-
How nasopharyngeal pneumococcal carriage evolved during and after a PCV13-to-PCV10 vaccination programme switch in Belgium, 2016 to 2018
- Ine Wouters1 , Stefanie Desmet2 , Liesbet Van Heirstraeten3 , Sereina A Herzog4 , Philippe Beutels4 , Jan Verhaegen2 , Herman Goossens3 , Pierre Van Damme1 , Surbhi Malhotra-Kumar3 , Heidi Theeten1 , NPcarriage Study Group5
-
View Affiliations Hide AffiliationsAffiliations: 1 Centre for the Evaluation of Vaccination, Vaccine and Infectious Disease Institute, University of Antwerp, Wilrijk, Belgium 2 Reference Centre for Pneumococci, University Hospitals Leuven, Leuven, Belgium 3 Laboratory of Medical Microbiology, Vaccine and Infectious Disease Institute, University of Antwerp, Wilrijk, Belgium 4 Centre for Health Economics Research and Modelling Infectious Diseases, University of Antwerp, Wilrijk, Belgium 5 The members of the NPcarriage Study Group are listed at the end of the articleIne Woutersine.wouters uantwerpen.be
-
View Citation Hide Citation
Citation style for this article: Wouters Ine, Desmet Stefanie, Van Heirstraeten Liesbet, Herzog Sereina A, Beutels Philippe, Verhaegen Jan, Goossens Herman, Van Damme Pierre, Malhotra-Kumar Surbhi, Theeten Heidi, NPcarriage Study Group. How nasopharyngeal pneumococcal carriage evolved during and after a PCV13-to-PCV10 vaccination programme switch in Belgium, 2016 to 2018. Euro Surveill. 2020;25(5):pii=1900303. https://doi.org/10.2807/1560-7917.ES.2020.25.5.1900303 Received: 16 May 2019; Accepted: 10 Dec 2019
- Previous Article
- Table of Contents
- Next Article
Abstract
The current carriage study was set up to reinforce surveillance during/after the PCV13-to-PCVC10 switch in Belgium.
This observational study monitored carriage of Streptococcus pneumoniae (Sp) serotypes, particularly those no longer covered (3, 6A, 19A), as well as Haemophilus influenzae (Hi), because PCV10 contains the non-typeable Hi protein D.
A total of 2,615 nasopharyngeal swabs from children (6–30 months old) attending day care were collected in three periods over 2016–2018. Children’s demographic and clinical characteristics and vaccination status were obtained through a questionnaire. Sp and Hi were identified by culture and PCR. Pneumococcal strains were tested for antimicrobial (non-)susceptibility by disc diffusion and serotyped by Quellung-reaction (Quellung-reaction and PCR for serotypes 3, 6A, 19A).
The carriage prevalence of Sp (> 75%) remained stable over the successive periods but that of Hi increased (87.4%, 664 Hi-carriers/760 in 2016 vs 93.9%, 895/953 in 2017–2018). The proportion of non-PCV13 vaccine serotypes decreased (94.6%, 438 isolates/463 in 2016 vs 89.7%, 599/668 in 2017–2018) while that of PCV13-non-PCV10 vaccine serotypes (3 + 6A + 19A) increased (0.9%, 4 isolates/463 in 2016 vs 7.8%, 52/668 in 2017–2018), with serotype 19A most frequently identified (87.9%, 58/66 isolates). Non-susceptibility of pneumococci against any of the tested antibiotics was stable over the study period (> 44%).
During and after the PCV13-to-PCV10 vaccine switch, the proportion of non-PCV13 serotypes decreased, mainly due to a serotype 19A carriage prevalence increase. These results complement invasive pneumococcal disease surveillance data, providing further basis for pneumococcal vaccination programme policy making.

Article metrics loading...

-
From This Site
/content/10.2807/1560-7917.ES.2020.25.5.1900303dcterms_title,dcterms_subject,pub_keyword-contentType:Journal -contentType:Contributor -contentType:Concept -contentType:Institution105 -
PubMed
-
Google Scholar

Full text loading...
