Lower Density and Shorter Duration of Nasopharyngeal Carriage by Pneumococcal Serotype 1 (ST217) May Explain Its Increased Invasiveness over Other Serotypes

ABSTRACT Streptococcus pneumoniae is a frequent colonizer of the human nasopharynx and a major cause of life-threating invasive infections such as pneumonia, meningitis and sepsis. Over 1 million people die every year due to invasive pneumococcal disease (IPD), mainly in developing countries. Seroty...

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Autores principales:	Laura Bricio-Moreno, Chrispin Chaguza, Reham Yahya, Rebecca K. Shears, Jennifer E. Cornick, Karsten Hokamp, Marie Yang, Daniel R. Neill, Neil French, Jay C. D. Hinton, Dean B. Everett, Aras Kadioglu
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	pneumococcus serotype 1 murine model colonization pneumonia respiratory infection Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d130bf11bdac4f6db9ab76bb89201d2d
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spelling	oai:doaj.org-article:d130bf11bdac4f6db9ab76bb89201d2d2021-11-15T15:55:44ZLower Density and Shorter Duration of Nasopharyngeal Carriage by Pneumococcal Serotype 1 (ST217) May Explain Its Increased Invasiveness over Other Serotypes10.1128/mBio.00814-202150-7511https://doaj.org/article/d130bf11bdac4f6db9ab76bb89201d2d2020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00814-20https://doaj.org/toc/2150-7511ABSTRACT Streptococcus pneumoniae is a frequent colonizer of the human nasopharynx and a major cause of life-threating invasive infections such as pneumonia, meningitis and sepsis. Over 1 million people die every year due to invasive pneumococcal disease (IPD), mainly in developing countries. Serotype 1 is a common cause of IPD; however, unlike other serotypes, it is rarely found in the carrier state in the nasopharynx, which is often considered a prerequisite for disease. The aim of this study was to understand this dichotomy. We used murine models of carriage and IPD to characterize the pathogenesis of African serotype 1 (sequence type 217) pneumococcal strains obtained from the Queen Elizabeth Central Hospital in Blantyre, Malawi. We found that ST217 pneumococcal strains were highly virulent in a mouse model of invasive pneumonia, but in contrast to the generally accepted assumption, can also successfully establish nasopharyngeal carriage. Interestingly, we found that cocolonizing serotypes may proliferate in the presence of serotype 1, suggesting that acquisition of serotype 1 carriage could increase the risk of developing IPD by other serotypes. RNA sequencing analysis confirmed that key virulence genes associated with inflammation and tissue invasiveness were upregulated in serotype 1. These data reveal important new insights into serotype 1 pathogenesis, with implications for carriage potential and risk of invasive disease through interactions with other cocolonizing serotypes, an often-overlooked factor in transmission and disease progression. IMPORTANCE The pneumococcus causes serious diseases such as pneumonia, sepsis, and meningitis and is a major cause of morbidity and mortality worldwide. Serotype 1 accounts for the majority of invasive pneumococcal disease cases in sub-Saharan Africa but is rarely found during nasopharyngeal carriage. Understanding the mechanisms leading to nasopharyngeal carriage and invasive disease by this serotype can help reduce its burden on health care systems worldwide. In this study, we also uncovered the potential impact of serotype 1 on disease progression of other coinfecting serotypes, which can have important implications for vaccine efficacy. Understanding the interactions between different serotypes during nasopharyngeal carriage may lead to improved intervention methods and therapies to reduce pneumococcal invasive disease levels.Laura Bricio-MorenoChrispin ChaguzaReham YahyaRebecca K. ShearsJennifer E. CornickKarsten HokampMarie YangDaniel R. NeillNeil FrenchJay C. D. HintonDean B. EverettAras KadiogluAmerican Society for Microbiologyarticlepneumococcusserotype 1murine modelcolonizationpneumoniarespiratory infectionMicrobiologyQR1-502ENmBio, Vol 11, Iss 6 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	pneumococcus serotype 1 murine model colonization pneumonia respiratory infection Microbiology QR1-502
