Long Term Impact of Conjugate Vaccines on Haemophilus influenzae Meningitis: Narrative Review
Abstract
:1. Introduction
2. Method
3. Global Burden of Hib Meningitis before the Introduction of Routine Hib Immunization
4. Hib Vaccines
4.1. Plain PRP Vaccine
4.2. Hib Protein-Conjugate Vaccines
5. Introduction of Hib Conjugate Vaccine in National Immunization Programs (NIPs)
6. Impact of Hib Conjugate Vaccine on Hib Meningitis
7. Resurgence of Hib Meningitis in Some Countries
7.1. Resurgence of Hib in the UK
7.2. Resurgence of Hib in South Africa
7.3. Resurgence of Hib in the Gambia
7.4. Is a Booster Dose of Hib Vaccine Needed?
8. Current Burden of H. influenzae Meningitis
9. Meningitis Due to Non-b Serotypes of H. influenzae
9.1. Meningitis Due to Serotype a (Hia)
9.2. Meningitis Due to Serotypes e and f (Hie and Hif)
9.3. Meningitis Due to Non-Typeable H.influenzae (NTHi)
10. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Pittman, M. Variation and type specificity in the bacterial species Haemophilus influenzae. J. Exp. Med. 1931, 53, 471–492. [Google Scholar] [CrossRef] [PubMed]
- Kilian, M.; Frederiksen, W. Ecology of Haemophilus, Pasteurella and Actinobacillus. In Haemophilus, Pasteurella and Actinobacillus; Kilian, M., Frederiksen, W., Biberstein, E.L., Eds.; Academic Press: London, UK, 1981; pp. 11–38. [Google Scholar]
- Ingham, H.R.; Turk, D.C. Haemophili from eyes. J. Clin. Pathol. 1969, 22, 258–262. [Google Scholar] [CrossRef] [Green Version]
- Moxon, E.R. Haemophilus influenzae. In Mandell, Douglas abnd Bennett’s Principles and Practice of Infectious Disease, 4th ed.; Mandell, G.L., Bennett, J., Dolin, R., Eds.; Churchill Livingstone: New York, NY, USA, 1995; Volume 2, pp. 2039–2050. [Google Scholar]
- Hammerschlag, M.R.; Alpert, S.; Rosner, I.; Thurston, P.; Semine, D.; McComb, D.; McCormack, W.M. Microbiology of the vagina in children: Normal and potentially pathogenic organisms. Pediatrics 1978, 62, 57–62. [Google Scholar] [PubMed]
- Cox, R.A.; Slack, M.P. Clinical and microbiological features of Haemophilus influenzae vulvovaginitis in young girls. J. Clin. Pathol. 2002, 55, 961–964. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moxon, E.R. The carrier state: Haemophilus influenzae. J. Antimicrob. Chemother. 1986, 18, 17–24. [Google Scholar] [CrossRef] [PubMed]
- Kilian, M.; Frederiksen, W.; Biberstein, E.L. Haemophilus, Pasteurella and Actinobacillus; Academic Press Inc.: London, UK, 1981; 294p. [Google Scholar]
- Wenger, J.D.; Hightower, A.W.; Facklam, R.R.; Gaventa, S.; Broome, C.V. Bacterial meningitis in the United States, 1986: Report of a multistate surveillance study. The Bacterial Meningitis Study Group. J. Infect. Dis. 1990, 162, 1316–1323. [Google Scholar] [CrossRef]
- Broome, C.V. Epidemiology of Haemophilus influenzae type b infections in the United States. Pediatr. Infect. Dis. J. 1987, 6, 779–782. [Google Scholar] [CrossRef]
- Salwén, K.M.; Vikerfors, T.; Olcén, P. Increased incidence of childhood bacterial meningitis. A 25-year study in a defined population in Sweden. Scand. J. Infect. Dis. 1987, 19, 1–11. [Google Scholar] [CrossRef]
- Snaebjarnardóttir, K.; Erlendsdóttir, H.; Reynisson, I.K.; Kristinsson, K.; Halldórsdóttir, S.; Hardardóttir, H.; Gudnason, T.; Gottfredsson, M.; Haraldsson, Á. Bacterial meningitis in children in Iceland, 1975–2010: A nationwide epidemiological study. Scand. J. Infect. Dis. 2013, 45, 819–824. [Google Scholar] [CrossRef]
- Spanjaard, L.; Bol, P.; Ekker, W.; Zanen, H.C. The incidence of bacterial meningitis in the Netherlands--a comparison of three registration systems, 1977–1982. J. Infect. 1985, 11, 259–268. [Google Scholar] [CrossRef]
- Davison, K.L.; Ramsay, M.E. The epidemiology of acute meningitis in children in England and Wales. Arch. Dis. Child. 2003, 88, 662–664. [Google Scholar] [CrossRef] [Green Version]
- Måkelå, P.H.; Takala, A.K.; Peltola, H.; Eskola, J. Epidemiology of Invasive Haemophilus influenzae Type b Disease. J. Infect. Dis. 1992, 165, S2–S6. [Google Scholar] [CrossRef]
- Wilfert, C.M. Epidemiology of Haemophilus influenzae type b infections. Pediatrics 1990, 85, 631–635. [Google Scholar]
- World Health Organization. Haemophilus influenzae Type b (Hib) Meningitis in the Pre-Vaccine Era: A Global Review of Incidence, Age Distributions, and Case-Fatality Rates; World Health Organization: Geneva, Switzerland, 2002; Available online: https://apps.who.int/iris/handle/10665/67572 (accessed on 6 April 2021).