References
-
Satzke C, Dunne EM, Porter BD, Klugman KP, Mulholland EKPneuCarriage project group. The PneuCarriage Project: A Multi-Centre Comparative Study to Identify the Best Serotyping Methods for Examining Pneumococcal Carriage in Vaccine Evaluation Studies. PLoS Med. 2015;12(11):e1001903, discussion e1001903. https://doi.org/10.1371/journal.pmed.1001903 PMID: 26575033
-
Simell B, Auranen K, Käyhty H, Goldblatt D, Dagan R, O’Brien KLPneumococcal Carriage Group. The fundamental link between pneumococcal carriage and disease. Expert Rev Vaccines. 2012;11(7):841-55. https://doi.org/10.1586/erv.12.53 PMID: 22913260
-
Syrjänen RK, Kilpi TM, Kaijalainen TH, Herva EE, Takala AK. Nasopharyngeal carriage of Streptococcus pneumoniae in Finnish children younger than 2 years old. J Infect Dis. 2001;184(4):451-9. https://doi.org/10.1086/322048 PMID: 11471103
-
World Health Organization (WHO). Pneumococcal conjugate vaccines in infants and children under 5 years of age: WHO position paper - February 2019. WER. 2019;94(8):85-104.
-
Bogaert D, De Groot R, Hermans PW. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis. 2004;4(3):144-54. https://doi.org/10.1016/S1473-3099(04)00938-7 PMID: 14998500
-
Prevention of pneumococcal disease: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 1997;46(RR-8):1-24. PMID: 9132580
-
Faden H, Duffy L, Wasielewski R, Wolf J, Krystofik D, Tung Y. Relationship between nasopharyngeal colonization and the development of otitis media in children. Tonawanda/Williamsville Pediatrics. J Infect Dis. 1997;175(6):1440-5. https://doi.org/10.1086/516477 PMID: 9180184
-
Gray BM, Converse GM 3rd, Dillon HC Jr. Epidemiologic studies of Streptococcus pneumoniae in infants: acquisition, carriage, and infection during the first 24 months of life. J Infect Dis. 1980;142(6):923-33. https://doi.org/10.1093/infdis/142.6.923 PMID: 7462701
-
Principi N, Marchisio P, Schito GC, Mannelli SAscanius Project Collaborative Group. Risk factors for carriage of respiratory pathogens in the nasopharynx of healthy children. Pediatr Infect Dis J. 1999;18(6):517-23. https://doi.org/10.1097/00006454-199906000-00008 PMID: 10391181
-
Vanderkooi OG, Church DL, MacDonald J, Zucol F, Kellner JD. Community-based outbreaks in vulnerable populations of invasive infections caused by Streptococcus pneumoniae serotypes 5 and 8 in Calgary, Canada. PLoS One. 2011;6(12):e28547. https://doi.org/10.1371/journal.pone.0028547 PMID: 22216100
-
O’Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, McCall N, et al. Hib and Pneumococcal Global Burden of Disease Study Team. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet. 2009;374(9693):893-902. https://doi.org/10.1016/S0140-6736(09)61204-6 PMID: 19748398
-
Geno KA, Gilbert GL, Song JY, Skovsted IC, Klugman KP, Jones C, et al. Pneumococcal Capsules and Their Types: Past, Present, and Future. Clin Microbiol Rev. 2015;28(3):871-99. https://doi.org/10.1128/CMR.00024-15 PMID: 26085553
-
Jauneikaite E, Tocheva AS, Jefferies JM, Gladstone RA, Faust SN, Christodoulides M, et al. Current methods for capsular typing of Streptococcus pneumoniae. J Microbiol Methods. 2015;113:41-9. https://doi.org/10.1016/j.mimet.2015.03.006 PMID: 25819558
