Impact of a Single-Tube PCR Assay for the Detection of Serotypes A, C, D, E and F on the Epidemiological Surveillance in Greece

Overview

Journal Microorganisms

Specialty Microbiology

Date 2022 Jul 27

PMID 35889086

Authors

Athanasia Xirogianni

Theano Georgakopoulou

Vassileios Patsourakos

Ioanna Magaziotou

Anastasia Papandreou

Stelmos Simantirakis

Georgina Tzanakaki

Affiliations

Soon will be listed here.

Abstract

Background: The decrease in the rate of meningitis due to Haemophilus influenzae type b after vaccine introduction and a possible change in epidemiology of H. influenzae disease highlights the need for continuous serotype surveillance. Methods: A single-tube multiplex PCR assay for serotyping of H. influenzae was developed and deployed. Results: During 2003−2020, 108 meningitis cases due to H. influenzae were notified; 86 (80%) were confirmed and serotyped by molecular methods. The overall specificity and sensitivity of the assay were estimated (100% PPV and NPV respectively). The overall mean annual reported incidence for H. influenzae was 0.02, while for Hib and non-b meningitis equaled 0.02 and 0.03 per 100 000, respectively. Analysis by age group revealed that H. influenzae peaks in toddlers and children 0−4 years and in adults >45 years old. Among the serotyped cases, 39.8% were identified as Hib, 46.3% as NTHi, and 0.9% and 2.8% as serotypes a (Hia) and f (Hif)) respectively. Conclusions: Low incidence due to Hib was observed while non-typeable H. influenzae (NTHi) and serotypes Hia and Hif seem to emerge. The application of the current assay discloses the ongoing change of invasive H. influenzae disease trends during the Hib post-vaccine era.

References

Sarangi J, Cartwright K, Stuart J, Brookes S, Morris R, Slack M . Invasive Haemophilus influenzae disease in adults. Epidemiol Infect. 2000; 124(3):441-7. PMC: 2810930. DOI: 10.1017/s0950268899003611. View

Heath P, McVernon J . The UK Hib vaccine experience. Arch Dis Child. 2002; 86(6):396-9. PMC: 1762993. DOI: 10.1136/adc.86.6.396. View

Maaroufi Y, De Bruyne J, Heymans C, Crokaert F . Real-time PCR for determining capsular serotypes of Haemophilus influenzae. J Clin Microbiol. 2007; 45(7):2305-8. PMC: 1932976. DOI: 10.1128/JCM.00102-07. View

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(Pt 11):1161-1165. DOI: 10.1099/jmm.0.45749-0. View

Georgakopoulou T, Menegas D, Katsioulis A, Theodoridou M, Kremastinou J, Hadjichristodoulou C . A cross-sectional vaccination coverage study in preschool children attending nurseries-kindergartens: Implications on economic crisis effect. Hum Vaccin Immunother. 2016; 13(1):190-197. PMC: 5287328. DOI: 10.1080/21645515.2016.1230577. View

Peltola H, Salo E, Saxen H . Incidence of Haemophilus influenzae type b meningitis during 18 years of vaccine use: observational study using routine hospital data. BMJ. 2004; 330(7481):18-9. PMC: 539842. DOI: 10.1136/bmj.38301.657014.79. View

Whittaker R, Economopoulou A, Gomes Dias J, Bancroft E, Ramliden M, Pastore Celentano L . Epidemiology of Invasive Haemophilus influenzae Disease, Europe, 2007-2014. Emerg Infect Dis. 2017; 23(3):396-404. PMC: 5382729. DOI: 10.3201/eid2303.161552. View

Ulanova M, Tsang R . Invasive Haemophilus influenzae disease: changing epidemiology and host-parasite interactions in the 21st century. Infect Genet Evol. 2009; 9(4):594-605. DOI: 10.1016/j.meegid.2009.03.001. View

St Geme 3rd J . The pathogenesis of nontypable Haemophilus influenzae otitis media. Vaccine. 2001; 19 Suppl 1:S41-50. DOI: 10.1016/s0264-410x(00)00277-2. View

10.

Giufre M, Lindh E, Cardines R, Pezzotti P, Cerquetti M . Invasive Haemophilus influenzae type b (Hib) disease in children in Italy, after 20 years of routine use of conjugate Hib vaccines. Vaccine. 2020; 38(42):6533-6538. DOI: 10.1016/j.vaccine.2020.08.022. View

11.

Jalalvand F, Riesbeck K . Haemophilus influenzae: recent advances in the understanding of molecular pathogenesis and polymicrobial infections. Curr Opin Infect Dis. 2014; 27(3):268-74. DOI: 10.1097/QCO.0000000000000056. View

12.

Murphy T . Respiratory infections caused by non-typeable Haemophilus influenzae. Curr Opin Infect Dis. 2003; 16(2):129-34. DOI: 10.1097/00001432-200304000-00009. View

13.

Tsolia M, Theodoridou M, Mostrou G, Paraskaki I, Pangali A, Yelesme A . Epidemiology of invasive Haemophilus influenzae type b infections among children in Greece before the introduction of immunization. Scand J Infect Dis. 1998; 30(2):165-8. DOI: 10.1080/003655498750003564. View

14.

Theodoridou M, Vasilopoulou V, Atsali E, Pangalis A, Mostrou G, Syriopoulou V . Meningitis registry of hospitalized cases in children: epidemiological patterns of acute bacterial meningitis throughout a 32-year period. BMC Infect Dis. 2007; 7:101. PMC: 2031898. DOI: 10.1186/1471-2334-7-101. View

15.

Papavasileiou K, Papavasileiou E, Tzanakaki G, Voyatzi A, Kremastinou J, Chatzipanagiotou S . Acute bacterial meningitis cases diagnosed by culture and PCR in a children's hospital throughout a 9-Year period (2000-2008) in Athens, Greece. Mol Diagn Ther. 2011; 15(2):109-13. DOI: 10.1007/BF03256400. View

16.

Lam T, Elias J, Frosch M, Vogel U, Claus H . New diagnostic PCR for Haemophilus influenzae serotype e based on the cap locus of strain ATCC 8142. Int J Med Microbiol. 2010; 301(2):176-9. DOI: 10.1016/j.ijmm.2010.07.004. View

17.

McElligott M, Meyler K, Bennett D, Mulhall R, Drew R, Cunney R . Epidemiology of Haemophilus influenzae in the Republic of Ireland, 2010-2018. Eur J Clin Microbiol Infect Dis. 2020; 39(12):2335-2344. DOI: 10.1007/s10096-020-03971-z. View

18.

Ladomenou F, Tzanakaki G, Kolyva S, Katsarakis I, Maraki S, Galanakis E . Conjugate vaccines dramatically reshaped the epidemiology of bacterial meningitis in a well-defined child population. Acta Paediatr. 2019; 109(2):368-374. DOI: 10.1111/apa.14957. View

19.

Perdue D, Bulkow L, Gellin B, Davidson M, Petersen K, Singleton R . Invasive Haemophilus influenzae disease in Alaskan residents aged 10 years and older before and after infant vaccination programs. JAMA. 2000; 283(23):3089-94. DOI: 10.1001/jama.283.23.3089. View

20.

Takla A, Schonfeld V, Claus H, Krone M, An der Heiden M, Koch J . Invasive Infections in Germany After the Introduction of Routine Childhood Immunization, 2001-2016. Open Forum Infect Dis. 2020; 7(10):ofaa444. PMC: 7585332. DOI: 10.1093/ofid/ofaa444. View