- Fothergill, L.D.; Wright, J. Influenzal Meningitis. J. Immunol. 1933, 24, 273. [Google Scholar]
- Peltola, H.; Käyhty, H.; Sivonen, A.; Mäkelä, H. Haemophilus influenzae type b capsular polysaccharide vaccine in children: A double-blind field study of 100,000 vaccinees 3 months to 5 years of age in Finland. Pediatrics 1977, 60, 730–737. [Google Scholar]
- Käyhty, H.; Peltola, H.; Karanko, V.; Mäkelä, P.H. The protective level of serum antibodies to the capsular polysaccharide of Haemophilus influenzae type b. J. Infect. Dis. 1983, 147, 1100. [Google Scholar] [CrossRef]
- Anderson, P. The protective level of serum antibodies to the capsular polysaccharide of Haemophilus influenzae type b. J. Infect. Dis. 1984, 149, 1034–1035. [Google Scholar] [CrossRef] [PubMed]
- Collins, S.; Ramsay, M.; Campbell, H.; Slack, M.P.; Ladhani, S.N. Invasive Haemophilus influenzae type b disease in England and Wales: Who is at risk after 2 decades of routine childhood vaccination? Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2013, 57, 1715–1721. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ulanova, M.; Tsang, R.S.W. Haemophilus influenzae serotype a as a cause of serious invasive infections. Lancet Infect. Dis. 2014, 14, 70–82. [Google Scholar] [CrossRef]
- Collins, S.; Litt, D.J.; Flynn, S.; Ramsay, M.E.; Slack, M.P.; Ladhani, S.N. Neonatal invasive Haemophilus influenzae disease in England and Wales: Epidemiology, clinical characteristics, and outcome. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2015, 60, 1786–1792. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- World Health Organization. Defeating Meningitis by 2030. Available online: https://www.who.int/initiatives/defeating-meningitis-by-2030 (accessed on 6 April 2021).
- 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. [Google Scholar] [CrossRef]
- Bijlmer, H.A.; van Alphen, L.; Greenwood, B.M.; Brown, J.; Schneider, G.; Hughes, A.; Menon, A.; Zanen, H.C.; Valkenburg, H.A. The epidemiology of Haemophilus influenzae meningitis in children under five years of age in The Gambia, West Africa. J. Infect. Dis. 1990, 161, 1210–1215. [Google Scholar] [CrossRef]
- Ward, J.I.; Margolis, H.S.; Lum, M.K.; Fraser, D.W.; Bender, T.R.; Anderson, P. Haemophilus influenzae disease in Alaskan Eskimos: Characteristics of a population with an unusual incidence of invasive disease. Lancet 1981, 1, 1281–1285. [Google Scholar] [CrossRef]
- Losonsky, G.A.; Santosham, M.; Sehgal, V.M.; Zwahlen, A.; Moxon, E.R. Haemophilus influenzae disease in the White Mountain Apaches: Molecular epidemiology of a high risk population. Pediatr. Infect. Dis. 1984, 3, 539–547. [Google Scholar] [CrossRef] [PubMed]
- Coulehan, J.L.; Michaels, R.H.; Hallowell, C.; Schults, R.; Welty, T.K.; Kuo, J.S. Epidemiology of Haemophilus influenzae type B disease among Navajo Indians. Public Health Rep. 1984, 99, 404–409. [Google Scholar]
- Hanna, J.N.; Wild, B.E. Bacterial meningitis in children under five years of age in Western Australia. Med. J. Aust. 1991, 155, 160–164. [Google Scholar] [CrossRef] [PubMed]
- Hammond, G.W.; Rutherford, B.E.; Malazdrewicz, R.; MacFarlane, N.; Pillay, N.; Tate, R.B.; Nicolle, L.E.; Postl, B.D.; Stiver, H.G. Haemophilus influenzae meningitis in Manitoba and the Keewatin District, NWT: Potential for mass vaccination. Can. Med. Assoc. J. 1988, 139, 743–747. [Google Scholar]
- Bijlmer, H.A. World-wide epidemiology of Haemophilus influenzae meningitis; industrialized versus non-industrialized countries. Vaccine 1991, 9, S5–S9. [Google Scholar] [CrossRef]
- Gilbert, G.L. Epidemiology of Haemophilus influenzae type b disease in Australia and New Zealand. Vaccine 1991, 9, S10–S13, discussion S25. [Google Scholar] [CrossRef]
- Ward, J.I.; Lum, M.K.; Hall, D.B.; Silimperi, D.R.; Bender, T.R. Invasive Haemophilus influenzae type b disease in Alaska: Background epidemiology for a vaccine efficacy trial. J. Infect. Dis. 1986, 153, 17–26. [Google Scholar] [CrossRef] [PubMed]
- Takala, A.K.; Eskola, J.; Peltola, H.; Måkelå, P.H. Epidemiology of invasive Haemophilus influenzae type b disease among children in Finland before vaccination with Haemophilus influenzae type b conjugate vaccine. Pediatr. Infect. Dis. J. 1989, 8, 297–302. [Google Scholar] [CrossRef] [PubMed]
- Anderson, E.C.; Begg, N.T.; Crawshaw, S.C.; Hargreaves, R.M.; Howard, A.J.; Slack, M.P. Epidemiology of invasive Haemophilus influenzae infections in England and Wales in the pre-vaccination era (1990-2). Epidemiol. Infect. 1995, 115, 89–100. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Clements, D.A.; Booy, R.; Dagan, R.; Gilbert, G.L.; Moxon, E.R.; Slack, M.P.; Takala, A.; Zimmermann, H.P.; Zuber, P.L.; Eskola, J. Comparison of the epidemiology and cost of Haemophilus influenzae type b disease in five western countries. Pediatr. Infect. Dis. J. 1993, 12, 362–367. [Google Scholar] [CrossRef]
- Gervaix, A.; Suter, S. Epidemiology of invasive Haemophilus influenzae type b infections in Geneva, Switzerland, 1976 to 1989. Pediatr. Infect. Dis. J. 1991, 10, 370–374. [Google Scholar] [CrossRef] [PubMed]
- Trollfors, B.; Claesson, B.A.; Strangert, K.; Taranger, J. Haemophilus influenzae meningitis in Sweden 1981–1983. Arch. Dis. Child. 1987, 62, 1220–1223. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dagan, R. Epidemiology of invasive Haemophilus influenzae type b (Hib) disease in Israel. Vaccine 1993, 11 (Suppl. 1), S43–S45. [Google Scholar] [CrossRef]
