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Volume 21, Number 9—September 2015
THEME ISSUE
Emerging Infections Program
Emerging Infections Program

Improving Accuracy of Influenza-Associated Hospitalization Rate Estimates

Alexander J. MillmanComments to Author , Carrie Reed, Pam Daily Kirley, Deborah Aragon, James I. Meek, Monica M. Farley, Patricia Ryan, Jim Collins, Ruth Lynfield, Joan Baumbach, Shelley Zansky, Nancy M. Bennett, Brian Fowler, Ann Thomas, Mary L. Lindegren, Annette Atkinson, Lyn Finelli, and Sandra Chaves
Author affiliations: Centers for Disease Control and Prevention, Atlanta, Georgia, USA (A.J. Millman, C. Reed, L. Finelli, S.S. Chaves); California Emerging Infections Program, Oakland, California, USA (P. Daily Kirley); Colorado Department of Public Health and Environment, Denver, Colorado, USA (D. Aragon); Connecticut Emerging Infections Program, New Haven, Connecticut, USA (J. Meek); Emory University School of Medicine, Atlanta (M.M. Farley); Atlanta Veterans Administration Medical Center, Atlanta (M.M. Farley); Maryland Department of Health and Mental Hygiene, Baltimore, Maryland, USA (P. Ryan); Michigan Department of Health and Human Services, Lansing, Michigan, USA (J. Collins); Minnesota Department of Health, St. Paul, Minnesota, USA (R. Lynfield); New Mexico Department of Health, Santa Fe, New Mexico, USA (J. Baumbach); New York State Department of Health, Albany, New York, USA (S. Zansky); University of Rochester School of Medicine and Dentistry, Rochester, New York, USA (N.M. Bennett); Monroe County Department of Public Health, Rochester (N.M. Bennett); Ohio Department of Health, Columbus, Ohio, USA (B. Fowler); Oregon Public Health Division, Portland, Oregon, USA (A. Thomas); Vanderbilt University School of Medicine, Nashville, Tennessee, USA (M.L. Lindegren); Utah Department of Health, Salt Lake City, Utah, USA (A. Atkinson)

Main Article

Table

Influenza diagnostic test sensitivity range, by patient age group (years), FluSurv-NET, 2003–2013*

Diagnostic test/patient age group, y Range from literature review, % References Bootstrap estimate (95% CI)
RT-PCR
0–17 79.2–100 (19,2124) 95.0 (82–98.7)
18–64 79.2–100 (19,2123) 94.1 (81.1–98.7)
>65 79.2–93 (19,21,25) 86.1 (79.6–92.7)
Culture
0–17 45–100 (4,19,24,26) 69.3 (48.3–95.9)
18–64 45–100 (4,19,26) 72.8 (47.2–96.3)
>65 19.4–53.8 (8,25) 36.2 (20.3–52.1)
DFA
0–17 45–90 (24,2730) 70.9 (46.8–86.6)
18–64 53–84.2 (27,28) 68.0 (53.8–83.4)
>65 53–84.2 (27,28) 68.0 (53.8–83.4)
RIDT
0–17 61.6–71.7 (7) 66.7 (61.3–71.7)
18–64 47.7–59.8 (7) 53.9 (47.8–59.8)
>65 8–43 (8,17,25,31) 20.1 (8.8–41.4)

*DFA, direct fluorescent antibody; FluSurv-NET, Centers for Disease Control and Prevention Influenza Hospital Surveillance Network; RIDT, rapid influenza diagnostic test; RT-PCR, reverse transcription PCR.

