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Abstract

Since the introduction of (Hi) serotype b (Hib) vaccination, reports of increasing incidence rates of non-Hib serotypes have emerged. A systematic review was performed to investigate whether the Hi serotype f (Hif) incidence rate has increased globally and to describe its associated disease burden. In the post-Hib vaccine era, evidence shows that the incidence rate of Hif infection is increasing worldwide. In total 94 studies including 2 701 patients reported Hif infections. The estimated pooled incidence rate of Hif infection was 0.15/100 000 population per year (range: 0.05–0.40/100 000), with a median case fatality ratio of 14.3 %. Invasive infections most frequently presented as pneumonia (45 %), septicaemia (34 %) and meningitis (20 %). Of 191 Hif isolates, 87 % were ampicillin-susceptible. Multi-locus sequence typing revealed that Hif were relatively clonal, with the majority belonging to clonal complex 124. Hif causes invasive infections of significant variance in both severity and presentation. Globally, the Hif population shows little genetic variability and currently appears to possess low resistance to antimicrobials.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-10-28
2024-12-07
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References

  1. McElligott M, Meyler K, Bennett D, Mulhall R, Drew RJ et al. Epidemiology of Haemophilus influenzae in the Republic of Ireland, 2010-2018. Eur J Clin Microbiol Infect Dis 2020; 39:2335–2344 [View Article] [PubMed]
    [Google Scholar]
  2. Peltola H. Worldwide Haemophilus influenzae type b disease at the beginning of the 21st century: global analysis of the disease burden 25 years after the use of the polysaccharide vaccine and a decade after the advent of conjugates. Clin Microbiol Rev 2000; 13:302–317 [View Article] [PubMed]
    [Google Scholar]
  3. Kelly DF, Moxon ER, Pollard AJ. Haemophilus influenzae type b conjugate vaccines. Immunology 2004; 113:163–174 [View Article] [PubMed]
    [Google Scholar]
  4. HSE Haemophilus inflenzae type b (hib), chapter 7; 2018
  5. Whittaker R, Economopoulou A, Dias JG, Bancroft E, Ramliden M et al. Epidemiology of invasive Haemophilus influenzae disease, Europe, 2007-2014. Emerg Infect Dis 2017; 23:396–404 [View Article]
    [Google Scholar]
  6. Ladhani SN, Collins S, Vickers A, Litt DJ, Crawford C et al. Invasive Haemophilus influenzae serotype e and f disease, England and Wales. Emerg Infect Dis 2012; 18:725–732 [View Article]
    [Google Scholar]
  7. Urwin G, Krohn JA, Deaver-Robinson K, Wenger JD, Farley MM. Invasive disease due to Haemophilus influenzae serotype f: clinical and epidemiologic characteristics in the H. influenzae serotype b vaccine era. the Haemophilus influenzae study group. Clin Infect Dis 1996; 22:1069–1076 [View Article]
    [Google Scholar]
  8. Moher D, Liberati A, Tetzlaff J, Altman DG. PRISMA Group Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 2009; 339:b2535 [View Article]
    [Google Scholar]
  9. von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC et al. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Int J Surg 2014; 12:1495–1499 [View Article]
    [Google Scholar]
  10. Puig C, Grau I, Marti S, Tubau F, Calatayud L et al. Clinical and molecular epidemiology of Haemophilus influenzae causing invasive disease in adult patients. PLoS One 2014; 9:e112711 [View Article]
    [Google Scholar]
  11. Wenger JD, Pierce R, Deaver K, Franklin R, Bosley G et al. Invasive Haemophilus influenzae disease: a population-based evaluation of the role of capsular polysaccharide serotype. Haemophilus Influenzae Study Group. J Infect Dis 1992; 165 Suppl 1:S34–5 [View Article]