- Gilbert, G.L.; Clements, D.A.; Broughton, S.J. Haemophilus influenzae type b infections in Victoria, Australia, 1985 to 1987. Pediatr. Infect. Dis. J. 1990, 9, 252–257. [Google Scholar] [CrossRef]
- Hansman, D.; Hanna, J.; Morey, F. High prevalence of invasive Haemophilus influenzae disease in central Australia, 1986. Lancet 1986, 2, 927. [Google Scholar] [CrossRef]
- Peltola, H. Haemophilus influenzae type b disease and vaccination in Latin America and the Caribbean. Pediatr. Infect. Dis. J. 1997, 16, 780–787. [Google Scholar] [CrossRef]
- Peltola, H. Spectrum and burden of severe Haemophilus influenzae type b diseases in Asia. Bull. World Health Organ. 1999, 77, 878–887. [Google Scholar]
- Scott, S.; Altanseseg, D.; Sodbayer, D.; Nymadawa, P.; Bulgan, D.; Mendsaikhan, J.; Watt, J.P.; Slack, M.P.; Carvalho, M.G.; Hajjeh, R.; et al. Impact of Haemophilus influenzae Type b conjugate vaccine in Mongolia: Prospective population-based surveillance, 2002–2010. J. Pediatr. 2013, 163, S8–S11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grimwood, K.; Anderson, V.A.; Bond, L.; Catroppa, C.; Hore, R.L.; Keir, E.H.; Nolan, T.; Roberton, D.M. Adverse outcomes of bacterial meningitis in school-age survivors. Pediatrics 1995, 95, 646–656. [Google Scholar]
- Baraff, L.J.; Lee, S.I.; Schriger, D.L. Outcomes of bacterial meningitis in children: A meta-analysis. Pediatr. Infect. Dis. J. 1993, 12, 389–394. [Google Scholar] [CrossRef] [PubMed]
- Letson, G.W.; Gellin, B.G.; Bulkow, L.R.; Parks, D.J.; Ward, J.I. Severity and frequency of sequelae of bacterial meningitis in Alaska Native infants. Correlation with a scoring system for severity of sequelae. Am. J. Dis. Child. 1992, 146, 560–566. [Google Scholar] [CrossRef] [PubMed]
- D’Angio, C.T.; Froehlke, R.G.; Plank, G.A.; Meehan, D.J.; Aguilar, C.M.; Lande, M.B.; Hugar, L. Long-term Outcome of Haemophilus influenzae Meningitis in Navajo Indian Children. Arch. Pediatr. Adolesc. Med. 1995, 149, 1001–1008. [Google Scholar] [CrossRef]
- Goetghebuer, T.; West, T.E.; Wermenbol, V.; Cadbury, A.L.; Milligan, P.; Lloyd-Evans, N.; Adegbola, R.A.; Mulholland, E.K.; Greenwood, B.M.; Weber, M.W. Outcome of meningitis caused by Streptococcus pneumoniae and Haemophilus influenzae type b in children in The Gambia. Trop. Med. Int. Health 2000, 5, 207–213. [Google Scholar] [CrossRef]
- Eskola, J.; Peltola, H.; Takala, A.K.; Käyhty, H.; Hakulinen, M.; Karanko, V.; Kela, E.; Rekola, P.; Ronnberg, P.R.; Samuelson, J.S.; et al. Efficacy of Haemophilus influenzae type b polysaccharide-diphtheria toxoid conjugate vaccine in infancy. N. Engl. J. Med. 1987, 317, 717–722. [Google Scholar] [CrossRef]
- Käyhty, H.; Karanko, V.; Peltola, H.; Mäkelä, P.H. Serum antibodies after vaccination with Haemophilus influenzae type b capsular polysaccharide and responses to reimmunization: No evidence of immunologic tolerance or memory. Pediatrics 1984, 74, 857–865. [Google Scholar]
- O’Brien, K.L.; Steinhoff, M.C.; Edwards, K.; Keyserling, H.; Thoms, M.L.; Madore, D. Immunologic priming of young children by pneumococcal glycoprotein conjugate, but not polysaccharide, vaccines. Pediatr. Infect. Dis. J. 1996, 15, 425–430. [Google Scholar] [CrossRef]
- Ladhani, S.N. Two decades of experience with the Haemophilus influenzae serotype b conjugate vaccine in the United Kingdom. Clin. Ther. 2012, 34, 385–399. [Google Scholar] [CrossRef]
- Anderson, P.; Pichichero, M.E.; Insel, R.A. Immunization of 2-month-old infants with protein-coupled oligosaccharides derived from the capsule of Haemophilus influenzae type b. J. Pediatr. 1985, 107, 346–351. [Google Scholar] [CrossRef]
- Barbour, M.L.; Booy, R.; Crook, D.W.; Griffiths, H.; Chapel, H.M.; Moxon, E.R.; Mayon-White, D. Haemophilus influenzae type b carriage and immunity four years after receiving the Haemophilus influenzae oligosaccharide-CRM197 (HbOC) conjugate vaccine. Pediatr. Infect. Dis. J. 1993, 12, 478–484. [Google Scholar] [CrossRef]
- Kelly, D.F.; Moxon, E.R.; Pollard, A.J. Haemophilus influenzae type b conjugate vaccines. Immunology 2004, 113, 163–174. [Google Scholar] [CrossRef] [PubMed]
- Ward, J.; Brenneman, G.; Letson, G.W.; Heyward, W.L. Limited efficacy of a Haemophilus influenzae type b conjugate vaccine in Alaska Native infants. The Alaska H. influenzae Vaccine Study Group. N. Engl. J. Med. 1990, 323, 1393–1401. [Google Scholar] [CrossRef] [PubMed]
- Bulkow, L.R.; Wainwright, R.B.; Letson, G.W.; Chang, S.J.; Ward, J.I. Comparative immunogenicity of four Haemophilus influenzae type b conjugate vaccines in Alaska Native infants. Pediatr. Infect. Dis. J. 1993, 12, 484–492. [Google Scholar] [CrossRef] [PubMed]
- Decker, M.D.; Edwards, K.M.; Bradley, R.; Palmer, P. Comparative trial in infants of four conjugate Haemophilus influenzae type b vaccines. J. Pediatr. 1992, 120, 184–189. [Google Scholar] [CrossRef]
- Centers for Disease Control. Haemophilus b Conjugate Vaccines for Prevention of Haemophilus influenzae Type b Disease among Infants and Children Two Months of Age and Older: Recommendations of the Immunization Practices Advisory Committee (ACIP). Available online: https://www.cdc.gov/mmwr/preview/mmwrhtml/00041736.htm (accessed on 6 April 2021).
