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PMID: 19521509 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Pneumococcal capsular polysaccharide structure predicts serotype prevalence.

PLoS pathogens ·Vol. 5 ·No. 6 ·2009-06-00 ·Pages e1000476

Weinberger DM, Trzciński K, Lu YJ, Bogaert D, Brandes A, Galagan J, Anderson PW, Malley R, Lipsitch M

Abstract

There are 91 known capsular serotypes of Streptococcus pneumoniae. The nasopharyngeal carriage prevalence of particular serotypes is relatively stable worldwide, but the host and bacterial factors that maintain these patterns are poorly understood. Given the possibility of serotype replacement following vaccination against seven clinically important serotypes, it is increasingly important to understand these factors. We hypothesized that the biochemical structure of the capsular polysaccharides could influence the degree of encapsulation of different serotypes, their susceptibility to killing by neutrophils, and ultimately their success during nasopharyngeal carriage. We sought to measure biological differences among capsular serotypes that may account for epidemiological patterns. Using an in vitro assay with both isogenic capsule-switch variants and clinical carriage isolates, we found an association between increased carriage prevalence and resistance to non-opsonic neutrophil-mediated killing, and serotypes that were resistant to neutrophil-mediated killing tended to be more heavily encapsulated, as determined by FITC-dextran exclusion. Next, we identified a link between polysaccharide structure and carriage prevalence. Significantly, non-vaccine serotypes that have become common in vaccinated populations tend to be those with fewer carbons per repeat unit and low energy expended per repeat unit, suggesting a novel biological principle to explain patterns of serotype replacement. More prevalent serotypes are more heavily encapsulated and more resistant to neutrophil-mediated killing, and these phenotypes are associated with the structure of the capsular polysaccharide, suggesting a direct relationship between polysaccharide biochemistry and the success of a serotype during nasopharyngeal carriage and potentially providing a method for predicting serotype replacement.

MeSH Terms
Animals Bacterial Capsules/chemistry,genetics Carrier State/immunology,microbiology Fructose/metabolism Glucose/metabolism Humans Linear Models Mice Mice, Inbred C57BL Neutrophils/immunology Pneumococcal Infections/epidemiology,immunology,microbiology Pneumococcal Vaccines/immunology Prevalence Serotyping Statistics, Nonparametric Streptococcus pneumoniae/classification,genetics,immunology,pathogenicity
Chemicals
Pneumococcal Vaccines Fructose Glucose
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Weinberger Daniel M
Department of Immunology and Infectious Diseases, Harvard School of Public Health, Boston, MA, USA.
Trzciński Krzysztof
Lu Ying-Jie
Bogaert Debby
Brandes Aaron
Galagan James
Anderson Porter W
Malley Richard
Lipsitch Marc
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Article Info
Journal
PLoS pathogens
Abbr.
PLoS Pathog
ISSN
1553-7374
Published
2009-06-00
Epub
2009-00-12
Pages
e1000476
Language
English
Region
United States
NLM ID
101238921
PMCID
PMC2689349
Subset
IM
Grants
NIAID NIH HHS · R01 AI048935 · United States
PHS HHS · T32 A1007535 · United States
NIAID NIH HHS · AI066013 · United States
NIAID NIH HHS · R01 AI066013 · United States
NIAID NIH HHS · R01 AI067737 · United States
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