Main Article

References
  1. Dao  CN, Kamimoto  L, Nowell  M, Reingold  A, Gershman  K, Meek  J, Adult hospitalizations for laboratory-positive influenza during the 2005–2006 through 2007–2008 seasons in the United States. J Infect Dis. 2010;202:8818. DOIPubMedGoogle Scholar
  2. Dawood  FS, Fiore  A, Kamimoto  L, Bramley  A, Reingold  A, Gershman  K, Burden of seasonal influenza hospitalization in children, United States, 2003 to 2008. J Pediatr. 2010;157:80814. DOIPubMedGoogle Scholar
  3. Chaves  SS, Aragon  D, Bennett  N, Cooper  T, D'Mello  T, Farley  M, Patients hospitalized with laboratory-confirmed influenza during the 2010–2011 influenza season: exploring disease severity by virus type and subtype. J Infect Dis. 2013;208:130514. DOIPubMedGoogle Scholar
  4. Takahashi  H, Otsuka  Y, Patterson  BK. Diagnostic tests for influenza and other respiratory viruses: determining performance specifications based on clinical setting. J Infect Chemother. 2010;16:15561. DOIPubMedGoogle Scholar
  5. Jernigan  DB, Lindstrom  SL, Johnson  JR, Miller  JD, Hoelscher  M, Humes  R, Detecting 2009 pandemic influenza A (H1N1) virus infection: availability of diagnostic testing led to rapid pandemic response. Clin Infect Dis. 2011;52(Suppl 1):S3643. DOIPubMedGoogle Scholar
  6. Uyeki  TM, Prasad  R, Vukotich  C, Stebbins  S, Rinaldo  CR, Ferng  YH, Low sensitivity of rapid diagnostic test for influenza. Clin Infect Dis. 2009;48:e8992. DOIPubMedGoogle Scholar
  7. Chartrand  C, Leeflang  MM, Minion  J, Brewer  T, Pai  M. Accuracy of rapid influenza diagnostic tests: a meta-analysis. Ann Intern Med. 2012;156:50011. DOIPubMedGoogle Scholar
  8. Talbot  HK, Williams  JV, Zhu  Y, Poehling  KA, Griffin  MR, Edwards  KM. Failure of routine diagnostic methods to detect influenza in hospitalized older adults. Infect Control Hosp Epidemiol. 2010;31:6838. DOIPubMedGoogle Scholar
  9. Peterson  S, Dugas  AF, Rothman  RE. Evaluation of 11 commercially available rapid influenza diagnostic tests-United States, 2011–2012. Ann Emerg Med. 2013;61:5737. DOIPubMedGoogle Scholar
  10. Mahony  JB. Nucleic acid amplification-based diagnosis of respiratory virus infections. Expert Rev Anti Infect Ther. 2010;8:127392. DOIPubMedGoogle Scholar
  11. Kumar  S, Henrickson  KJ. Update on influenza diagnostics: lessons from the novel H1N1 influenza A pandemic. Clin Microbiol Rev. 2012;25:34461. DOIPubMedGoogle Scholar
  12. Cox  CM, D'Mello  T, Perez  A, Reingold  A, Gershman  K, Yousey-Hindes  K, Increase in rates of hospitalization due to laboratory-confirmed influenza among children and adults during the 2009–10 influenza pandemic. J Infect Dis. 2012;206:13508. DOIPubMedGoogle Scholar
  13. Zhou  H, Thompson  WW, Viboud  CG, Ringholz  CM, Cheng  PY, Steiner  C, Hospitalizations associated with influenza and respiratory syncytial virus in the United States, 1993–2008. Clin Infect Dis. 2012;54:142736. DOIPubMedGoogle Scholar
  14. Pinner  RW, Rebmann  CA, Schuchat  A, Hughes  JM. Disease surveillance and the academic, clinical, and public health communities. Emerg Infect Dis. 2003;9:7817. DOIPubMedGoogle Scholar
  15. Dawood  FS, Fiore  A, Kamimoto  L, Nowell  M, Reingold  A, Gershman  K, Influenza-associated pneumonia in children hospitalized with laboratory-confirmed influenza, 2003–2008. Pediatr Infect Dis J. 2010;29:58590. DOIPubMedGoogle Scholar
  16. Barker  WH, Menegus  MA, Hall  CB, Betts  RF, Freundlich  CB, Long  CE, Communitywide laboratory-based influenza surveillance focused on older persons, 1989–1992. Am J Prev Med. 1995;11:14955 .PubMedGoogle Scholar
  17. Steininger  C, Redlberger  M, Graninger  W, Kundi  M, Popow-Kraupp  T. Near-patient assays for diagnosis of influenza virus infection in adult patients. Clin Microbiol Infect. 2009;15:26773. DOIPubMedGoogle Scholar
  18. Long  CE, Hall  CB, Cunningham  CK, Weiner  LB, Alger  KP, Gouveia  M, Influenza surveillance in community-dwelling elderly compared with children. Arch Fam Med. 1997;6:45965. DOIPubMedGoogle Scholar
  19. Steininger  C, Kundi  M, Aberle  SW, Aberle  JH, Popow-Kraupp  T. Effectiveness of reverse transcription–PCR, virus isolation, and enzyme-linked immunosorbent assay for diagnosis of influenza A virus infection in different age groups. J Clin Microbiol. 2002;40:20516. DOIPubMedGoogle Scholar
  20. Bradley Efron  RJT. An introduction to the bootstrap. London: Chapman and Hall; 1993.
  21. Novak-Weekley  SM, Marlowe  EM, Poulter  M, Dwyer  D, Speers  D, Rawlinson  W, Evaluation of the Cepheid Xpert Flu Assay for rapid identification and differentiation of influenza A, influenza A 2009 H1N1, and influenza B viruses. J Clin Microbiol. 2012;50:170410. DOIPubMedGoogle Scholar
