1887
  1. Home
  2. Eurosurveillance
  3. Volume 29, Issue 45, 07/Nov/2024
  4. Article
Research Open Access
Like 0
Download

Abstract

Background

Despite widely implemented pneumococcal vaccination programmes, remains a global risk for human health. can cause invasive (IPD) or non-invasive pneumococcal disease (NIPD). Surveillance is mainly focusing on IPD, assessing the full impact of pneumococcal vaccination programmes on pneumococcal disease is challenging.

Aim

We aimed to prospectively investigate serotype distribution and antimicrobial resistance (AMR) of isolates from patients with NIPD and compare with data on IPD isolates and with a 2007–2008 dataset on NIPD.

Methods

Between September 2020 and April 2023, we collected isolates and patient data from patients with NIPD from 23 clinical laboratories in Belgium. Capsular typing was performed by a validated Fourier-Transform Infrared spectroscopic method, and AMR was assessed with broth microdilution, using the European Committee on Antimicrobial Susceptibility Testing (EUCAST) clinical breakpoints.

Results

We received isolates from 1,008 patients with lower respiratory tract infections (n = 760), otitis media (n = 190) and sinusitis (n = 58). Serotype 3 was the most prevalent serotype among the NIPD isolates. Serotypes not included in the 20-valent pneumococcal conjugate vaccine (PCV20) were significantly more common among the NIPD than among the IPD isolates. Antimicrobial resistance levels were significantly higher among the NIPD isolates (n = 539; 2020–2022) compared with the IPD isolates (n = 2,344; 2021–2022). Resistance to several β-lactam antimicrobials had increased significantly compared with 15 years before.

Conclusions

The NIPD isolates were strongly associated with non-vaccine serotypes and with increased AMR levels. This underlines the importance of continued NIPD surveillance for informed policy making on vaccination programmes.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2024.29.45.2400108
2024-11-07
2024-12-26
/content/10.2807/1560-7917.ES.2024.29.45.2400108
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/29/45/eurosurv-29-45-7.html?itemId=/content/10.2807/1560-7917.ES.2024.29.45.2400108&mimeType=html&fmt=ahah