    [Google Scholar]
  12. MacNeil JR, Cohn AC, Farley M, Mair R, Baumbach J et al. Current epidemiology and trends in invasive Haemophilus influenzae disease--United States, 1989-2008. Clin Infect Dis 2011; 53:1230–1236 [View Article] [PubMed]
    [Google Scholar]
  13. Rubach MP, Bender JM, Mottice S, Hanson K, Weng HYC et al. Increasing incidence of invasive Haemophilus influenzae disease in adults, Utah, USA. Emerg Infect Dis 2011; 17:1645–1650 [View Article]
    [Google Scholar]
  14. Desai S, Jamieson FB, Patel SN, Seo CY, Dang V et al. The epidemiology of invasive Haemophilus influenzae non-serotype B disease in Ontario, Canada from 2004 to 2013. PLoS One 2015; 10:e0142179 [View Article]
    [Google Scholar]
  15. Campos J, Hernando M, Román F, Pérez-Vázquez M, Aracil B et al. Analysis of invasive Haemophilus influenzae infections after extensive vaccination against H. influenzae type b. J Clin Microbiol 2004; 42:524–529 [View Article] [PubMed]
    [Google Scholar]
  16. van Driel JJ, Bekker V, Spanjaard L, van der Ende A, Kuijpers TW. Epidemiologic and microbiologic characteristics of recurrent bacterial and fungal meningitis in the Netherlands, 1988-2005. Clin Infect Dis 2008; 47:e42–51 [View Article] [PubMed]
    [Google Scholar]
  17. Bajanca-Lavado MP, Simões AS, Betencourt CR, Sá-Leão R. Portuguese group for study of Haemophilus influenzae invasive infection Characteristics of Haemophilus influenzae invasive isolates from Portugal following routine childhood vaccination against H. influenzae serotype b (2002-2010). Eur J Clin Microbiol Infect Dis 2014; 33:603–610 [View Article]
    [Google Scholar]
  18. Campos J, Román F, Pérez-Vázquez M, Aracil B, Oteo J et al. Antibiotic resistance and clinical significance of Haemophilus influenzae type f. J Antimicrob Chemother 2003; 52:961–966 [View Article] [PubMed]
    [Google Scholar]
  19. Deghmane A-E, Hong E, Chehboub S, Terrade A, Falguières M et al. High diversity of invasive Haemophilus influenzae isolates in France and the emergence of resistance to third generation cephalosporins by alteration of ftsI gene. J Infect 2019; 79:7–14 [View Article] [PubMed]
    [Google Scholar]
  20. Hoshino T, Hachisu Y, Kikuchi T, Tokutake S, Okui H et al. Analysis of Haemophilus influenzae serotype f isolated from three Japanese children with invasive H. influenzae infection. J Med Microbiol 2015; 64:355–358 [View Article]
    [Google Scholar]
  21. Shuel M, Hoang L, Law DKS, Tsang R. Invasive Haemophilus influenzae in British Columbia: non-Hib and non-typeable strains causing disease in children and adults. Int J Infect Dis 2011; 15:e167–73 [View Article]
    [Google Scholar]
  22. Sill ML, Law DKS, Zhou J, Skinner S, Wylie J et al. Population genetics and antibiotic susceptibility of invasive Haemophilus influenzae in Manitoba, Canada, from 2000 to 2006. FEMS Immunol Med Microbiol 2007; 51:270–276 [View Article]
    [Google Scholar]
  23. Tsang RSW, Mubareka S, Sill ML, Wylie J, Skinner S et al. Invasive Haemophilus influenzae in Manitoba, Canada, in the postvaccination era. J Clin Microbiol 2006; 44:1530–1535 [View Article] [PubMed]
    [Google Scholar]
  24. Tsang RSW, Shuel M, Whyte K, Hoang L, Tyrrell G et al. Antibiotic susceptibility and molecular analysis of invasive haemophilus influenzae in canada 2007 to 2014. J Antimicrob Chemother 2017; 72:1314–1319 [View Article]
    [Google Scholar]
  25. Yokota S, Ohkoshi Y, Sato K, Fujii N. High prevalence of beta-lactam-resistant Haemophilus influenzae type b isolates derived from respiratory tract specimens in Japanese patients. Int J Infect Dis 2009; 13:584–588 [View Article] [PubMed]
    [Google Scholar]
