Molecular characterization and epidemiology of <i>Streptococcus pneumoniae</i> serotype 8 in Denmark

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Abstract

Background

Streptococcus pneumoniae serotype 8 incidence has increased in Denmark after the introduction of pneumococcal conjugated vaccines (PCV). The mechanism behind the serotype 8 replacement is not well understood. In this study, we aimed to present epidemiological data on invasive pneumococcal disease (IPD) and molecular characterization of 96 serotype 8 clinical isolates.

Methods

IPD data from 1999 to 2019 were used to calculate the incidence and age distribution. Whole-genome sequencing (WGS) analysis was performed on 96 isolates (6.8% of the total serotype 8 IPD isolates in the period) to characterize the isolates with respect to pneumococcal lineage traits, a range of genes with potential species discrimination, presence of colonization and virulence factors, and molecular resistance pattern.

Results

The serotype 8 IPD incidence increased significantly ( P < 0.05) for the age groups above 15 years after the introduction of PCV13, primarily affecting the elderly (65+). All isolates were phenotypically susceptible to penicillin, erythromycin and clindamycin.

Molecular characterization revealed seven different MLST profiles with ST53 as the most prevalent lineage (87.5%) among the analyzed serotype 8 isolates. The genes covering the cell-surface proteins: lytA, rspB, pspA, psaA & Xisco and the pneumococcal toxin pneumolysin = ply were present in all isolates, while genes for the membrane transporter proteins: piaA/piaB/piaC; the capsular genes: cpsA (wzg) & psrP; the metallo-binding proteins zmpB & zmpC; and the neuroamidase proteins: nanA/nanB were variably present. Surprisingly, the putative transcriptional regulator gene SP2020 was not present in all isolates (98%). Susceptibility to penicillin, erythromycin and clindamycin was molecularly confirmed.

Conclusion

The observed serotype 8 replacement was not significantly reflected with a change in the MLST profile or changes in antibiotic resistance- or virulence determinants.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12879-021-06103-w.

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Most cited references 45

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Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain

Keith Jolley, Carly M. Bliss, Julia S. Bennett … (2012)

No single genealogical reconstruction or typing method currently encompasses all levels of bacterial diversity, from domain to strain. We propose ribosomal multilocus sequence typing (rMLST), an approach which indexes variation of the 53 genes encoding the bacterial ribosome protein subunits (rps genes), as a means of integrating microbial genealogy and typing. As with multilocus sequence typing (MLST), rMLST employs curated reference sequences to identify gene variants efficiently and rapidly. The rps loci are ideal targets for a universal characterization scheme as they are: (i) present in all bacteria; (ii) distributed around the chromosome; and (iii) encode proteins which are under stabilizing selection for functional conservation. Collectively, the rps loci exhibit variation that resolves bacteria into groups at all taxonomic and most typing levels, providing significantly more resolution than 16S small subunit rRNA gene phylogenies. A web-accessible expandable database, comprising whole-genome data from more than 1900 bacterial isolates, including 28 draft genomes assembled de novo from the European Bioinformatics Institute (EBI) sequence read archive, has been assembled. The rps gene variation catalogued in this database permits rapid and computationally non-intensive identification of the phylogenetic position of any bacterial sequence at the domain, phylum, class, order, family, genus, species and strain levels. The groupings generated with rMLST data are consistent with current nomenclature schemes and independent of the clustering algorithm used. This approach is applicable to the other domains of life, potentially providing a rational and universal approach to the classification of life that is based on one of its fundamental features, the translation mechanism.

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SKESA: strategic k-mer extension for scrupulous assemblies

Alexandre Souvorov, Richa Agarwala, David Lipman (2018)

SKESA is a DeBruijn graph-based de-novo assembler designed for assembling reads of microbial genomes sequenced using Illumina. Comparison with SPAdes and MegaHit shows that SKESA produces assemblies that have high sequence quality and contiguity, handles low-level contamination in reads, is fast, and produces an identical assembly for the same input when assembled multiple times with the same or different compute resources. SKESA has been used for assembling over 272,000 read sets in the Sequence Read Archive at NCBI and for real-time pathogen detection. Source code for SKESA is freely available at https://github.com/ncbi/SKESA/releases. Electronic supplementary material The online version of this article (10.1186/s13059-018-1540-z) contains supplementary material, which is available to authorized users.