References

  1. Ikuta KS, Swetschinski LR, Robles Aguilar G, Sharara F, Mestrovic T, Gray AP, et al. . Global mortality associated with 33 bacterial pathogens in 2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet. 2022;400(10369):2221-48.  https://doi.org/10.1016/S0140-6736(22)02185-7  PMID: 36423648 
  2. 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 
  3. Feldman C, Anderson R. Recent advances in the epidemiology and prevention of Streptococcus pneumoniae infections. F1000 Res. 2020;9:338.  https://doi.org/10.12688/f1000research.22341.1  PMID: 32411353 
  4. Hanquet G, Krizova P, Valentiner-Branth P, Ladhani SN, Nuorti JP, Lepoutre A, et al. Effect of childhood pneumococcal conjugate vaccination on invasive disease in older adults of 10 European countries: implications for adult vaccination. Thorax. 2019;74(5):473-82.  https://doi.org/10.1136/thoraxjnl-2018-211767  PMID: 30355641 
  5. Savulescu C, Krizova P, Valentiner-Branth P, Ladhani S, Rinta-Kokko H, Levy C, et al. Effectiveness of 10 and 13-valent pneumococcal conjugate vaccines against invasive pneumococcal disease in European children: SpIDnet observational multicentre study. Vaccine. 2022;40(29):3963-74.  https://doi.org/10.1016/j.vaccine.2022.05.011  PMID: 35637067 
  6. Amin-Chowdhury Z, Collins S, Sheppard C, Litt D, Fry NK, Andrews N, et al. Characteristics of invasive pneumococcal disease caused by emerging serotypes after the introduction of the 13-valent pneumococcal conjugate vaccine in England: a prospective observational cohort study, 2014-2018. Clin Infect Dis. 2020;71(8):e235-43.  https://doi.org/10.1093/cid/ciaa043  PMID: 31955196 
  7. Desmet S, Lagrou K, Wyndham-Thomas C, Braeye T, Verhaegen J, Maes P, et al. Dynamic changes in paediatric invasive pneumococcal disease after sequential switches of conjugate vaccine in Belgium: a national retrospective observational study. Lancet Infect Dis. 2021;21(1):127-36.  https://doi.org/10.1016/S1473-3099(20)30173-0  PMID: 32702303 
  8. Janoff EN, Musher DM. 201 — Streptococcus pneumoniae. In: Bennett JE, Dolin R, Blaser MJ (editors). Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases. Eighth ed., Amsterdam: Elsevier; 2014, p. 2310-27. Available from: https://www.sciencedirect.com/science/article/abs/pii/B9781455748013002010
  9. Blasi F, Mantero M, Santus P, Tarsia P. Understanding the burden of pneumococcal disease in adults. Clin Microbiol Infect. 2012;18(Suppl 5):7-14.  https://doi.org/10.1111/j.1469-0691.2012.03937.x  PMID: 22882668 
  10. Pick H, Daniel P, Rodrigo C, Bewick T, Ashton D, Lawrence H, et al. Pneumococcal serotype trends, surveillance and risk factors in UK adult pneumonia, 2013-18. Thorax. 2020;75(1):38-49.  https://doi.org/10.1136/thoraxjnl-2019-213725  PMID: 31594801 
  11. Uddén F, Rünow E, Slotved H-C, Fuursted K, Ahl J, Riesbeck K. Characterization of Streptococcus pneumoniae detected in clinical respiratory tract samples in southern Sweden 2 to 4 years after introduction of PCV13. J Infect. 2021;83(2):190-6.  https://doi.org/10.1016/j.jinf.2021.05.031  PMID: 34062179 
  12. Forstner C, Kolditz M, Kesselmeier M, Ewig S, Rohde G, Barten-Neiner G, et al. Pneumococcal conjugate serotype distribution and predominating role of serotype 3 in German adults with community-acquired pneumonia. Vaccine. 2020;38(5):1129-36.  https://doi.org/10.1016/j.vaccine.2019.11.026  PMID: 31761500 
  13. Janssens A, Vaes B, Abels C, Crèvecoeur J, Mamouris P, Merckx B, et al. Pneumococcal vaccination coverage and adherence to recommended dosing schedules in adults: a repeated cross-sectional study of the INTEGO morbidity registry. BMC Public Health. 2023;23(1):1104.  https://doi.org/10.1186/s12889-023-15939-7  PMID: 37286969 
  14. Boey L, Bosmans E, Ferreira LB, Heyvaert N, Nelen M, Smans L, et al. Vaccination coverage of recommended vaccines and determinants of vaccination in at-risk groups. Hum Vaccin Immunother. 2020;16(9):2136-43.  https://doi.org/10.1080/21645515.2020.1763739  PMID: 32614656 