  26. Bruun B, Gahrn-Hansen B, Westh H, Kilian M. Clonal relationship of recent invasive Haemophilus influenzae serotype f isolates from Denmark and the United States. J Med Microbiol 2004; 53:1161–1165 [View Article] [PubMed]
    [Google Scholar]
  27. Hoshino T, Hachisu Y, Kikuchi T, Tokutake S, Okui H et al. Analysis of Haemophilus influenzae serotype f isolated from three Japanese children with invasive H. influenzae infection. J Med Microbiol 2015; 64:355–358 [View Article]
    [Google Scholar]
  28. Giufrè M, Cardines R, Accogli M, Pardini M, Cerquetti M. Identification of Haemophilus influenzae clones associated with invasive disease a decade after introduction of H. influenzae serotype b vaccination in Italy. Clin Vaccine Immunol 2013; 20:1223–1229 [View Article] [PubMed]
    [Google Scholar]
  29. Watson ME, Nelson KL, Nguyen V, Burnham C-AD, Clarridge JE et al. Adhesin genes and serum resistance in Haemophilus influenzae type f isolates. J Med Microbiol 2013; 62:514–524 [View Article] [PubMed]
    [Google Scholar]
  30. Tudor-Williams G, Frankland J, Isaacs D, Mayon-White RT, MacFarlane JA et al. Haemophilus influenzae type b disease in the Oxford region. Arch Dis Child 1989; 64:517–519 [View Article] [PubMed]
    [Google Scholar]
  31. Gilsdorf JR. Hib vaccines: Their impact on Haemophilus influenzae type b disease. J Infect Dis 2021; 224:S321–S330 [View Article]
    [Google Scholar]
  32. Ulanova M, Tsang RSW. Haemophilus influenzae serotype a as a cause of serious invasive infections. Lancet Infect Dis 2014; 14:70–82 [View Article] [PubMed]
    [Google Scholar]
  33. Waggoner-Fountain LA, Hendley JO, Cody EJ, Perriello VA, Donowitz LG. The emergence of Haemophilus influenzae types e and f as significant pathogens. Clin Infect Dis 1995; 21:1322–1324 [View Article] [PubMed]
    [Google Scholar]
  34. Vallejo JG, McNeil JC, Hultén KG, Sommer LM, Dunn JJ et al. Invasive Haemophilus influenzae disease at texas children’s Hospital, 2011 to 2018. Pediatr Infect Dis J 2019; 38:900–905 [View Article]
    [Google Scholar]
  35. Sadeghi-Aval P, Tsang RS, Jamieson FB, Ulanova M. Emergence of non-serotype b encapsulated Haemophilus influenzae as a cause of pediatric meningitis in Northwestern Ontario. Can J Infect Dis Med Microbiol 2013; 24:13–16 [View Article] [PubMed]
    [Google Scholar]
  36. Ronit A, Berg RMG, Bruunsgaard H, Plovsing RR. Haemophilus influenzae type f meningitis in a previously healthy boy. BMJ Case Rep 2013; 2013:bcr2013008854 [View Article]
    [Google Scholar]
  37. Heliodoro CIM, Bettencourt CR, Bajanca-Lavado MP. Portuguese group for the study of Haemophilus influenzae invasive infection Molecular epidemiology of invasive Haemophilus influenzae disease in Portugal: an update of the post-vaccine period, 2011-2018. Eur J Clin Microbiol Infect Dis 2020; 39:1471–1480 [View Article]
    [Google Scholar]
  38. Staples M, Graham RMA, Jennison AV. Characterisation of invasive clinical Haemophilus influenzae isolates in Queensland, Australia using whole-genome sequencing. Epidemiol Infect 2017; 145:1727–1736 [View Article]
    [Google Scholar]
  39. WHO WHO publishes list of bacteria for which new antibiotics are urgently needed; 2017 https://www.who.int/news/item/27-02-2017-who-publishes-list-of-bacteria-for-which-new-antibiotics-are-urgently-needed
  40. Brueggemann AB, van Rensburg MJJ, Shaw D, McCarthy N, Jolley KA et al. The invasive respiratory infection surveillance (IRIS) initiative reveals significant reductions in invasive bacterial infections during the COVID-19 pandemic. Infect Dis 2020 [View Article]
    [Google Scholar]
  41. Adam HJ, Richardson SE, Jamieson FB, Rawte P, Low DE et al. Changing epidemiology of invasive Haemophilus influenzae in Ontario, Canada: evidence for herd effects and strain replacement due to Hib vaccination. Vaccine 2010; 28:4073–4078 [View Article] [PubMed]