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Evaluation and improvement of real-time PCR assays targeting lytA, ply, and psaA genes for detection of pneumococcal DNA.

Maria da Glória S. Carvalho, Maria Tondella, Karen McCaustland … (2007)

The accurate diagnosis of pneumococcal disease has frequently been hampered not only by the difficulties in obtaining isolates of the organism from patient specimens but also by the misidentification of pneumococcus-like viridans group streptococci (P-LVS) as Streptococcus pneumoniae. This is especially critical when the specimen comes from the respiratory tract. In this study, three novel real-time PCR assays designed for the detection of specific sequence regions of the lytA, ply, and psaA genes were developed (lytA-CDC, ply-CDC, and psaA, respectively). These assays showed high sensitivity (<10 copies for lytA-CDC and ply-CDC and an approximately twofold less sensitivity for psaA). Two additional real-time PCR assays for lytA and ply described previously for pneumococcal DNA detection were also evaluated. A panel of isolates consisting of 67 S. pneumoniae isolates (44 different serotypes and 3 nonencapsulated S. pneumoniae isolates from conjunctivitis outbreaks) and 104 nonpneumococcal isolates was used. The 67 S. pneumoniae isolates were reactive in all five assays. The new real-time detection assays targeting the lytA and psaA genes were the most specific for the detection of isolates confirmed to be S. pneumoniae, with lytA-CDC showing the greatest specificity. Both ply PCRs were positive for all isolates of S. pseudopneumoniae, along with 13 other isolates of other P-LVS isolates confirmed to be non-S. pneumoniae by DNA-DNA reassociation. Thus, the use of the ply gene for the detection of pneumococci can lead to false-positive reactions in the presence of P-LVS. The five assays were applied to 15 culture-positive cerebrospinal fluid specimens with 100% sensitivity; and serum and ear fluid specimens were also evaluated. Both the lytA-CDC and psaA assays, particularly the lytA-CDC assay, have improved specificities compared with those of currently available assays and should therefore be considered the assays of choice for the detection of pneumococcal DNA, particularly when upper respiratory P-LVS might be present in the clinical specimen.

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Author and article information

Contributors

H-C Slotved:

ORCID: http://orcid.org/0000-0002-7294-4911

hcs@ssi.dk

Journal

Journal ID (nlm-ta): BMC Infect Dis

Journal ID (iso-abbrev): BMC Infect Dis

Title: BMC Infectious Diseases

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2334

Publication date (Electronic): 5 May 2021

Publication date PMC-release: 5 May 2021

Publication date Collection: 2021

Volume: 21

Electronic Location Identifier: 421

Affiliations

[1 ]GRID grid.6203.7, ISNI 0000 0004 0417 4147, Department of Bacteria, Parasites and Fungi, , Statens Serum Institut, ; Artillerivej 5, DK-2300 Copenhagen S, Denmark

[2 ]GRID grid.6203.7, ISNI 0000 0004 0417 4147, Infectious Disease Epidemiology and Prevention, , Statens Serum Institut, ; Copenhagen, Denmark

[3 ]GRID grid.6203.7, ISNI 0000 0004 0417 4147, Department of Virus and Microbiological Special Diagnostics, , Statens Serum Institut, ; Copenhagen, Denmark

Author information

H-C Slotved http://orcid.org/0000-0002-7294-4911

Article

Publisher ID: 6103

DOI: 10.1186/s12879-021-06103-w

PMC ID: 8097992

PubMed ID: 33952197

SO-VID: 6bca9a78-1466-4be4-a13d-44261f3d1fe4

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 11 January 2021

Date accepted : 22 April 2021

Custom metadata

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: denmark,whole genome sequencing,mlst,serotype 8,ipd,pcv13,streptococcus pneumoniae

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ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: denmark, whole genome sequencing, mlst, serotype 8, ipd, pcv13, streptococcus pneumoniae

Molecular characterization and epidemiology of Streptococcus pneumoniae serotype 8 in Denmark

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Supplementary Information

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Coronaviruses, COVID-19 and SARS-CoV-2

Most cited references 45

Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain

SKESA: strategic k-mer extension for scrupulous assemblies

Evaluation and improvement of real-time PCR assays targeting lytA, ply, and psaA genes for detection of pneumococcal DNA.

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