  15. Desmet S, Verhaegen J, Van Ranst M, Peetermans W, Lagrou K. Switch in a childhood pneumococcal vaccination programme from PCV13 to PCV10: a defendable approach? Lancet Infect Dis. 2018;18(8):830-1.  https://doi.org/10.1016/S1473-3099(18)30346-3  PMID: 30001857 
  16. Wouters I, Desmet S, Van Heirstraeten L, Herzog SA, Beutels P, Verhaegen J, et al. 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):1900303.  https://doi.org/10.2807/1560-7917.ES.2020.25.5.1900303  PMID: 32046817 
  17. Ekinci E, Van Heirstraeten L, Willen L, Desmet S, Wouters I, Vermeulen H, et al. , NP Carriage Study Group. Serotype 19A and 6C account for one third of pneumococcal carriage among Belgian day-care children four years after a shift to a lower-valent PCV. J Pediatric Infect Dis Soc. 2023;12(1):36-42.  https://doi.org/10.1093/jpids/piac117  PMID: 36377804 
  18. Desmet S, Wouters I, Heirstraeten LV, Beutels P, Van Damme P, Malhotra-Kumar S, et al. In-depth analysis of pneumococcal serotypes in Belgian children (2015-2018): Diversity, invasive disease potential, and antimicrobial susceptibility in carriage and disease. Vaccine. 2021;39(2):372-9.  https://doi.org/10.1016/j.vaccine.2020.11.044  PMID: 33308889 
  19. Ekinci E, Desmet S, Van Heirstraeten L, Mertens C, Wouters I, Beutels P, et al. Streptococcus pneumoniae serotypes carried by young children and their association with acute otitis media during the period 2016-2019. Front Pediatr. 2021;9:664083.  https://doi.org/10.3389/fped.2021.664083  PMID: 34291017 
  20. Lewnard JA, Hong V, Bruxvoort KJ, Grant LR, Jódar L, Cané A, et al. Burden of lower respiratory tract infections preventable by adult immunization with 15- and 20-valent pneumococcal conjugate vaccines in the United States. Clin Infect Dis. 2023;77(9):1340-52.  https://doi.org/10.1093/cid/ciad355  PMID: 37293708 
  21. Platt HL, Cardona JF, Haranaka M, Schwartz HI, Narejos Perez S, Dowell A, et al. A phase 3 trial of safety, tolerability, and immunogenicity of V114, 15-valent pneumococcal conjugate vaccine, compared with 13-valent pneumococcal conjugate vaccine in adults 50 years of age and older (PNEU-AGE). Vaccine. 2022;40(1):162-72.  https://doi.org/10.1016/j.vaccine.2021.08.049  PMID: 34507861 
  22. Cannon K, Cardona JF, Yacisin K, Thompson A, Belanger TJ, Lee D-Y, et al. Safety and immunogenicity of a 20-valent pneumococcal conjugate vaccine coadministered with quadrivalent influenza vaccine: A phase 3 randomized trial. Vaccine. 2023;41(13):2137-46.  https://doi.org/10.1016/j.vaccine.2022.11.046  PMID: 36828719 
  23. Fairman J, Agarwal P, Barbanel S, Behrens C, Berges A, Burky J, et al. Non-clinical immunological comparison of a Next-Generation 24-valent pneumococcal conjugate vaccine (VAX-24) using site-specific carrier protein conjugation to the current standard of care (PCV13 and PPV23). Vaccine. 2021;39(23):3197-206.  https://doi.org/10.1016/j.vaccine.2021.03.070  PMID: 33965258 
  24. Simon MW, Bataille R, Caldwell NS, Gessner BD, Jodar L, Lamberth E, et al. Safety and immunogenicity of a multivalent pneumococcal conjugate vaccine given with 13-valent pneumococcal conjugate vaccine in healthy infants: A phase 2 randomized trial. Hum Vaccin Immunother. 2023;19(2):2245727.  https://doi.org/10.1080/21645515.2023.2245727  PMID: 37927075 
  25. McGuinness D, Kaufhold RM, McHugh PM, Winters MA, Smith WJ, Giovarelli C, et al. Immunogenicity of PCV24, an expanded pneumococcal conjugate vaccine, in adult monkeys and protection in mice. Vaccine. 2021;39(30):4231-7.  https://doi.org/10.1016/j.vaccine.2021.04.067  PMID: 34074546 
  26. Platt H, Omole T, Cardona J, Fraser NJ, Mularski RA, Andrews C, et al. Safety, tolerability, and immunogenicity of a 21-valent pneumococcal conjugate vaccine, V116, in healthy adults: phase 1/2, randomised, double-blind, active comparator-controlled, multicentre, US-based trial. Lancet Infect Dis. 2023;23(2):233-46.  https://doi.org/10.1016/S1473-3099(22)00526-6  PMID: 36116461 