-
Pichichero ME, Khan MN, Xu Q. Next generation protein based Streptococcus pneumoniae vaccines. Hum Vaccin Immunother. 2016;12(1):194-205. https://doi.org/10.1080/21645515.2015.1052198 PMID: 26539741
-
Varghese R, Jayaraman R, Veeraraghavan B. Current challenges in the accurate identification of Streptococcus pneumoniae and its serogroups/serotypes in the vaccine era. J Microbiol Methods. 2017;141:48-54. https://doi.org/10.1016/j.mimet.2017.07.015 PMID: 28780272
-
Tsaban G, Ben-Shimol S. Indirect (herd) protection, following pneumococcal conjugated vaccines introduction: A systematic review of the literature. Vaccine. 2017;35(22):2882-91. https://doi.org/10.1016/j.vaccine.2017.04.032 PMID: 28449971
-
Steens A, Caugant DA, Aaberge IS, Vestrheim DF. Decreased Carriage and Genetic Shifts in the Streptococcus pneumoniae Population After Changing the Seven-valent to the Thirteen-valent Pneumococcal Vaccine in Norway. Pediatr Infect Dis J. 2015;34(8):875-83. https://doi.org/10.1097/INF.0000000000000751 PMID: 26020410
-
Miller E, Andrews NJ, Waight PA, Slack MP, George RC. Herd immunity and serotype replacement 4 years after seven-valent pneumococcal conjugate vaccination in England and Wales: an observational cohort study. Lancet Infect Dis. 2011;11(10):760-8. https://doi.org/10.1016/S1473-3099(11)70090-1 PMID: 21621466
-
Navne JE, Børresen ML, Slotved HC, Andersson M, Melbye M, Ladefoged K, et al. Nasopharyngeal bacterial carriage in young children in Greenland: a population at high risk of respiratory infections. Epidemiol Infect. 2016;144(15):3226-36. https://doi.org/10.1017/S0950268816001461 PMID: 27405603
-
Pan H, Cui B, Huang Y, Yang J, Ba-Thein W. Nasal carriage of common bacterial pathogens among healthy kindergarten children in Chaoshan region, southern China: a cross-sectional study. BMC Pediatr. 2016;16(1):161. https://doi.org/10.1186/s12887-016-0703-x PMID: 27741941
-
Spijkerman J, Prevaes SM, van Gils EJ, Veenhoven RH, Bruin JP, Bogaert D, et al. Long-term effects of pneumococcal conjugate vaccine on nasopharyngeal carriage of S. pneumoniae, S. aureus, H. influenzae and M. catarrhalis. PLoS One. 2012;7(6):e39730. https://doi.org/10.1371/journal.pone.0039730 PMID: 22761879
-
Mendes da Costa E, et al. Infectieziekten bij kinderen, die voorkomen kunnen worden door vaccinatie, jaarrapport 2015. Brussel: Wetenschappelijk Instituut Volksgezondheid; 2016.
-
Robert E, Swennen B. Enquête de couverture vaccinale des enfants de 18 à 24 mois en Fédération Wallonie-Bruxelles (Bruxelles exceptée). Bruxelles: ULB; 2015.
-
Vandermeulen C, Hoppenbrouwers K, Roelants M, Theeten H, Braeckman T, Maertens K, Blaizot S, Van Damme P. Studie van de vaccinatiegraad in Vlaanderen, 2016. Vlaamse Overheid: Vlaams Agentschap Zorg en Gezondheid; 2017.
-
Hoppenbrouwers K, et al. Studie van de vaccinatiegraad bij jonge kinderen en adolescenten in Vlaanderen in 2008. Vlaamse Overheid: Vlaams Agentschap Zorg en Gezondheid; 2009.
-
Robert E, Swennen B. Enquête de couverture vaccinale des enfants de 18 à 24 mois en Communauté Française (Bruxelles excepté) - Novembre 2009. Bruxelles: ULB; 2010.
