<italic toggle="yes">Streptococcus pneumoniae</italic> Transmission Is Blocked by Type-Specific Immunity in an Infant Mouse Model

ABSTRACT Epidemiological studies on Streptococcus pneumoniae show that rates of carriage are highest in early childhood and that the major benefit of the pneumococcal conjugate vaccine (PCV) is a reduction in the incidence of nasopharyngeal colonization through decreased transmission within a popula...

Full description

Bibliographic Details
Main Authors: Tonia Zangari, Yang Wang, Jeffrey N. Weiser
Format: Article
Language:English
Published: American Society for Microbiology 2017-05-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mBio.00188-17
_version_ 1818893300195655680
author Tonia Zangari
Yang Wang
Jeffrey N. Weiser
author_facet Tonia Zangari
Yang Wang
Jeffrey N. Weiser
author_sort Tonia Zangari
collection DOAJ
description ABSTRACT Epidemiological studies on Streptococcus pneumoniae show that rates of carriage are highest in early childhood and that the major benefit of the pneumococcal conjugate vaccine (PCV) is a reduction in the incidence of nasopharyngeal colonization through decreased transmission within a population. In this study, we sought to understand how anti-S. pneumoniae immunity affects nasal shedding of bacteria, the limiting step in experimental pneumococcal transmission. Using an infant mouse model, we examined the role of immunity (passed from mother to pup) on shedding and within-litter transmission of S. pneumoniae by pups infected at 4 days of life. Pups from both previously colonized immune and PCV-vaccinated mothers had higher levels of anti-S. pneumoniae IgG than pups from non-immune or non-vaccinated mothers and shed significantly fewer S. pneumoniae over the first 5 days of infection. By setting up cross-foster experiments, we demonstrated that maternal passage of antibody to pups either in utero or post-natally decreases S. pneumoniae shedding. Passive immunization experiments showed that type-specific antibody to capsular polysaccharide is sufficient to decrease shedding and that the agglutinating function of immunoglobulin is required for this effect. Finally, we established that anti-pneumococcal immunity and anti-PCV vaccination block host-to-host transmission of S. pneumoniae. Moreover, immunity in either the donor or recipient pups alone was sufficient to reduce rates of transmission, indicating that decreased shedding and protection from acquisition of colonization are both contributing factors. Our findings provide a mechanistic explanation for the reduced levels of S. pneumoniae transmission between hosts immune from prior exposure and among vaccinated children. IMPORTANCE Rates of carriage of the bacterial pathogen Streptococcus pneumoniae are highest among young children, and this is the target group for the pneumococcal conjugate vaccine (PCV). Epidemiological studies have suggested that a major benefit of the PCV is a reduction in host-to-host transmission, which also protects the non-vaccinated population (“herd immunity”). In this study, we examined the role of anti-pneumococcal immunity on nasal shedding and transmission of the pathogen using an infant mouse model. We found that shedding is decreased and transmission is blocked by anti-pneumococcal immunity and PCV vaccination. Additionally, transmission rates decreased if either the infected or contact pups were immune, indicating that reduced shedding and protection from the establishment of colonization are both contributing factors. Our study provides a mechanistic explanation for the herd immunity effect seen after the introduction of PCV and identifies potential points of intervention, which may have implications for future vaccine development.
first_indexed 2024-12-19T18:10:24Z
format Article
id doaj.art-4aa194b8be7945df9ac80a30d73e9887
institution Directory Open Access Journal
issn 2150-7511
language English
last_indexed 2024-12-19T18:10:24Z
publishDate 2017-05-01
publisher American Society for Microbiology
record_format Article
series mBio