  27. Bonten MJM, Huijts SM, Bolkenbaas M, Webber C, Patterson S, Gault S, et al. Polysaccharide conjugate vaccine against pneumococcal pneumonia in adults. N Engl J Med. 2015;372(12):1114-25.  https://doi.org/10.1056/NEJMoa1408544  PMID: 25785969 
  28. Lund E. Laboratory diagnosis of Pneumococcus infections. Bull World Health Organ. 1960;23(1):5-13. PMID: 14418893 
  29. 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 
  30. Metcalf BJ, Waldetoft KW, Beall BW, Brown SP. Variation in pneumococcal invasiveness metrics is driven by serotype carriage duration and initial risk of disease. Epidemics. 2023;45(45):100731.  https://doi.org/10.1016/j.epidem.2023.100731  PMID: 38039595 
  31. Vanhoof R, Camps K, Carpentier M, De Craeye S, Frans J, Glupczynski Y, et al. 10th survey of antimicrobial resistance in noninvasive clinical isolates of Streptococcus pneumoniae collected in Belgium during winter 2007-2008. Pathol Biol (Paris). 2010;58(2):147-51.  https://doi.org/10.1016/j.patbio.2009.07.018  PMID: 19892491 
  32. Passaris I, Mauder N, Kostrzewa M, Burckhardt I, Zimmermann S, van Sorge NM, et al. Validation of fourier transform infrared spectroscopy for serotyping of Streptococcus pneumoniae. J Clin Microbiol. 2022;60(7):e0032522.  https://doi.org/10.1128/jcm.00325-22  PMID: 35699436 
  33. National Reference Center for invasive Streptococcus pneumoniae invasive (NRC). Report National Reference Centre Streptococcus pneumoniae 2021 and 2022. Leuven: NRC. [Accessed: 9 Oct 2024]. Available from: https://www.sciensano.be/en/nrc-nrl/national-reference-center-nrc-streptococcus-pneumoniae-invasive
  34. Hausdorff WP, Bryant J, Paradiso PR, Siber GR. Which pneumococcal serogroups cause the most invasive disease: implications for conjugate vaccine formulation and use, part I. Clin Infect Dis. 2000;30(1):100-21.  https://doi.org/10.1086/313608  PMID: 10619740 
  35. Løchen A, Truscott JE, Croucher NJ. Analysing pneumococcal invasiveness using Bayesian models of pathogen progression rates. PLOS Comput Biol. 2022;18(2):e1009389.  https://doi.org/10.1371/journal.pcbi.1009389  PMID: 35176026 
  36. Dagan R, Pelton S, Bakaletz L, Cohen R. Prevention of early episodes of otitis media by pneumococcal vaccines might reduce progression to complex disease. Lancet Infect Dis. 2016;16(4):480-92.  https://doi.org/10.1016/S1473-3099(15)00549-6  PMID: 27036355 
  37. Feemster K, Hausdorff WP, Banniettis N, Platt H, Velentgas P, Esteves-Jaramillo A, et al. Implications of cross-reactivity and cross-protection for pneumococcal vaccine development. Vaccines (Basel). 2024;12(9):974.  https://doi.org/10.3390/vaccines12090974  PMID: 39340006 
  38. Luck JN, Tettelin H, Orihuela CJ. Sugar-coated killer: serotype 3 pneumococcal disease. Front Cell Infect Microbiol. 2020;10:613287.  https://doi.org/10.3389/fcimb.2020.613287  PMID: 33425786 
  39. Melin M, Jarva H, Siira L, Meri S, Käyhty H, Väkeväinen M. Streptococcus pneumoniae capsular serotype 19F is more resistant to C3 deposition and less sensitive to opsonophagocytosis than serotype 6B. Infect Immun. 2009;77(2):676-84.  https://doi.org/10.1128/IAI.01186-08  PMID: 19047408 
  40. Arends DW, Miellet WR, Langereis JD, Ederveen THA, van der Gaast-de Jongh CE, van Scherpenzeel M, et al. Examining the distribution and impact of single-nucleotide polymorphisms in the capsular locus of Streptococcus pneumoniae serotype 19A. Infect Immun. 2021;89(11):e0024621.  https://doi.org/10.1128/IAI.00246-21  PMID: 34251291 
  41. Weiser JN, Ferreira DM, Paton JC. Streptococcus pneumoniae: transmission, colonization and invasion. Nat Rev Microbiol. 2018;16(6):355-67.  https://doi.org/10.1038/s41579-018-0001-8  PMID: 29599457 
  42. Loughran AJ, Orihuela CJ, Tuomanen EI. Streptococcus pneumoniae: Invasion and Inflammation. Microbiol Spectr. 2019;7(2):10.1128.  https://doi.org/10.1128/microbiolspec.GPP3-0004-2018  PMID: 30873934 