- Gessner, B.D.; Sutanto, A.; Linehan, M.; Djelantik, I.G.; Fletcher, T.; Gerudug, I.K.; Mercer, D.; Moniaga, V.; Moulton, L.H.; Mulholland, K.; et al. Incidences of vaccine-preventable Haemophilus influenzae type b pneumonia and meningitis in Indonesian children: Hamlet-randomised vaccine-probe trial. Lancet 2005, 365, 43–52. [Google Scholar] [CrossRef]
- Feikin, D.R.; Nelson, C.B.; Watt, J.P.; Mohsni, E.; Wenger, J.D.; Levine, O.S. Rapid assessment tool for Haemophilus influenzae type b disease in developing countries. Emerg. Infect. Dis. 2004, 10, 1270–1276. [Google Scholar] [CrossRef]
- Hajjeh, R.A.; Privor-Dumm, L.; Edmond, K.; O’Loughlin, R.; Shetty, S.; Griffiths, U.K.; Bear, A.P.; Cohen, A.L.; Chandran, A.; Schuchat, A.; et al. Supporting new vaccine introduction decisions: Lessons learned from the Hib Initiative experience. Vaccine 2010, 28, 7123–7129. [Google Scholar] [CrossRef]
- World Health Organization. WHO Position Paper on Haemophilus influenzae type b conjugate vaccines. Wkly. Epidemiol. Rec. 2006, 81, 445–452. [Google Scholar]
- Ojo, L.R.; O’Loughlin, R.E.; Cohen, A.L.; Loo, J.D.; Edmond, K.M.; Shetty, S.S.; Bear, A.P.; Privor-Dumm, L.; Griffiths, U.K.; Hajjeh, R. Global use of Haemophilus influenzae type b conjugate vaccine. Vaccine 2010, 28, 7117–7122. [Google Scholar] [CrossRef] [Green Version]
- International Vaccine Access Center. VIEW-Hub Report:Global Vaccine Introduction and Implementation. Available online: https://www.jhsph.edu/ivac/wp-content/uploads/2021/02/VIEW-hubReport_Dec2020.pdf (accessed on 6 April 2021).
- Swingler, G.; Fransman, D.; Hussey, G. Conjugate vaccines for preventing Haemophilus influenzae type b infections. Cochrane Database Syst. Rev. 2007, Cd001729. [Google Scholar] [CrossRef] [Green Version]
- Watt, J.P.; Levine, O.S.; Santosham, M. Global reduction of Hib disease: What are the next steps? Proceedings of the meeting Scottsdale, Arizona, 22–25 September 2002. J. Pediatr. 2003, 143, S163–S187. [Google Scholar] [CrossRef]
- McIntyre, P.B.; O’Brien, K.L.; Greenwood, B.; van de Beek, D. Effect of vaccines on bacterial meningitis worldwide. Lancet 2012, 380, 1703–1711. [Google Scholar] [CrossRef]
- Watt, J.P.; Wolfson, L.J.; O’Brien, K.L.; Henkle, E.; Deloria-Knoll, M.; McCall, N.; Lee, E.; Levine, O.S.; Hajjeh, R.; Mulholland, K.; et al. Burden of disease caused by Haemophilus influenzae type b in children younger than 5 years: Global estimates. Lancet 2009, 374, 903–911. [Google Scholar] [CrossRef]
- Wahl, B.; O’Brien, K.L.; Greenbaum, A.; Majumder, A.; Liu, L.; Chu, Y.; Luksic, I.; Nair, H.; McAllister, D.A.; Campbell, H.; et al. Burden of Streptococcus pneumoniae and Haemophilus influenzae type b disease in children in the era of conjugate vaccines: Global, regional, and national estimates for 2000-15. Lancet. Glob. Health 2018, 6, e744–e757. [Google Scholar] [CrossRef] [Green Version]
- Davis, S.; Feikin, D.; Johnson, H.L. The effect of Haemophilus influenzae type b and pneumococcal conjugate vaccines on childhood meningitis mortality: A systematic review. BMC Public Health 2013, 13 (Suppl. 3), S21. [Google Scholar] [CrossRef] [Green Version]
- Morris, S.K.; Moss, W.J.; Halsey, N. Haemophilus influenzae type b conjugate vaccine use and effectiveness. Lancet Infect. Dis. 2008, 8, 435–443. [Google Scholar] [CrossRef]
- Schuchat, A.; Hilger, T.; Zell, E.; Farley, M.M.; Reingold, A.; Harrison, L.; Lefkowitz, L.; Danila, R.; Stefonek, K.; Barrett, N.; et al. Active bacterial core surveillance of the emerging infections program network. Emerg. Infect. Dis. 2001, 7, 92–99. [Google Scholar] [CrossRef] [PubMed]
- Thigpen, M.C.; Whitney, C.G.; Messonnier, N.E.; Zell, E.R.; Lynfield, R.; Hadler, J.L.; Harrison, L.H.; Farley, M.M.; Reingold, A.; Bennett, N.M.; et al. Bacterial meningitis in the United States, 1998–2007. N. Engl. J. Med. 2011, 364, 2016–2025. [Google Scholar] [CrossRef] [PubMed]
- Centers for Disease Control and Prevention. Nationally Notifiable Infectious Diseases and Conditions, United States: Annual Tables. Available online: https://wonder.cdc.gov/nndss/static/2018/annual/2018-table1.html (accessed on 6 April 2021).