spellingShingle	pneumococcus serotype 1 murine model colonization pneumonia respiratory infection Microbiology QR1-502 Laura Bricio-Moreno Chrispin Chaguza Reham Yahya Rebecca K. Shears Jennifer E. Cornick Karsten Hokamp Marie Yang Daniel R. Neill Neil French Jay C. D. Hinton Dean B. Everett Aras Kadioglu Lower Density and Shorter Duration of Nasopharyngeal Carriage by Pneumococcal Serotype 1 (ST217) May Explain Its Increased Invasiveness over Other Serotypes
description	ABSTRACT Streptococcus pneumoniae is a frequent colonizer of the human nasopharynx and a major cause of life-threating invasive infections such as pneumonia, meningitis and sepsis. Over 1 million people die every year due to invasive pneumococcal disease (IPD), mainly in developing countries. Serotype 1 is a common cause of IPD; however, unlike other serotypes, it is rarely found in the carrier state in the nasopharynx, which is often considered a prerequisite for disease. The aim of this study was to understand this dichotomy. We used murine models of carriage and IPD to characterize the pathogenesis of African serotype 1 (sequence type 217) pneumococcal strains obtained from the Queen Elizabeth Central Hospital in Blantyre, Malawi. We found that ST217 pneumococcal strains were highly virulent in a mouse model of invasive pneumonia, but in contrast to the generally accepted assumption, can also successfully establish nasopharyngeal carriage. Interestingly, we found that cocolonizing serotypes may proliferate in the presence of serotype 1, suggesting that acquisition of serotype 1 carriage could increase the risk of developing IPD by other serotypes. RNA sequencing analysis confirmed that key virulence genes associated with inflammation and tissue invasiveness were upregulated in serotype 1. These data reveal important new insights into serotype 1 pathogenesis, with implications for carriage potential and risk of invasive disease through interactions with other cocolonizing serotypes, an often-overlooked factor in transmission and disease progression. IMPORTANCE The pneumococcus causes serious diseases such as pneumonia, sepsis, and meningitis and is a major cause of morbidity and mortality worldwide. Serotype 1 accounts for the majority of invasive pneumococcal disease cases in sub-Saharan Africa but is rarely found during nasopharyngeal carriage. Understanding the mechanisms leading to nasopharyngeal carriage and invasive disease by this serotype can help reduce its burden on health care systems worldwide. In this study, we also uncovered the potential impact of serotype 1 on disease progression of other coinfecting serotypes, which can have important implications for vaccine efficacy. Understanding the interactions between different serotypes during nasopharyngeal carriage may lead to improved intervention methods and therapies to reduce pneumococcal invasive disease levels.
format	article
author	Laura Bricio-Moreno Chrispin Chaguza Reham Yahya Rebecca K. Shears Jennifer E. Cornick Karsten Hokamp Marie Yang Daniel R. Neill Neil French Jay C. D. Hinton Dean B. Everett Aras Kadioglu
author_facet	Laura Bricio-Moreno Chrispin Chaguza Reham Yahya Rebecca K. Shears Jennifer E. Cornick Karsten Hokamp Marie Yang Daniel R. Neill Neil French Jay C. D. Hinton Dean B. Everett Aras Kadioglu
author_sort	Laura Bricio-Moreno
title	Lower Density and Shorter Duration of Nasopharyngeal Carriage by Pneumococcal Serotype 1 (ST217) May Explain Its Increased Invasiveness over Other Serotypes
title_short	Lower Density and Shorter Duration of Nasopharyngeal Carriage by Pneumococcal Serotype 1 (ST217) May Explain Its Increased Invasiveness over Other Serotypes
title_full	Lower Density and Shorter Duration of Nasopharyngeal Carriage by Pneumococcal Serotype 1 (ST217) May Explain Its Increased Invasiveness over Other Serotypes
title_fullStr	Lower Density and Shorter Duration of Nasopharyngeal Carriage by Pneumococcal Serotype 1 (ST217) May Explain Its Increased Invasiveness over Other Serotypes
title_full_unstemmed	Lower Density and Shorter Duration of Nasopharyngeal Carriage by Pneumococcal Serotype 1 (ST217) May Explain Its Increased Invasiveness over Other Serotypes
title_sort	lower density and shorter duration of nasopharyngeal carriage by pneumococcal serotype 1 (st217) may explain its increased invasiveness over other serotypes
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/d130bf11bdac4f6db9ab76bb89201d2d
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Lower Density and Shorter Duration of Nasopharyngeal Carriage by Pneumococcal Serotype 1 (ST217) May Explain Its Increased Invasiveness over Other Serotypes

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