  22. Van Wesenbeeck  L, Meeuws  H, Van Immerseel  A, Ispas  G, Schmidt  K, Houspie  L, Comparison of the FilmArray RP, Verigene RV+, and Prodesse ProFLU+/FAST+ multiplex platforms for detection of influenza viruses in clinical samples from the 2011–2012 influenza season in Belgium. J Clin Microbiol. 2013;51:297785. DOIPubMedGoogle Scholar
  23. Templeton  KE, Scheltinga  SA, Beersma  MF, Kroes  AC, Claas  EC. Rapid and sensitive method using multiplex real-time PCR for diagnosis of infections by influenza A and influenza B viruses, respiratory syncytial virus, and parainfluenza viruses 1, 2, 3, and 4. J Clin Microbiol. 2004;42:15649. DOIPubMedGoogle Scholar
  24. Gharabaghi  F, Tellier  R, Cheung  R, Collins  C, Broukhanski  G, Drews  SJ, Comparison of a commercial qualitative real-time RT-PCR kit with direct immunofluorescence assay (DFA) and cell culture for detection of influenza A and B in children. J Clin Virol. 2008;42:1903. DOIPubMedGoogle Scholar
  25. Walsh  EE, Cox  C, Falsey  AR. Clinical features of influenza A virus infection in older hospitalized persons. J Am Geriatr Soc. 2002;50:1498503. DOIPubMedGoogle Scholar
  26. LaSala  PR, Bufton  KK, Ismail  N, Smith  MB. Prospective comparison of R-mix™ shell vial system with direct antigen tests and conventional cell culture for respiratory virus detection. J Clin Virol. 2007;38:2106. DOIPubMedGoogle Scholar
  27. Irmen  KE, Kelleher  JJ. Use of monoclonal antibodies for rapid diagnosis of respiratory viruses in a community hospital. Clin Diagn Lab Immunol. 2000;7:396403 .PubMedGoogle Scholar
  28. Rahman  M, Kieke  BA, Vandermause  MF, Mitchell  PD, Greenlee  RT, Belongia  EA. Performance of Directigen flu A+B enzyme immunoassay and direct fluorescent assay for detection of influenza infection during the 2004–2005 season. Diagn Microbiol Infect Dis. 2007;58:4138. DOIPubMedGoogle Scholar
  29. Uyeki  TM. Influenza diagnosis and treatment in children: a review of studies on clinically useful tests and antiviral treatment for influenza. Pediatr Infect Dis J. 2003;22:16477. DOIPubMedGoogle Scholar
  30. Stout  C, Murphy  MD, Lawrence  S, Julian  S. Evaluation of a monoclonal antibody pool for rapid diagnosis of respiratory viral infections. J Clin Microbiol. 1989;27:44852 .PubMedGoogle Scholar
  31. Fader  RC. Comparison of the Binax NOW Flu A enzyme immunochromatographic assay and R-Mix shell vial culture for the 2003–2004 influenza seasons. J Clin Microbiol. 2005;43:61335. DOIPubMedGoogle Scholar
  32. Nelson  EA, Ip  M, Tam  JS, Mounts  AW, Chau  SL, Law  SK, Burden of influenza infection in hospitalised children below 6 months of age and above in Hong Kong from 2005 to 2011. Vaccine. 2014;32:66928. DOIPubMedGoogle Scholar
  33. Ortiz  JR, Neuzil  KM, Shay  DK, Rue  TC, Neradilek  MB, Zhou  H, The burden of influenza-associated critical illness hospitalizations. Crit Care Med. 2014;42:232532. DOIPubMedGoogle Scholar
  34. Poehling  KA, Edwards  KM, Griffin  MR, Szilagyi  PG, Staat  MA, Iwane  MK, The burden of influenza in young children, 2004–2009. Pediatrics. 2013;131:20716. DOIPubMedGoogle Scholar
  35. Williamson  DA, Huang  QS, Roberts  SA, Grant  CC, McArthur  C, Baker  MG. Surveillance for influenza using hospital discharge data may underestimate the burden of influenza-related hospitalization. Infect Control Hosp Epidemiol. 2012;33:10646. DOIPubMedGoogle Scholar
  36. Widmer  K, Zhu  Y, Williams  JV, Griffin  MR, Edwards  KM, Talbot  HK. Rates of hospitalizations for respiratory syncytial virus, human metapneumovirus, and influenza virus in older adults. J Infect Dis. 2012;206:5662. DOIPubMedGoogle Scholar
  37. Burton  C, Vaudry  W, Moore  D, Bettinger  JA, Tran  D, Halperin  SA, Burden of seasonal influenza in children with neurodevelopmental conditions. Pediatr Infect Dis J. 2014;33:7104. DOIPubMedGoogle Scholar
  38. Emukule  GO, Khagayi  S, McMorrow  ML, Ochola  R, Otieno  N, Widdowson  MA, The burden of influenza and RSV among inpatients and outpatients in rural western Kenya, 2009–2012. PLoS ONE. 2014;9:e105543. DOIPubMedGoogle Scholar
  39. Reed  C, Chaves  SS, Daily Kirley  P, Emerson  R, Aragon  D, Hancock  EB, Estimating influenza disease burden from population-based surveillance data in the United States. PLoS ONE. 2015;10:e0118369. DOIPubMedGoogle Scholar

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Page updated: August 12, 2015
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