- Polkowska, A.; Toropainen, M.; Ollgren, J.; Lyytikäinen, O.; Nuorti, J.P. Bacterial meningitis in Finland, 1995–2014: A population-based observational study. BMJ Open 2017, 7, e015080. [Google Scholar] [CrossRef] [Green Version]
- Ali, M.; Chang, B.A.; Johnson, K.W.; Morris, S.K. Incidence and aetiology of bacterial meningitis among children aged 1–59 months in South Asia: Systematic review and meta-analysis. Vaccine 2018, 36, 5846–5857. [Google Scholar] [CrossRef]
- Ceyhan, M.; Ozsurekci, Y.; Tanır Basaranoglu, S.; Gurler, N.; Sali, E.; Keser Emiroglu, M.; Oz, F.N.; Belet, N.; Duman, M.; Ulusoy, E.; et al. Multicenter Hospital-Based Prospective Surveillance Study of Bacterial Agents Causing Meningitis and Seroprevalence of Different Serogroups of Neisseria meningitidis, Haemophilus influenzae type b, and Streptococcus pneumoniae during 2015 to 2018 in Turkey. mSphere 2020, 5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Suga, S.; Ishiwada, N.; Sasaki, Y.; Akeda, H.; Nishi, J.; Okada, K.; Fujieda, M.; Oda, M.; Asada, K.; Nakano, T.; et al. A nationwide population-based surveillance of invasive Haemophilus influenzae diseases in children after the introduction of the Haemophilus influenzae type b vaccine in Japan. Vaccine 2018, 36, 5678–5684. [Google Scholar] [CrossRef] [PubMed]
- Ladhani, S.N.; Ramsay, M.; Slack, M.P. The impact of Haemophilus influenzae serotype b resurgence on the epidemiology of childhood invasive Haemophilus influenzae disease in England and Wales. Pediatr. Infect. Dis. J. 2011, 30, 893–895. [Google Scholar] [CrossRef] [PubMed]
- McVernon, J.; Andrews, N.; Slack, M.P.; Ramsay, M.E. Risk of vaccine failure after Haemophilus influenzae type b (Hib) combination vaccines with acellular pertussis. Lancet 2003, 361, 1521–1523. [Google Scholar] [CrossRef]
- McVernon, J.; Johnson, P.D.; Pollard, A.J.; Slack, M.P.; Moxon, E.R. Immunologic memory in Haemophilus influenzae type b conjugate vaccine failure. Arch. Dis. Child. 2003, 88, 379–383. [Google Scholar] [CrossRef] [PubMed]
- Ramsay, M.E.; McVernon, J.; Andrews, N.J.; Heath, P.T.; Slack, M.P. Estimating Haemophilus influenzae type b vaccine effectiveness in England and Wales by use of the screening method. J. Infect. Dis. 2003, 188, 481–485. [Google Scholar] [CrossRef] [Green Version]
- McVernon, J.; Howard, A.J.; Slack, M.P.; Ramsay, M.E. Long-term impact of vaccination on Haemophilus influenzae type b (Hib) carriage in the United Kingdom. Epidemiol. Infect. 2004, 132, 765–767. [Google Scholar] [CrossRef]
- Johnson, N.G.; Ruggeberg, J.U.; Balfour, G.F.; Lee, Y.C.; Liddy, H.; Irving, D.; Sheldon, J.; Slack, M.P.; Pollard, A.J.; Heath, P.T. Haemophilus influenzae type b reemergence after combination immunization. Emerg. Infect. Dis. 2006, 12, 937–941. [Google Scholar] [CrossRef]
- Trotter, C.L.; McVernon, J.; Andrews, N.J.; Burrage, M.; Ramsay, M.E. Antibody to Haemophilus influenzae type b after routine and catch-up vaccination. Lancet 2003, 361, 1523–1524. [Google Scholar] [CrossRef]
- Ladhani, S.; Slack, M.P.; Heys, M.; White, J.; Ramsay, M.E. Fall in Haemophilus influenzae serotype b (Hib) disease following implementation of a booster campaign. Arch. Dis. Child. 2008, 93, 665–669. [Google Scholar] [CrossRef] [PubMed]
- Department of Health. Immunisation against Infectious Diseases Chapter 16: Haemophilus influenzae Type b (Hib). Available online: https://www.gov.uk/government/publications/haemophilus-influenzae-type-hib-the-green-book-chapter-16 (accessed on 6 April 2021).
- Litt, D.; Fry, N.K.; Ladhani, S.N. Epidemiology of invasive Haemophilus influenzae disease in England: National surveillance, 2017–2018 PO-019-(EMGM2019-13268). In Proceedings of the 15th EMGM Congress, Lisbon, Portugal, 27–30 May 2019; Available online: https://www.gov.uk/government/publications/haemophilus-influenzae-type-hib-the-green-book-chapter-16 (accessed on 6 April 2021).
- Von Gottberg, A.; de Gouveia, L.; Madhi, S.A.; du Plessis, M.; Quan, V.; Soma, K.; Huebner, R.; Flannery, B.; Schuchat, A.; Klugman, K. Impact of conjugate Haemophilus influenzae type b (Hib) vaccine introduction in South Africa. Bull. World Health Organ. 2006, 84, 811–818. [Google Scholar] [CrossRef]
- Von Gottberg, A.; Cohen, C.; Whitelaw, A.; Chhagan, M.; Flannery, B.; Cohen, A.L.; de Gouveia, L.; Plessis, M.; Madhi, S.A.; Klugman, K.P. Invasive disease due to Haemophilus influenzae serotype b ten years after routine vaccination, South Africa, 2003–2009. Vaccine 2012, 30, 565–571. [Google Scholar] [CrossRef] [PubMed]
- National Institute for Communicable Diseases. GERMS South Africa Annual Surveillance Review 2018. Available online: https://www.nicd.ac.za/wp-content/uploads/2019/11/GERMS-SA-AR-2018-Final.pdf (accessed on 6 April 2021).