-
Malfroot A, Verhaegen J, Dubru JM, Van Kerschaver E, Leyman S. A cross-sectional survey of the prevalence of Streptococcus pneumoniae nasopharyngeal carriage in Belgian infants attending day care centres. Clin Microbiol Infect. 2004;10(9):797-803. https://doi.org/10.1111/j.1198-743X.2004.00926.x PMID: 15355410
-
Rodrigues F, Foster D, Caramelo F, Serranho P, Gonçalves G, Januário L, et al. Progressive changes in pneumococcal carriage in children attending daycare in Portugal after 6 years of gradual conjugate vaccine introduction show falls in most residual vaccine serotypes but no net replacement or trends in diversity. Vaccine. 2012;30(26):3951-6. https://doi.org/10.1016/j.vaccine.2012.03.058 PMID: 22480926
-
Vestrheim DF, Høiby EA, Aaberge IS, Caugant DA. Phenotypic and genotypic characterization of Streptococcus pneumoniae strains colonizing children attending day-care centers in Norway. J Clin Microbiol. 2008;46(8):2508-18. https://doi.org/10.1128/JCM.02296-07 PMID: 18524970
-
Wouters I, Van Heirstraeten L, Desmet S, Blaizot S, Verhaegen J, Goossens H, et al. NPcarriage Study Group. Nasopharyngeal s. pneumoniae carriage and density in Belgian infants after 9 years of pneumococcal conjugate vaccine programme. Vaccine. 2018;36(1):15-22. https://doi.org/10.1016/j.vaccine.2017.11.052 PMID: 29180027
-
Wouters I, Desmet S, Van Heirstraeten L, Blaizot S, Verhaegen J, Van Damme P, et al. NPcarriage Study Group. Follow-up of serotype distribution and antimicrobial susceptibility of Streptococcus pneumoniae in child carriage after a PCV13-to-PCV10 vaccine switch in Belgium. Vaccine. 2019;37(8):1080-6. https://doi.org/10.1016/j.vaccine.2018.12.068 PMID: 30665775
-
Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing; Supplement M100. Wayne, PA: CSLI; 2017.
-
European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Version 7.1. Växjö: EUCAST; 2017. Available from: http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_7.1_Breakpoint_Tables.pdf
-
Boelsen LK, Dunne EM, Lamb KE, Bright K, Cheung YB, Tikoduadua L, et al. Long-term impact of pneumococcal polysaccharide vaccination on nasopharyngeal carriage in children previously vaccinated with various pneumococcal conjugate vaccine regimes. Vaccine. 2015;33(42):5708-14. https://doi.org/10.1016/j.vaccine.2015.07.059 PMID: 26232540
-
Nakamura S, Yanagihara K, Morinaga Y, Izumikawa K, Seki M, Kakeya H, et al. Multiplex real-time polymerase chain reaction for rapid detection of beta-lactamase-negative, ampicillin-resistant Haemophilus influenzae. Diagn Microbiol Infect Dis. 2009;64(1):64-9. https://doi.org/10.1016/j.diagmicrobio.2009.01.023 PMID: 19232868
-
Azzari C, Moriondo M, Indolfi G, Cortimiglia M, Canessa C, Becciolini L, et al. Realtime PCR is more sensitive than multiplex PCR for diagnosis and serotyping in children with culture negative pneumococcal invasive disease. PLoS One. 2010;5(2):e9282. https://doi.org/10.1371/journal.pone.0009282 PMID: 20174571
-
Slinger R, Duval M, Langill J, Bromwich M, MacCormick J, Chan F, et al. Direct molecular detection of a broad range of bacterial and viral organisms and Streptococcus pneumoniae vaccine serotypes in children with otitis media with effusion. BMC Res Notes. 2016;9(1):247. https://doi.org/10.1186/s13104-016-2040-4 PMID: 27130295
-