spelling doaj.art-4aa194b8be7945df9ac80a30d73e98872022-12-21T20:11:20ZengAmerican Society for MicrobiologymBio2150-75112017-05-018210.1128/mBio.00188-17<italic toggle="yes">Streptococcus pneumoniae</italic> Transmission Is Blocked by Type-Specific Immunity in an Infant Mouse ModelTonia Zangari0Yang Wang1Jeffrey N. Weiser2Department of Microbiology, New York University School of Medicine, New York, New York, USADepartment of Microbiology, New York University School of Medicine, New York, New York, USADepartment of Microbiology, New York University School of Medicine, New York, New York, USAABSTRACT Epidemiological studies on Streptococcus pneumoniae show that rates of carriage are highest in early childhood and that the major benefit of the pneumococcal conjugate vaccine (PCV) is a reduction in the incidence of nasopharyngeal colonization through decreased transmission within a population. In this study, we sought to understand how anti-S. pneumoniae immunity affects nasal shedding of bacteria, the limiting step in experimental pneumococcal transmission. Using an infant mouse model, we examined the role of immunity (passed from mother to pup) on shedding and within-litter transmission of S. pneumoniae by pups infected at 4 days of life. Pups from both previously colonized immune and PCV-vaccinated mothers had higher levels of anti-S. pneumoniae IgG than pups from non-immune or non-vaccinated mothers and shed significantly fewer S. pneumoniae over the first 5 days of infection. By setting up cross-foster experiments, we demonstrated that maternal passage of antibody to pups either in utero or post-natally decreases S. pneumoniae shedding. Passive immunization experiments showed that type-specific antibody to capsular polysaccharide is sufficient to decrease shedding and that the agglutinating function of immunoglobulin is required for this effect. Finally, we established that anti-pneumococcal immunity and anti-PCV vaccination block host-to-host transmission of S. pneumoniae. Moreover, immunity in either the donor or recipient pups alone was sufficient to reduce rates of transmission, indicating that decreased shedding and protection from acquisition of colonization are both contributing factors. Our findings provide a mechanistic explanation for the reduced levels of S. pneumoniae transmission between hosts immune from prior exposure and among vaccinated children. IMPORTANCE Rates of carriage of the bacterial pathogen Streptococcus pneumoniae are highest among young children, and this is the target group for the pneumococcal conjugate vaccine (PCV). Epidemiological studies have suggested that a major benefit of the PCV is a reduction in host-to-host transmission, which also protects the non-vaccinated population (“herd immunity”). In this study, we examined the role of anti-pneumococcal immunity on nasal shedding and transmission of the pathogen using an infant mouse model. We found that shedding is decreased and transmission is blocked by anti-pneumococcal immunity and PCV vaccination. Additionally, transmission rates decreased if either the infected or contact pups were immune, indicating that reduced shedding and protection from the establishment of colonization are both contributing factors. Our study provides a mechanistic explanation for the herd immunity effect seen after the introduction of PCV and identifies potential points of intervention, which may have implications for future vaccine development.https://journals.asm.org/doi/10.1128/mBio.00188-17PCVStreptococcus pneumoniaeimmunitytransmission
spellingShingle Tonia Zangari
Yang Wang
Jeffrey N. Weiser
<italic toggle="yes">Streptococcus pneumoniae</italic> Transmission Is Blocked by Type-Specific Immunity in an Infant Mouse Model
mBio
PCV
Streptococcus pneumoniae
immunity
transmission
title <italic toggle="yes">Streptococcus pneumoniae</italic> Transmission Is Blocked by Type-Specific Immunity in an Infant Mouse Model
title_full <italic toggle="yes">Streptococcus pneumoniae</italic> Transmission Is Blocked by Type-Specific Immunity in an Infant Mouse Model
title_fullStr <italic toggle="yes">Streptococcus pneumoniae</italic> Transmission Is Blocked by Type-Specific Immunity in an Infant Mouse Model
title_full_unstemmed <italic toggle="yes">Streptococcus pneumoniae</italic> Transmission Is Blocked by Type-Specific Immunity in an Infant Mouse Model
title_short <italic toggle="yes">Streptococcus pneumoniae</italic> Transmission Is Blocked by Type-Specific Immunity in an Infant Mouse Model
title_sort italic toggle yes streptococcus pneumoniae italic transmission is blocked by type specific immunity in an infant mouse model
topic PCV
Streptococcus pneumoniae
immunity
transmission
url https://journals.asm.org/doi/10.1128/mBio.00188-17
work_keys_str_mv AT toniazangari italictoggleyesstreptococcuspneumoniaeitalictransmissionisblockedbytypespecificimmunityinaninfantmousemodel
AT yangwang italictoggleyesstreptococcuspneumoniaeitalictransmissionisblockedbytypespecificimmunityinaninfantmousemodel
AT jeffreynweiser italictoggleyesstreptococcuspneumoniaeitalictransmissionisblockedbytypespecificimmunityinaninfantmousemodel