- Howie, S.R.; Oluwalana, C.; Secka, O.; Scott, S.; Ideh, R.C.; Ebruke, B.E.; Balloch, A.; Sambou, S.; Erskine, J.; Lowe, Y.; et al. The effectiveness of conjugate Haemophilus influenzae type b vaccine in The Gambia 14 years after introduction. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2013, 57, 1527–1534. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mackenzie, G.A.; Ikumapayi, U.N.; Scott, S.; Idoko, O.; Odutola, A.; Ndiaye, M.; Sahito, S.M.; Osuorah, C.D.; Manjang, A.; Jarju, S.; et al. Increased disease due to Haemophilus influenzae type b: Population-based surveillance in eastern Gambia, 2008–2013. Pediatr. Infect. Dis. J. 2015, 34, e107–e112. [Google Scholar] [CrossRef]
- Hammitt, L.L.; Crane, R.J.; Karani, A.; Mutuku, A.; Morpeth, S.C.; Burbidge, P.; Goldblatt, D.; Kamau, T.; Sharif, S.; Mturi, N.; et al. Effect of Haemophilus influenzae type b vaccination without a booster dose on invasive H influenzae type b disease, nasopharyngeal carriage, and population immunity in Kilifi, Kenya: A 15-year regional surveillance study. Lancet. Glob. Health 2016, 4, e185–e194. [Google Scholar] [CrossRef] [Green Version]
- Low, N.; Redmond, S.M.; Rutjes, A.W.; Martínez-González, N.A.; Egger, M.; di Nisio, M.; Scott, P. Comparing Haemophilus influenzae type b conjugate vaccine schedules: A systematic review and meta-analysis of vaccine trials. Pediatr. Infect. Dis. J. 2013, 32, 1245–1256. [Google Scholar] [CrossRef] [PubMed]
- Mangtani, P.; Mulholland, K.; Madhi, S.A.; Edmond, K.; O’Loughlin, R.; Hajjeh, R. Haemophilus influenzae type b disease in HIV-infected children: A review of the disease epidemiology and effectiveness of Hib conjugate vaccines. Vaccine 2010, 28, 1677–1683. [Google Scholar] [CrossRef]
- Tsang, R.S.W.; Ulanova, M. The changing epidemiology of invasive Haemophilus influenzae disease: Emergence and global presence of serotype a strains that may require a new vaccine for control. Vaccine 2017, 35, 4270–4275. [Google Scholar] [CrossRef]
- Ladhani, S.N.; Collins, S.; Vickers, A.; Litt, D.J.; Crawford, C.; Ramsay, M.E.; Slack, M.P. Invasive Haemophilus influenzae serotype e and f disease, England and Wales. Emerg. Infect. Dis. 2012, 18, 725–732. [Google Scholar] [CrossRef] [PubMed]
- Ladhani, S.; Slack, M.P.; Heath, P.T.; von Gottberg, A.; Chandra, M.; Ramsay, M.E. Invasive Haemophilus influenzae Disease, Europe, 1996–2006. Emerg. Infect. Dis. 2010, 16, 455–463. [Google Scholar] [CrossRef] [Green Version]
- Van Eldere, J.; Slack, M.P.; Ladhani, S.; Cripps, A.W. Non-typeable Haemophilus influenzae, an under-recognised pathogen. Lancet Infect. Dis. 2014, 14, 1281–1292. [Google Scholar] [CrossRef] [Green Version]
- Gratten, M.; Barker, J.; Shann, F.; Gerega, G.; Montgomery, J.; Kajoi, M.; Lupiwa, T. Non-type b Haemophilus influenzae meningitis. Lancet 1985, 1, 1343–1344. [Google Scholar] [CrossRef]
- Gratten, M.; Montgomery, J. The bacteriology of acute pneumonia and meningitis in children in Papua New Guinea: Assumptions, facts and technical strategies. Papua New Guin. Med. J. 2005, 48, 73–86. [Google Scholar]
- Millar, E.V.; O’Brien, K.L.; Watt, J.P.; Lingappa, J.; Pallipamu, R.; Rosenstein, N.; Hu, D.; Reid, R.; Santosham, M. Epidemiology of invasive Haemophilus influenzae type A disease among Navajo and White Mountain Apache children, 1988–2003. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2005, 40, 823–830. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsang, R.S.; Mubareka, S.; Sill, M.L.; Wylie, J.; Skinner, S.; Law, D.K. Invasive Haemophilus influenzae in Manitoba, Canada, in the postvaccination era. J. Clin. Microbiol. 2006, 44, 1530–1535. [Google Scholar] [CrossRef] [Green Version]
- Tsang, R.S.; Bruce, M.G.; Lem, M.; Barreto, L.; Ulanova, M. A review of invasive Haemophilus influenzae disease in the Indigenous populations of North America. Epidemiol. Infect. 2014, 142, 1344–1354. [Google Scholar] [CrossRef] [Green Version]
- Bruce, M.G.; Deeks, S.L.; Zulz, T.; Navarro, C.; Palacios, C.; Case, C.; Hemsley, C.; Hennessy, T.; Corriveau, A.; Larke, B.; et al. Epidemiology of Haemophilus influenzae serotype a, North American Arctic, 2000–2005. Emerg. Infect. Dis. 2008, 14, 48–55. [Google Scholar] [CrossRef]
- McConnell, A.; Tan, B.; Scheifele, D.; Halperin, S.; Vaudry, W.; Law, B.; Embree, J. Invasive infections caused by Haemophilus influenzae serotypes in twelve Canadian IMPACT centers, 1996–2001. Pediatr. Infect. Dis. J. 2007, 26, 1025–1031. [Google Scholar] [CrossRef] [PubMed]
- Zwahlen, A.; Kroll, J.S.; Rubin, L.G.; Moxon, E.R. The molecular basis of pathogenicity in Haemophilus influenzae: Comparative virulence of genetically-related capsular transformants and correlation with changes at the capsulation locus cap. Microb. Pathog. 1989, 7, 225–235. [Google Scholar] [CrossRef]
