Impact of age on pneumococcal colonization of the nasopharynx and oral cavity: an ecological perspective.

IF 5.1 Q1 ECOLOGY ISME communications Pub Date : 2024-01-12 eCollection Date: 2024-01-01 DOI:10.1093/ismeco/ycae002
Willem R Miellet, Rob Mariman, Janieke van Veldhuizen, Paul Badoux, Alienke J Wijmenga-Monsuur, David Litt, Thijs Bosch, Elizabeth Miller, Norman K Fry, Marianne A van Houten, Nynke Y Rots, Elisabeth A M Sanders, Krzysztof Trzciński
{"title":"Impact of age on pneumococcal colonization of the nasopharynx and oral cavity: an ecological perspective.","authors":"Willem R Miellet, Rob Mariman, Janieke van Veldhuizen, Paul Badoux, Alienke J Wijmenga-Monsuur, David Litt, Thijs Bosch, Elizabeth Miller, Norman K Fry, Marianne A van Houten, Nynke Y Rots, Elisabeth A M Sanders, Krzysztof Trzciński","doi":"10.1093/ismeco/ycae002","DOIUrl":null,"url":null,"abstract":"<p><p>Pneumococcal carriage studies have suggested that pneumococcal colonization in adults is largely limited to the oral cavity and oropharynx. In this study, we used total abundance-based β-diversity (dissimilarity) and β-diversity components to characterize age-related differences in pneumococcal serotype composition of respiratory samples. quantitative PCR (qPCR) was applied to detect pneumococcal serotypes in nasopharyngeal samples collected from 946 toddlers and 602 adults, saliva samples collected from a subset of 653 toddlers, and saliva and oropharyngeal samples collected from a subset of 318 adults. Bacterial culture rates from nasopharyngeal samples were used to characterize age-related differences in rates of colonizing bacteria. Dissimilarity in pneumococcal serotype composition was low among saliva and nasopharyngeal samples from children. In contrast, respiratory samples from adults exhibited high serotype dissimilarity, which predominantly consisted of abundance gradients and was associated with reduced nasopharyngeal colonization. Age-related serotype dissimilarity was high among nasopharyngeal samples and relatively low for saliva samples. Reduced nasopharyngeal colonization by pneumococcal serotypes coincided with significantly reduced <i>Moraxella catarrhalis</i> and <i>Haemophilus influenzae</i> and increased <i>Staphylococcus aureus</i> nasopharyngeal colonization rates among adults. Findings from this study suggest that within-host environmental conditions, utilized in the upper airways by pneumococcus and other bacteria, undergo age-related changes. It may result in a host-driven ecological succession of bacterial species colonizing the nasopharynx and lead to competitive exclusion of pneumococcus from the nasopharynx but not from the oral habitat. This explains the poor performance of nasopharyngeal samples for pneumococcal carriage among adults and indicates that in adults saliva more accurately represents the epidemiology of pneumococcal carriage than nasopharyngeal samples.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae002"},"PeriodicalIF":5.1000,"publicationDate":"2024-01-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10881297/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"ISME communications","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/ismeco/ycae002","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"ECOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Pneumococcal carriage studies have suggested that pneumococcal colonization in adults is largely limited to the oral cavity and oropharynx. In this study, we used total abundance-based β-diversity (dissimilarity) and β-diversity components to characterize age-related differences in pneumococcal serotype composition of respiratory samples. quantitative PCR (qPCR) was applied to detect pneumococcal serotypes in nasopharyngeal samples collected from 946 toddlers and 602 adults, saliva samples collected from a subset of 653 toddlers, and saliva and oropharyngeal samples collected from a subset of 318 adults. Bacterial culture rates from nasopharyngeal samples were used to characterize age-related differences in rates of colonizing bacteria. Dissimilarity in pneumococcal serotype composition was low among saliva and nasopharyngeal samples from children. In contrast, respiratory samples from adults exhibited high serotype dissimilarity, which predominantly consisted of abundance gradients and was associated with reduced nasopharyngeal colonization. Age-related serotype dissimilarity was high among nasopharyngeal samples and relatively low for saliva samples. Reduced nasopharyngeal colonization by pneumococcal serotypes coincided with significantly reduced Moraxella catarrhalis and Haemophilus influenzae and increased Staphylococcus aureus nasopharyngeal colonization rates among adults. Findings from this study suggest that within-host environmental conditions, utilized in the upper airways by pneumococcus and other bacteria, undergo age-related changes. It may result in a host-driven ecological succession of bacterial species colonizing the nasopharynx and lead to competitive exclusion of pneumococcus from the nasopharynx but not from the oral habitat. This explains the poor performance of nasopharyngeal samples for pneumococcal carriage among adults and indicates that in adults saliva more accurately represents the epidemiology of pneumococcal carriage than nasopharyngeal samples.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
年龄对鼻咽和口腔肺炎球菌定植的影响:生态学视角。
肺炎球菌携带研究表明,肺炎球菌在成人中的定植主要局限于口腔和口咽部。在这项研究中,我们使用基于总丰度的 β 多样性(异质性)和 β 多样性成分来描述呼吸道样本中肺炎球菌血清型组成与年龄有关的差异。我们采用定量 PCR(qPCR)技术检测了从 946 名幼儿和 602 名成人中采集的鼻咽样本、从 653 名幼儿中采集的唾液样本以及从 318 名成人中采集的唾液和口咽样本中的肺炎球菌血清型。鼻咽样本的细菌培养率被用来描述与年龄有关的定植细菌率差异。儿童唾液和鼻咽样本中肺炎球菌血清型组成的差异较小。相比之下,成人呼吸道样本的血清型相似性较高,主要由丰度梯度组成,与鼻咽部定植率降低有关。鼻咽样本中与年龄相关的血清型相似度较高,而唾液样本的血清型相似度相对较低。肺炎球菌血清型鼻咽定植率降低的同时,白喉摩拉菌和流感嗜血杆菌的鼻咽定植率也显著降低,而金黄色葡萄球菌的鼻咽定植率则有所上升。这项研究的结果表明,肺炎球菌和其他细菌在上呼吸道利用的宿主内环境条件会发生与年龄相关的变化。这可能导致在鼻咽部定植的细菌种类在宿主驱动下发生生态演替,并导致肺炎球菌在鼻咽部而不是在口腔栖息地受到竞争性排斥。这解释了鼻咽样本在成人肺炎球菌携带方面表现不佳的原因,并表明在成人中,唾液比鼻咽样本更能准确地反映肺炎球菌携带的流行病学。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
自引率
0.00%
发文量
0
期刊最新文献
Recurrent association between Trichodesmium colonies and calcifying amoebae. Taxon-specific contributions of microeukaryotes to biological carbon pump in the Oyashio region. Significant role of symbiotic bacteria in the blood digestion and reproduction of Dermanyssus gallinae mites. Cover crop monocultures and mixtures enhance bacterial abundance and functionality in the maize root zone. Genomic dissection of Escherichia marmotae provides insights into diversity and pathogenic potential.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1