    [Google Scholar]
  42. Berndsen MR, Erlendsdóttir H, Gottfredsson M. Evolving epidemiology of invasive Haemophilus infections in the post-vaccination era: results from a long-term population-based study. Clin Microbiol Infect 2012; 18:918–923 [View Article] [PubMed]
    [Google Scholar]
  43. Boula A, Senghore M, Ngoh R, Tassadjo F, Fonkoua M-C et al. Hospital-based surveillance provides insights Into the etiology of pediatric bacterial meningitis in Yaoundé, Cameroon, in the post-vaccine era. Clin Infect Dis 2019; 69:S148–S155 [View Article]
    [Google Scholar]
  44. Campos J, Hernando M, Román F, Pérez-Vázquez M, Aracil B et al. Analysis of invasive Haemophilus influenzae infections after extensive vaccination against H. influenzae type b. J Clin Microbiol 2004; 42:524–529 [View Article] [PubMed]
    [Google Scholar]
  45. Collins S, Litt DJ, Flynn S, Ramsay ME, Slack MPE et al. Neonatal invasive Haemophilus influenzae disease in England and Wales: epidemiology, clinical characteristics, and outcome. Clin Infect Dis 2015; 60:1786–1792 [View Article] [PubMed]
    [Google Scholar]
  46. Dworkin MS, Park L, Borchardt SM. The changing epidemiology of invasive Haemophilus influenzae disease, especially in persons > or = 65 years old. Clin Infect Dis 2007; 44:810–816 [View Article] [PubMed]
    [Google Scholar]
  47. Falla TJ, Dobson SR, Crook DW, Kraak WA, Nichols WW et al. Population-based study of non-typable Haemophilus influenzae invasive disease in children and neonates. Lancet 1993; 341:851–854 [View Article] [PubMed]
    [Google Scholar]
  48. McConnell A, Tan B, Scheifele D, Halperin S, Vaudry W et al. Invasive infections caused by Haemophilus influenzae serotypes in twelve Canadian IMPACT centers, 1996-2001. Pediatr Infect Dis J 2007; 26:1025–1031 [View Article]
    [Google Scholar]
  49. Muhlemann K, Balz M, Aebi S, Schopfer K. Molecular characteristics of Haemophilus influenzae causing invasive disease during the period of vaccination in Switzerland: analysis of strains isolated between 1986 and 1993. J Clin Microbiol 1996; 34:560–563 [View Article] [PubMed]
    [Google Scholar]
  50. Naranjo L, Suarez JA, DeAntonio R, Sanchez F, Calvo A et al. Non-capsulated and capsulated Haemophilus influenzae in children with acute otitis media in Venezuela: a prospective epidemiological study. BMC Infect Dis 2012; 12:40 [View Article]
    [Google Scholar]
  51. Pedersen TI, Howitz M, Ostergaard C. Clinical characteristics of Haemophilus influenzae meningitis in Denmark in the post-vaccination era. Clin Microbiol Infect 2010; 16:439–446 [View Article] [PubMed]
    [Google Scholar]
  52. Perdue DG, Bulkow LR, Gellin BG, Davidson M, Petersen KM et al. Invasive Haemophilus influenzae disease in Alaskan residents aged 10 years and older before and after infant vaccination programs. JAMA 2000; 283:3089–3094 [View Article] [PubMed]
    [Google Scholar]
  53. Skoczyńska A, Kadłubowski M, Empel J, Hryniewicz W. Characteristics of Haemophilus influenzae type b responsible for meningitis in Poland from 1997 to 2004. J Clin Microbiol 2005; 43:5665–5669 [View Article] [PubMed]
    [Google Scholar]
  54. van Alphen L, Riemens T, Poolman J, Zanen HC. Characteristics of major outer membrane proteins of Haemophilus influenzae. J Bacteriol 1983; 155:878–885 [View Article]
    [Google Scholar]
  55. Yee ME, Bakshi N, Graciaa SH, Lane PA, Jerris RC et al. Incidence of invasive Haemophilus influenzae infections in children with sickle cell disease. Pediatr Blood Cancer 2019; 66:e27642 [View Article] [PubMed]
    [Google Scholar]
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