- Soeters, H.M.; Blain, A.; Pondo, T.; Doman, B.; Farley, M.M.; Harrison, L.H.; Lynfield, R.; Miller, L.; Petit, S.; Reingold, A.; et al. Current Epidemiology and Trends in Invasive Haemophilus influenzae Disease-United States, 2009–2015. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2018, 67, 881–889. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Soeters, H.M.; Oliver, S.E.; Plumb, I.D.; Blain, A.E.; Zulz, T.; Simons, B.C.; Barnes, M.; Farley, M.M.; Harrison, L.H.; Lynfield, R.; et al. Epidemiology of Invasive Haemophilus influenzae Serotype a Disease-United States, 2008–2017. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2020. [Google Scholar] [CrossRef]
- Bender, J.M.; Cox, C.M.; Mottice, S.; She, R.C.; Korgenski, K.; Daly, J.A.; Pavia, A.T. Invasive Haemophilus influenzae disease in Utah children: An 11-year population-based study in the era of conjugate vaccine. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2010, 50, e41–e46. [Google Scholar] [CrossRef] [Green Version]
- Crandall, H.; Christiansen, J.; Varghese, A.A.; Russon, A.; Korgenski, E.K.; Bengtson, E.K.; Dickey, M.; Killpack, J.; Knackstedt, E.D.; Daly, J.A.; et al. Clinical and Molecular Epidemiology of Invasive Haemophilus influenzae Serotype a Infections in Utah Children. J. Pediatr. Infect. Dis. 2019, 9, 650–655. [Google Scholar] [CrossRef] [PubMed]
- Antony, S.; Kaushik, A.; Mauriello, C.; Chatterjee, A. Non-Type b Haemophilus influenzae Invasive Infections in North Dakota and South Dakota, 2013–2015. J. Pediatr. Infect. Dis. 2017, 6, 281–284. [Google Scholar]
- Ribeiro, G.S.; Lima, J.B.; Reis, J.N.; Gouveia, E.L.; Cordeiro, S.M.; Lobo, T.S.; Pinheiro, R.M.; Ribeiro, C.T.; Neves, A.B.; Salgado, K.; et al. Haemophilus influenzae meningitis 5 years after introduction of the Haemophilus influenzae type b conjugate vaccine in Brazil. Vaccine 2007, 25, 4420–4428. [Google Scholar] [CrossRef]
- Zanella, R.C.; Bokermann, S.; Andrade, A.L.; Flannery, B.; Brandileone, M.C. Changes in serotype distribution of Haemophilus influenzae meningitis isolates identified through laboratory-based surveillance following routine childhood vaccination against H. influenzae type b in Brazil. Vaccine 2011, 29, 8937–8942. [Google Scholar] [CrossRef] [PubMed]
- Lima, J.B.; Ribeiro, G.S.; Cordeiro, S.M.; Gouveia, E.L.; Salgado, K.; Spratt, B.G.; Godoy, D.; Reis, M.G.; Ko, A.I.; Reis, J.N. Poor clinical outcome for meningitis caused by Haemophilus influenzae serotype a strains containing the IS1016-bexA deletion. J. Infect. Dis. 2010, 202, 1577–1584. [Google Scholar] [CrossRef] [PubMed]
- Giufrè, M.; Cardines, R.; Brigante, G.; Orecchioni, F.; Cerquetti, M. Emergence of Invasive Haemophilus influenzae type a Disease in Italy. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2017, 64, 1626–1628. [Google Scholar] [CrossRef] [Green Version]
- Collins, S.; Fry, N.K.; Ladhani, S.N.; Litt, D. The rise (and fall) of invasive Haemophilus influenzae serotype a (Hia) disease in England )C-(EMGM2019-13311). In Proceedings of the 15th EMGM Congress, Lisbon, Portugal, 27–30 May 2019; Available online: https://emgm.eu/meetings/emgm2019/emgm2019_abstracts.pdf (accessed on 6 April 2021).
- Roaa, Z.; Abdulsalam, A.; Shahid, G.; Kamaldeen, B.; Tariq, A.F. Pediatric invasive disease due to Haemophilus influenzae serogroup a in Riyadh, Saudi Arabia: Case series. J. Infect. Dev. Ctries 2016, 10, 528–532. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cox, A.D.; Barreto, L.; Ulanova, M.; Bruce, M.G.; Tsang, R. Developing a vaccine for Haemophilus influenzae serotype a: Proceedings of a workshop. Can. Commun. Dis. Rep. 2017, 43, 89–95. [Google Scholar] [CrossRef] [PubMed]
- Whittaker, R.; Economopoulou, A.; Dias, J.G.; Bancroft, E.; Ramliden, M.; Celentano, L.P. Epidemiology of Invasive Haemophilus influenzae Disease, Europe, 2007–2014. Emerg. Infect. Dis. 2017, 23, 396–404. [Google Scholar] [CrossRef] [Green Version]
- Takla, A.; Schönfeld, V.; Claus, H.; Krone, M.; An der Heiden, M.; Koch, J.; Vogel, U.; Wichmann, O.; Lâm, T.-T. Invasive Haemophilus influenzae Infections in Germany After the Introduction of Routine Childhood Immunization, 2001–2016. Open Forum Infect. Dis. 2020, 7, ofaa444. [Google Scholar] [CrossRef]
- Urwin, G.; Krohn, J.A.; Deaver-Robinson, K.; Wenger, J.D.; Farley, M.M. 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. Off. Publ. Infect. Dis. Soc. Am. 1996, 22, 1069–1076. [Google Scholar] [CrossRef]
- MacNeil, J.R.; Cohn, A.C.; Farley, M.; Mair, R.; Baumbach, J.; Bennett, N.; Gershman, K.; Harrison, L.H.; Lynfield, R.; Petit, S.; et al. Current epidemiology and trends in invasive Haemophilus influenzae disease--United States, 1989–2008. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2011, 53, 1230–1236. [Google Scholar] [CrossRef]
