Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 28, Number 3—March 2022
CME ACTIVITY - Research

Neutralizing Enterovirus D68 Antibodies in Children after 2014 Outbreak, Kansas City, Missouri, USA

Robyn A. Livingston1, Christopher J. Harrison1Comments to Author , and Rangaraj Selvarangan1
Author affiliation: Children’s Mercy Hospital Kansas City, Kansas City, Missouri, USA; University of Missouri, Kansas City

Main Article

Table 2

Low versus high neutralizing antibody titers for enterovirus D68 clades B1, B2, and D in serum collected in 2017 compared with titers previously reported from 2012–2013, from patients <18 years of age, Kansas City, Missouri, USA*

Group
Total
No. (%) patients
B1 clade virus
B2 clade virus
D clade virus
Serum obtained in 2017 300
Low titer† 0 110 (36.7) 66 (22.0)
High titer

300 (100)
190 (63.3)
234 (78.0)
Serum obtained in 2012–2013 (18) 273
Low titer† 54 (19.8) 117 (42.9) 133 (48.7)
High titer 219 (80.2) 156 (57.1) 140 (51.3)

*Antibody titers were measured by using the cell viability kit ATPlite (Perkin Elmer, http://www.perkinelmer.com). Seronegative patients are included. †Low neutralizing titer defined as <6 log2 (<1:64 titer).