  43. Hausdorff WP, Feikin DR, Klugman KP. Epidemiological differences among pneumococcal serotypes. Lancet Infect Dis. 2005;5(2):83-93.  https://doi.org/10.1016/S1473-3099(05)70083-9  PMID: 15680778 
  44. Brueggemann AB, Griffiths DT, Meats E, Peto T, Crook DW, Spratt BG. Clonal relationships between invasive and carriage Streptococcus pneumoniae and serotype- and clone-specific differences in invasive disease potential. J Infect Dis. 2003;187(9):1424-32.  https://doi.org/10.1086/374624  PMID: 12717624 
  45. Simell B, Auranen K, Käyhty H, Goldblatt D, Dagan R, O’Brien KL,, et al. 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 
  46. Fernández-Delgado L, Càmara J, González-Díaz A, Grau I, Shoji H, Tubau F, et al. Serotypes in adult pneumococcal pneumonia in Spain in the era of conjugate vaccines. Microorganisms. 2021;9(11):2245.  https://doi.org/10.3390/microorganisms9112245  PMID: 34835371 
  47. Silva-Costa C, Gomes-Silva J, Santos A, Ramirez M, Melo-Cristino J, Portuguese Group for the Study of Streptococcal Infections. Adult non-invasive pneumococcal pneumonia in Portugal is dominated by serotype 3 and non-PCV13 serotypes 3-years after near universal PCV13 use in children. Front Public Health. 2023;11:1279656.  https://doi.org/10.3389/fpubh.2023.1279656  PMID: 38186693 
  48. Shaw D, Abad R, Amin-Chowdhury Z, Bautista A, Bennett D, Broughton K, et al. Trends in invasive bacterial diseases during the first 2 years of the COVID-19 pandemic: analyses of prospective surveillance data from 30 countries and territories in the IRIS Consortium. Lancet Digit Health. 2023;5(9):e582-93.  https://doi.org/10.1016/S2589-7500(23)00108-5  PMID: 37516557 
  49. Brissac T, Martínez E, Kruckow KL, Riegler AN, Ganaie F, Im H, et al. Capsule promotes intracellular survival and vascular endothelial cell translocation during invasive pneumococcal disease. MBio. 2021;12(5):e0251621.  https://doi.org/10.1128/mBio.02516-21  PMID: 34634940 
  50. Kietzman CC, Gao G, Mann B, Myers L, Tuomanen EI. Dynamic capsule restructuring by the main pneumococcal autolysin LytA in response to the epithelium. Nat Commun. 2016;7(1):10859.  https://doi.org/10.1038/ncomms10859  PMID: 26924467 
  51. Rueff A-S, van Raaphorst R, Aggarwal SD, Santos-Moreno J, Laloux G, Schaerli Y, et al. Synthetic genetic oscillators demonstrate the functional importance of phenotypic variation in pneumococcal-host interactions. Nat Commun. 2023;14(1):7454.  https://doi.org/10.1038/s41467-023-43241-y  PMID: 37978173 
  52. Alghofaili F, Najmuldeen H, Kareem BO, Shlla B, Fernandes VE, Danielsen M, et al. Host stress signals stimulate pneumococcal transition from colonization to dissemination into the lungs. MBio. 2021;12(6):e0256921.  https://doi.org/10.1128/mBio.02569-21  PMID: 34696596 
  53. Glanville DG, Gazioglu O, Marra M, Tokars VL, Kushnir T, Habtom M, et al. Pneumococcal capsule expression is controlled through a conserved, distal cis-regulatory element during infection. PLoS Pathog. 2023;19(1):e1011035.  https://doi.org/10.1371/journal.ppat.1011035  PMID: 36719895 
  54. Gladstone RA, Lo SW, Lees JA, Croucher NJ, van Tonder AJ, Corander J, et al. International genomic definition of pneumococcal lineages, to contextualise disease, antibiotic resistance and vaccine impact. EBioMedicine. 2019;43:338-46.  https://doi.org/10.1016/j.ebiom.2019.04.021  PMID: 31003929 
  55. Obolski U, Gori A, Lourenço J, Thompson C, Thompson R, French N, et al. Identifying genes associated with invasive disease in S. pneumoniae by applying a machine learning approach to whole genome sequence typing data. Sci Rep. 2019;9(1):4049.  https://doi.org/10.1038/s41598-019-40346-7  PMID: 30858412 
  56. Jacques LC, Panagiotou S, Baltazar M, Senghore M, Khandaker S, Xu R, et al. Increased pathogenicity of pneumococcal serotype 1 is driven by rapid autolysis and release of pneumolysin. Nat Commun. 2020;11(1):1892.  https://doi.org/10.1038/s41467-020-15751-6  PMID: 32312961 
