf H, Pelosi E, Cooper A, Pappachan J, Sykes K, MacIntosh I, et al. Severe enterovirus infections in hospitalized children in the South of England: clinical phenotypes and causative genotypes. Pediatr Infect Dis J. 2016;35(7):723-7.  https://doi.org/10.1097/INF.0000000000001093  PMID: 26882165 
  27. Harvala H, Jasir A, Penttinen P, Pastore Celentano L, Greco D, Broberg E. Surveillance and laboratory detection for non-polio enteroviruses in the European Union/European Economic Area, 2016. Euro Surveill. 2017;22(45):16-00807.  https://doi.org/10.2807/1560-7917.ES.2017.22.45.16-00807  PMID: 29162204 
  28. Tebruegge M, Curtis N. Enterovirus infections in neonates. Semin Fetal Neonatal Med. 2009;14(4):222-7.  https://doi.org/10.1016/j.siny.2009.02.002  PMID: 19303380 
  29. Verma NA, Zheng XT, Harris MU, Cadichon SB, Melin-Aldana H, Khetsuriani N, et al. Outbreak of life-threatening coxsackievirus B1 myocarditis in neonates. Clin Infect Dis. 2009;49(5):759-63.  https://doi.org/10.1086/605089  PMID: 19622042 
  30. Cortina G, Best D, Deisenberg M, Chiletti R, Butt W. Extracorporeal membrane oxygenation for neonatal collapse caused by enterovirus myocarditis. Arch Dis Child Fetal Neonatal Ed. 2018;103(4):F370-6.  https://doi.org/10.1136/archdischild-2016-312429  PMID: 28970319 
Increased reports of severe myocarditis associated with enterovirus infection in neonates, United Kingdom, 27 June 2022 to 26 April 2023
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Anika+Singanayagam&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Singanayagam Anika</a>, <a href="/search?value1=Catherine+Moore&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Moore Catherine</a>, <a href="/search?value1=Susannah+Froude&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Froude Susannah</a>, <a href="/search?value1=Cristina+Celma&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Celma Cristina</a>, <a href="/search?value1=Julia+Stowe&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Stowe Julia</a>, <a href="/search?value1=Erjola+Hani&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Hani Erjola</a>, <a href="/search?value1=Khuen+Foong+Ng&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ng Khuen Foong</a>, <a href="/search?value1=Peter+Muir&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Muir Peter</a>, <a href="/search?value1=Marion+Roderick&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Roderick Marion</a>, <a href="/search?value1=Simon+Cottrell&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cottrell Simon</a>, <a href="/search?value1=David+F.+Bibby&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bibby David F.</a>, <a href="/search?value1=Barry+Vipond&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Vipond Barry</a>, <a href="/search?value1=Sophie+Gillett&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Gillett Sophie</a>, <a href="/search?value1=Peter+J.+Davis&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Davis Peter J.</a>, <a href="/search?value1=Jack+Gibb&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Gibb Jack</a>, <a href="/search?value1=Mai+Barry&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Barry Mai</a>, <a href="/search?value1=Phillippa+Harris&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Harris Phillippa</a>, <a href="/search?value1=Frances+Rowley&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rowley Frances</a>, <a href="/search?value1=Jiao+Song&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Song Jiao</a>, <a href="/search?value1=Ananda+Giri+Shankar&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Shankar Ananda Giri</a>, <a href="/search?value1=Danielle+McMichael&option1=author&noRedirect=true" class="nonDisambigAuthorLink">McMichael Danielle</a>, <a href="/search?value1=Jonathan+M.+Cohen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cohen Jonathan M.</a>, <a href="/search?value1=Abirami+Manian&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Manian Abirami</a>, <a href="/search?value1=Ciaran+Harvey&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Harvey Ciaran</a>, <a href="/search?value1=Louise+Shaw+Primrose&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Primrose Louise Shaw</a>, <a href="/search?value1=Stefanie+Wilson&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wilson Stefanie</a>, <a href="/search?value1=Declan+T.+Bradley&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bradley Declan T.</a>, <a href="/search?value1=Karthik+Paranthaman&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Paranthaman Karthik</a>, <a href="/search?value1=Stuart+Beard&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Beard Stuart</a>, <a href="/search?value1=Maria+Zambon&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Zambon Maria</a>, <a href="/search?value1=Mary+Ramsay&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ramsay Mary</a>, <a href="/search?value1=Vanessa+Saliba&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Saliba Vanessa</a>, <a href="/search?value1=Shamez+Ladhani&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ladhani Shamez</a>, <a href="/search?value1=Christopher+Williams&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Williams Christopher</a></span>. Increased reports of severe myocarditis associated with enterovirus infection in neonates, United Kingdom, 27 June 2022 to 26 April 2023. <a href="/content/ecdc">Euro Surveill.</a> 2023;28(39):pii=2300313. <a href="https://doi.org/10.2807/1560-7917.ES.2023.28.39.2300313" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2023.28.39.2300313</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 25 Jun 2023;&nbsp;&nbsp; <span class="generated">Accepted</span>: 27 Aug 2023 </span> </p>
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