Main Article

References
  1. Aliabadi  N, Messacar  K, Pastula  DM, Robinson  CC, Leshem  E, Sejvar  JJ, et al. Enterovirus D68 infection in children with acute flaccid myelitis, Colorado, USA, 2014. Emerg Infect Dis. 2016;22:138794. DOIPubMedGoogle Scholar
  2. Greninger  AL, Naccache  SN, Messacar  K, Clayton  A, Yu  G, Somasekar  S, et al. A novel outbreak enterovirus D68 strain associated with acute flaccid myelitis cases in the USA (2012-14): a retrospective cohort study. Lancet Infect Dis. 2015;15:67182. DOIPubMedGoogle Scholar
  3. Khetsuriani  N, Lamonte-Fowlkes  A, Oberst  S, Pallansch  MA; Centers for Disease Control and Prevention. Enterovirus surveillance—United States, 1970-2005. MMWR Surveill Summ. 2006;55:120.PubMedGoogle Scholar
  4. Schuster  JE, Miller  JO, Selvarangan  R, Weddle  G, Thompson  MT, Hassan  F, et al. Severe enterovirus 68 respiratory illness in children requiring intensive care management. J Clin Virol. 2015;70:7782. DOIPubMedGoogle Scholar
  5. Wang  H, Diaz  A, Moyer  K, Mele-Casas  M, Ara-Montojo  MF, Torrus  I, et al. Molecular and clinical comparison of enterovirus D68 outbreaks among hospitalized children, Ohio, USA, 2014 and 2018. Emerg Infect Dis. 2019;25:205563. DOIPubMedGoogle Scholar
  6. Oermann  CM, Schuster  JE, Conners  GP, Newland  JG, Selvarangan  R, Jackson  MA. Enterovirus d68. A focused review and clinical highlights from the 2014 U.S. Outbreak. Ann Am Thorac Soc. 2015;12:77581. DOIPubMedGoogle Scholar
  7. Park  SW, Pons-Salort  M, Messacar  K, Cook  C, Meyers  L, Farrar  J, et al. Epidemiological dynamics of enterovirus D68 in the United States and implications for acute flaccid myelitis. Sci Transl Med. 2021;13:eabd2400. DOIPubMedGoogle Scholar
  8. Midgley  CM, Watson  JT, Nix  WA, Curns  AT, Rogers  SL, Brown  BA, et al.; EV-D68 Working Group. Severe respiratory illness associated with a nationwide outbreak of enterovirus D68 in the USA (2014): a descriptive epidemiological investigation. Lancet Respir Med. 2015;3:87987. DOIPubMedGoogle Scholar
  9. Abedi  GR, Watson  JT, Nix  WA, Oberste  MS, Gerber  SI. Enterovirus and parechovirus surveillance—United States, 2014–2016. MMWR Morb Mortal Wkly Rep. 2018;67:5158. DOIPubMedGoogle Scholar
  10. Huang  W, Wang  G, Zhuge  J, Nolan  SM, Dimitrova  N, Fallon  JT. Whole-genome sequence analysis reveals the enterovirus D68 isolates during the United States 2014 outbreak mainly belong to a novel clade. Sci Rep. 2015;5:15223. DOIPubMedGoogle Scholar
  11. Tan  Y, Hassan  F, Schuster  JE, Simenauer  A, Selvarangan  R, Halpin  RA, et al. Molecular evolution and intraclade recombination of enterovirus D68 during the 2014 outbreak in the United States. J Virol. 2015;90:19972007. DOIPubMedGoogle Scholar
  12. Eshaghi  A, Duvvuri  VR, Isabel  S, Banh  P, Li  A, Peci  A, et al. Global distribution and evolutionary history of enterovirus D68, with emphasis on the 2014 outbreak in Ontario, Canada. Front Microbiol. 2017;8:257. DOIPubMedGoogle Scholar
  13. Kujawski  SA, Midgley  CM, Rha  B, Lively  JY, Nix  WA, Curns  AT, et al. Enterovirus D68–associated acute respiratory illness—New Vaccine Surveillance Network, United States, July–October, 2017 and 2018. MMWR Morb Mortal Wkly Rep. 2019;68:27780. DOIPubMedGoogle Scholar
  14. Pakala  SB, Tan  Y, Hassan  F, Mai  A, Markowitz  RH, Shilts  MH, et al. Nearly complete genome sequences of 17 enterovirus D68 strains from Kansas City, Missouri, 2018. Microbiol Resour Announc. 2019;8:e0038819. DOIPubMedGoogle Scholar
  15. Sun  S, Gao  F, Hu  Y, Bian  L, Wu  X, Su  Y, et al. A cross-sectional seroepidemiology study of EV-D68 in China. Emerg Microbes Infect. 2018;7:99. DOIPubMedGoogle Scholar
  16. Xiang  Z, Li  L, Ren  L, Guo  L, Xie  Z, Liu  C, et al. Seroepidemiology of enterovirus D68 infection in China. Emerg Microbes Infect. 2017;6:e32. DOIPubMedGoogle Scholar
  17. Sun  SY, Gao  F, Hu  YL, Bian  LL, Mao  QY, Wu  X, et al. Seroepidemiology of enterovirus D68 infection in infants and children in Jiangsu, China. J Infect. 2018;76:5639. DOIPubMedGoogle Scholar
  18. Liu  Y, Gong  C, Luo  M, Zhang  T, Li  M, Shen  L, et al. Seroepidemiology of enterovirus D68 in a healthy population in Beijing, China, between 2012 and 2017: a retrospective study. J Med Virol. 2020.PubMedGoogle Scholar
  19. Hu  YL, Huang  LM, Lu  CY, Fang  TY, Cheng  AL, Chang  LY. Manifestations of enterovirus D68 and high seroconversion among children attending a kindergarten. J Microbiol Immunol Infect. 2019;52:85864. DOIPubMedGoogle Scholar
  20. Karelehto  E, Koen  G, Benschop  K, van der Klis  F, Pajkrt  D, Wolthers  K. Enterovirus D68 serosurvey: evidence for endemic circulation in the Netherlands, 2006 to 2016. Euro Surveill. 2019;24:24. DOIPubMedGoogle Scholar
  21. Harrison  CJ, Weldon  WC, Pahud  BA, Jackson  MA, Oberste  MS, Selvarangan  R. Neutralizing antibody against enterovirus D68 in children and adults before 2014 outbreak, Kansas City, Missouri, USA. Emerg Infect Dis. 2019;25:5858. DOIPubMedGoogle Scholar
  22. Wallace  GS, Pahud  BA, Weldon  WC, Curns  AT, Oberste  MS, Harrison  CJ. Seroprevalence of poliovirus antibodies in the Kansas City metropolitan area, 2012-2013. Hum Vaccin Immunother. 2017;13:77683. DOIPubMedGoogle Scholar
  23. Weldon  WC, Oberste  MS, Pallansch  MA. Standardized methods for detection of poliovirus antibodies. In: Walker JM, editor. Methods in Molecular Biology. New York: Humana Press; 2016. p. 145–76.
  24. Schieble  JH, Fox  VL, Lennette  EH. A probable new human picornavirus associated with respiratory diseases. Am J Epidemiol. 1967;85:297310. DOIPubMedGoogle Scholar
  25. Oberste  MS, Maher  K, Schnurr  D, Flemister  MR, Lovchik  JC, Peters  H, et al. Enterovirus 68 is associated with respiratory illness and shares biological features with both the enteroviruses and the rhinoviruses. J Gen Virol. 2004;85:257784. DOIPubMedGoogle Scholar
  26. Kadji  FMN, Nishimura  H, Okamoto  M, Sato  K, Ohmiya  S, Ito  H, et al. Fluctuations in antibody titers against enterovirus D68 in pediatric sera collected in a community before, during, and after a possible outbreak. Jpn J Infect Dis. 2020;73:557. DOIPubMedGoogle Scholar
  27. Freeman  MC, Wells  AI, Ciomperlik-Patton  J, Myerburg  MM, Yang  L, Konopka-Anstadt  J, et al. Respiratory and intestinal epithelial cells exhibit differential susceptibility and innate immune responses to contemporary EV-D68 isolates. eLife. 2021;10:10. DOIPubMedGoogle Scholar
  28. Kamau  E, Harvala  H, Blomqvist  S, Nguyen  D, Horby  P, Pebody  R, et al. Increase in enterovirus D68 infections in young children, United Kingdom, 2006–2016. Emerg Infect Dis. 2019;25:12003. DOIPubMedGoogle Scholar
  29. Lee  JT, Shih  WL, Yen  TY, Cheng  AL, Lu  CY, Chang  LY, et al. Enterovirus D68 seroepidemiology in Taiwan, a cross sectional study from 2017. PLoS One. 2020;15:e0230180. DOIPubMedGoogle Scholar
  30. Looi  K, Buckley  AG, Rigby  PJ, Garratt  LW, Iosifidis  T, Zosky  GR, et al. Effects of human rhinovirus on epithelial barrier integrity and function in children with asthma. Clin Exp Allergy. 2018;48:51324. DOIPubMedGoogle Scholar
  31. Blanco  JC, Pletneva  LM, Wan  H, Araya  Y, Angel  M, Oue  RO, et al. Receptor characterization and susceptibility of cotton rats to avian and 2009 pandemic influenza virus strains. J Virol. 2013;87:203645. DOIPubMedGoogle Scholar
  32. Wang  SM, Liu  CC. Update of enterovirus 71 infection: epidemiology, pathogenesis and vaccine. Expert Rev Anti Infect Ther. 2014;12:44756. DOIPubMedGoogle Scholar
  33. Vogt  MR, Fu  J, Kose  N, Williamson  LE, Bombardi  R, Setliff  I, et al. Human antibodies neutralize enterovirus D68 and protect against infection and paralytic disease. Sci Immunol. 2020;5:eaba4902. DOIPubMedGoogle Scholar

Main Article

1All authors contributed equally to this article.

Page created: January 03, 2022
Page updated: February 18, 2022
Page reviewed: February 18, 2022
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external