Sakai F, Chochua S, Satzke C, Dunne EM, Mulholland K, Klugman KP, et al. Single-plex quantitative assays for the detection and quantification of most pneumococcal serotypes. PLoS One. 2015;10(3):e0121064. https://doi.org/10.1371/journal.pone.0121064 PMID: 25798884
-
Andrade DC, Borges IC, Bouzas ML, Oliveira JR, Käyhty H, Ruuskanen O, et al. Antibody responses against Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis in children with acute respiratory infection with or without nasopharyngeal bacterial carriage. Infect Dis (Lond). 2018;50(9):705-13. https://doi.org/10.1080/23744235.2018.1463451 PMID: 29688138
-
Brandileone MC, Zanella RC, Almeida SCG, Brandao AP, Ribeiro AF, Carvalhanas TMP, et al. Pneumococcal Carriage Study Group. Effect of 10-valent pneumococcal conjugate vaccine on nasopharyngeal carriage of Streptococcus pneumoniae and Haemophilus influenzae among children in São Paulo, Brazil. Vaccine. 2016;34(46):5604-11. https://doi.org/10.1016/j.vaccine.2016.09.027 PMID: 27692770
-
van den Bergh MR, Spijkerman J, Swinnen KM, François NA, Pascal TG, Borys D, et al. Effects of the 10-valent pneumococcal nontypeable Haemophilus influenzae protein D-conjugate vaccine on nasopharyngeal bacterial colonization in young children: a randomized controlled trial. Clin Infect Dis. 2013;56(3):e30-9. https://doi.org/10.1093/cid/cis922 PMID: 23118268
-
Regev-Yochay G, Dagan R, Raz M, Carmeli Y, Shainberg B, Derazne E, et al. Association between carriage of Streptococcus pneumoniae and Staphylococcus aureus in Children. JAMA. 2004;292(6):716-20. https://doi.org/10.1001/jama.292.6.716 PMID: 15304469
-
Lewnard JA, Givon-Lavi N, Huppert A, Pettigrew MM, Regev-Yochay G, Dagan R, et al. Epidemiological Markers for Interactions Among Streptococcus pneumoniae, Haemophilus influenzae, and Staphylococcus aureus in Upper Respiratory Tract Carriage. J Infect Dis. 2016;213(10):1596-605. https://doi.org/10.1093/infdis/jiv761 PMID: 26704617
-
Verhaegen J. Surveillance van de pneumokokkeninfecties in België. Verslag voor 2017. UZ Leuven: Nationaal Referentiecentum voor invasieve pneumokokkeninfecties; 2018.
-
Desmet S, Peetermans WE, Patteet S, Top G, Verhaegen J, Lagrou K. Increase of ST19A invasive pneumococcal disease in young children after switch from PCV13 to PCV10. 39th Annual meeting of the European Society for Paediatric Infectious Dieseases (ESPID); 2019. Ljubljana (Slovenia).
-
Dagan R, Klugman KP. Impact of conjugate pneumococcal vaccines on antibiotic resistance. Lancet Infect Dis. 2008;8(12):785-95. https://doi.org/10.1016/S1473-3099(08)70281-0 PMID: 19022193
-
Naucler P, Galanis I, Morfeldt E, Darenberg J, Örtqvist Å, Henriques-Normark B. Comparison of the Impact of Pneumococcal Conjugate Vaccine 10 or Pneumococcal Conjugate Vaccine 13 on Invasive Pneumococcal Disease in Equivalent Populations. Clin Infect Dis. 2017;65(11):1780-90. https://doi.org/10.1093/cid/cix685 PMID: 29020171
-
Finnish Institute for Health and Welfare (THL). Incidence of invasive pneumococcal disease in Finland. Helsinki: THL; 2017. [Accessed 11 Mar 2019]. Available from: https://thl.fi/en/web/thlfi-en/research-and-expertwork/projects-and-programmes/monitoring-the-population-effectiveness-of-pneumococcal-conjugate-vaccination-in-the-finnish-national-vaccination-programme/incidence-of-invasive-pneumococcal-disease-in-finland#figures

Data & Media loading...