  57. Chaguza C, Yang M, Cornick JE, du Plessis M, Gladstone RA, Kwambana-Adams BA, et al. Bacterial genome-wide association study of hyper-virulent pneumococcal serotype 1 identifies genetic variation associated with neurotropism. Commun Biol. 2020;3(1):559.  https://doi.org/10.1038/s42003-020-01290-9  PMID: 33033372 
  58. Higgs C, Kumar LS, Stevens K, Strachan J, Korman T, Horan K, et al. Comparison of contemporary invasive and non-invasive Streptococcus pneumoniae isolates reveals new insights into circulating anti-microbial resistance determinants. Antimicrob Agents Chemother. 2023;67(11):e0078523.  https://doi.org/10.1128/aac.00785-23  PMID: 37823632 
  59. Bruyndonckx R, Coenen S, Hens N, Vandael E, Catry B, Goossens H. Antibiotic use and resistance in Belgium: the impact of two decades of multi-faceted campaigning. Acta Clin Belg. 2021;76(4):280-8.  https://doi.org/10.1080/17843286.2020.1721135  PMID: 32024450 
  60. Dewé TCM, D’Aeth JC, Croucher NJ. Genomic epidemiology of penicillin-non-susceptible Streptococcus pneumoniae. Microb Genom. 2019;5(10):e000305.  https://doi.org/10.1099/mgen.0.000305  PMID: 31609685 
  61. Andrejko K, Ratnasiri B, Lewnard JA. Association of pneumococcal serotype with susceptibility to antimicrobial drugs: a systematic review and meta-analysis. Clin Infect Dis. 2022;75(1):131-40.  https://doi.org/10.1093/cid/ciab852  PMID: 34599811 
  62. Brueggemann AB, Jansen van Rensburg MJ, Shaw D, McCarthy ND, Jolley KA, Maiden MCJ, et al. Changes in the incidence of invasive disease due to Streptococcus pneumoniae, Haemophilus influenzae, and Neisseria meningitidis during the COVID-19 pandemic in 26 countries and territories in the Invasive Respiratory Infection Surveillance Initiative: a prospective analysis of surveillance data. Lancet Digit Health. 2021;3(6):e360-70.  https://doi.org/10.1016/S2589-7500(21)00077-7  PMID: 34045002 
Non-invasive Streptococcus pneumoniae infections are associated with different serotypes than invasive infections, Belgium, 2020 to 2023
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Ioannis+Passaris&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Passaris Ioannis</a>, <a href="/search?value1=St%C3%A9phanie+Depick%C3%A8re&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Depickère Stéphanie</a>, <a href="/search?value1=Toon+Braeye&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Braeye Toon</a>, <a href="/search?value1=Marina+Mukovnikova&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mukovnikova Marina</a>, <a href="/search?value1=Alexandra+Vodolazkaia&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Vodolazkaia Alexandra</a>, <a href="/search?value1=Chlo%C3%A9+Abels&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Abels Chloé</a>, <a href="/search?value1=Lize+Cuypers&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cuypers Lize</a>, <a href="/search?value1=Stefanie+Desmet&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Desmet Stefanie</a>, <a href="/search?value1=Pieter-Jan+Ceyssens&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ceyssens Pieter-Jan</a>, <a href="/search?value1=NIPD+study+group+Belgium&option1=author&noRedirect=true" class="nonDisambigAuthorLink">NIPD study group Belgium</a></span>. Non-invasive Streptococcus pneumoniae infections are associated with different serotypes than invasive infections, Belgium, 2020 to 2023. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(45):pii=2400108. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.45.2400108" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.45.2400108</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 15 Feb 2024;&nbsp;&nbsp; <span class="generated">Accepted</span>: 02 May 2024 </span> </p>
/content/10.2807/1560-7917.ES.2024.29.45.2400108
/content/10.2807/1560-7917.ES.2024.29.45.2400108
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error