- Abou-Hanna, J.; Panning, K.; Mehta, H. Haemophilus influenzae Type f Meningitis Complicated by Bilateral Subdural Empyema, Central Venous Thrombosis, and Bilateral Sensorineural Hearing Loss in an Immunocompetent 12-month-old. Cureus 2019, 11, e4850. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Resman, F.; Ristovski, M.; Ahl, J.; Forsgren, A.; Gilsdorf, J.R.; Jasir, A.; Kaijser, B.; Kronvall, G.; Riesbeck, K. Invasive disease caused by Haemophilus influenzae in Sweden 1997–2009; evidence of increasing incidence and clinical burden of non-type b strains. Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis. 2011, 17, 1638–1645. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Collins, S.; Vickers, A.; Ladhani, S.N.; Flynn, S.; Platt, S.; Ramsay, M.E.; Litt, D.J.; Slack, M.P. Clinical and Molecular Epidemiology of Childhood Invasive Nontypeable Haemophilus influenzae Disease in England and Wales. Pediatr. Infect. Dis. J. 2016, 35, e76–e84. [Google Scholar] [CrossRef] [PubMed]
- Ulu-Kilic, A.; Altay, F.A.; Gürbüz, Y.; Otgun, S.N.; Sencan, I. Haemophilus influenzae serotype e meningitis in an adult. J. Infect. Dev. Ctries 2010, 4, 253–255. [Google Scholar] [CrossRef] [Green Version]
- Gkentzi, D.; Slack, M.P.; Ladhani, S.N. The burden of nonencapsulated Haemophilus influenzae in children and potential for prevention. Curr. Opin. Infect. Dis. 2012, 25, 266–272. [Google Scholar] [CrossRef]
- Van Wessel, K.; Rodenburg, G.D.; Veenhoven, R.H.; Spanjaard, L.; van der Ende, A.; Sanders, E.A. Nontypeable Haemophilus influenzae invasive disease in The Netherlands: A retrospective surveillance study 2001–2008. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2011, 53, e1–e7. [Google Scholar] [CrossRef] [PubMed]
- Cardines, R.; Giufre, M.; Mastrantonio, P.; Ciofi degli Atti, M.L.; Cerquetti, M. Nontypeable Haemophilus influenzae meningitis in children: Phenotypic and genotypic characterization of isolates. Pediatr. Infect. Dis. J. 2007, 26, 577–582. [Google Scholar] [CrossRef]
- Kalies, H.; Siedler, A.; Grondahl, B.; Grote, V.; Milde-Busch, A.; von Kries, R. Invasive Haemophilus influenzae infections in Germany: Impact of non-type b serotypes in the post-vaccine era. BMC Infect. Dis. 2009, 9, 45. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sarangi, J.; Cartwright, K.; Stuart, J.; Brookes, S.; Morris, R.; Slack, M. Invasive Haemophilus influenzae disease in adults. Epidemiol. Infect. 2000, 124, 441–447. [Google Scholar] [CrossRef] [PubMed]
- Dworkin, M.S.; Park, L.; Borchardt, S.M. The changing epidemiology of invasive Haemophilus influenzae disease, especially in persons ≥ 65 years old. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2007, 44, 810–816. [Google Scholar] [CrossRef]
- Desai, S.; Jamieson, F.B.; Patel, S.N.; Seo, C.Y.; Dang, V.; Fediurek, J.; Navaranjan, D.; Deeks, S.L. The Epidemiology of Invasive Haemophilus influenzae Non-Serotype b Disease in Ontario, Canada from 2004 to 2013. PLoS ONE 2015, 10, e0142179. [Google Scholar] [CrossRef] [Green Version]
- Slack, M.; Esposito, S.; Haas, H.; Mihalyi, A.; Nissen, M.; Mukherjee, P.; Harrington, L. Haemophilus influenzae type b disease in the era of conjugate vaccines: Critical factors for successful eradication. Exp. Rev. Vaccines 2020, 19, 903–917. [Google Scholar] [CrossRef]
Region | Hib Meningitis (Cases/100,000 Children < 5 Years of Age) |
---|---|
USA | 54 |
North America (Indigenous) | 152–530 |
Europe | 23–31 |
Israel | 18 |
The Gambia | 60 |
Australia and New Zealand (non-Indigenous) | 25–34 |
Australia and New Zealand (Indigenous) | 450 |
Latin America | 35 |
Asia | 25 |
Mongolia | 28 |
Global | African Region | Region of the Americas | Eastern Mediterranean Region | European Region | South East Asia Region | Western Pacific Region | |
---|---|---|---|---|---|---|---|
2000 Estimates | |||||||
Incidence | 31 (16–39) | 46 (31–52) | 25 (16–30) | 24 (14–35) | 16 (12–22) | 27 (11–38) | 34 (12–48) |
CFR | 43% (23–55%) | 67% (44–75%) | 28% (15–36%) | 44% (26–62%) | 27% (17–41%) | 44% (17–62%) | 22% (8–34%) |
2015 Estimates [73] | |||||||
Incidence | 5 (2–8) | 2 (1–3) | 0 (0–0) | 1 (0–1) | 3 (1–5) | 8 (3–12) | 11 (6–18) |
CFR | 19% (7–29%) | 61% (20–98%) | 30% (7–51%) | 54% (16–89%) | 5% (2–9%) | 32% (12–49%) | 5% (2–8%) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Slack, M.P.E. Long Term Impact of Conjugate Vaccines on Haemophilus influenzae Meningitis: Narrative Review. Microorganisms 2021, 9, 886. https://doi.org/10.3390/microorganisms9050886
Slack MPE. Long Term Impact of Conjugate Vaccines on Haemophilus influenzae Meningitis: Narrative Review. Microorganisms. 2021; 9(5):886. https://doi.org/10.3390/microorganisms9050886
Chicago/Turabian StyleSlack, Mary Paulina Elizabeth. 2021. "Long Term Impact of Conjugate Vaccines on Haemophilus influenzae Meningitis: Narrative Review" Microorganisms 9, no. 5: 886. https://doi.org/10.3390/microorganisms9050886
APA StyleSlack, M. P. E. (2021). Long Term Impact of Conjugate Vaccines on Haemophilus influenzae Meningitis: Narrative Review. Microorganisms, 9(5), 886. https://doi.org/10.3390/microorganisms9050886