Streptococcus pyogenes carriage and infection within households in The Gambia: a longitudinal cohort study

IF 20.9 1区 生物学 Q1 INFECTIOUS DISEASES
Edwin P Armitage BMBS , Gabrielle de Crombrugghe MD , Alexander J Keeley BMBS , Elina Senghore BSc , Fatoumata E Camara MSc , Musukoi Jammeh , Amat Bittaye ADN , Haddy Ceesay CHN , Isatou Ceesay RN , Bunja Samateh BSN , Muhammed Manneh TNA , Prof Beate Kampmann , Claire E Turner PhD , Prof Adam Kucharski , Anne Botteaux PhD , Prof Pierre R Smeesters , Prof Thushan I de Silva , Prof Michael Marks
{"title":"Streptococcus pyogenes carriage and infection within households in The Gambia: a longitudinal cohort study","authors":"Edwin P Armitage BMBS ,&nbsp;Gabrielle de Crombrugghe MD ,&nbsp;Alexander J Keeley BMBS ,&nbsp;Elina Senghore BSc ,&nbsp;Fatoumata E Camara MSc ,&nbsp;Musukoi Jammeh ,&nbsp;Amat Bittaye ADN ,&nbsp;Haddy Ceesay CHN ,&nbsp;Isatou Ceesay RN ,&nbsp;Bunja Samateh BSN ,&nbsp;Muhammed Manneh TNA ,&nbsp;Prof Beate Kampmann ,&nbsp;Claire E Turner PhD ,&nbsp;Prof Adam Kucharski ,&nbsp;Anne Botteaux PhD ,&nbsp;Prof Pierre R Smeesters ,&nbsp;Prof Thushan I de Silva ,&nbsp;Prof Michael Marks","doi":"10.1016/S2666-5247(24)00046-6","DOIUrl":null,"url":null,"abstract":"<div><h3>Background</h3><p><em>Streptococcus pyogenes</em> causes more than 500 000 deaths per year globally, which occur disproportionately in low-income and middle-income countries. The roles of <em>S pyogenes</em> skin and pharyngeal carriage in transmission are unclear. We aimed to investigate the clinical epidemiology and household transmission dynamics of both <em>S pyogenes</em> asymptomatic carriage and infection in a high-burden setting.</p></div><div><h3>Methods</h3><p>We did a 1-year prospective, longitudinal, household cohort study, recruiting healthy participants from households in Sukuta, The Gambia. Households were eligible if they comprised at least three members, including one child younger than 18 years, and were excluded if more than half of household members declined to participate. Households were identified by random GPS coordinates derived from census data. At monthly visits, pharyngeal and normal skin swabs were collected for <em>S pyogenes</em> culture, and sociodemographic data were recorded by interview. Incident pharyngitis and pyoderma infections were captured. Cultured isolates underwent <em>emm</em> genotyping. The primary outcome measures were incidence of <em>S pyogenes</em> carriage and disease. Additional outcomes were prevalence of <em>S pyogenes</em> skin and pharyngeal carriage, <em>S pyogenes</em> skin and pharyngeal clearance time, <em>S pyogenes emm</em> type, risk factors for carriage and disease events, household secondary attack rate, and <em>emm</em>-linked household transmission events. The study is registered on ClinicalTrials.gov, <span>NCT05117528</span><svg><path></path></svg>.</p></div><div><h3>Findings</h3><p>Between July 27, 2021, and Sept 28, 2022, 442 participants were enrolled from 44 households. The median age was 15 years (IQR 6–28) and 233 (53%) were female. We identified 17 pharyngitis and 99 pyoderma events and 49 pharyngeal and 39 skin <em>S pyogenes</em> carriage acquisition events. Mean monthly prevalence was 1·4% (95% CI 1·1–1·9) for <em>S pyogenes</em> pharyngeal carriage and 1·2% (0·9–1·6) for <em>S pyogenes</em> skin carriage. Incidence was 120 per 1000 person-years (95% CI 87–166) for <em>S pyogenes</em> pharyngeal carriage, 124 per 1000 person-years (90–170) for <em>S pyogenes</em> skin carriage, 51 per 1000 person-years (31–84) for <em>S pyogenes</em> pharyngitis, and 263 per 1000 person-years (212–327) for <em>S pyogenes</em> pyoderma. Pharyngeal carriage risk was higher during the rainy season (HR 5·67, 95% CI 2·19–14·69) and in larger households (per additional person: 1·03, 1·00–1·05), as was pharyngitis risk (rainy season: 3·00, 1·10–8·22; household size: 1·04, 1·02–1·07). Skin carriage risk was not affected by season or household size, but was lower in female than in male participants (0·45, 0·22–0·92) and highest in children younger than 5 years compared with adults (22·69, 3·08–167·21), with similar findings for pyoderma (female sex: 0·34, 0·19–0·61; age &lt;5 years: 7·00, 2·78–17·64). Median clearance time after carriage acquisition was 4·0 days for both skin (IQR 3·5–7·0) and pharynx (3·5–7·3). The mean household secondary attack rate was 4·9 (95% CI 3·5–6·3) for epidemiologically linked <em>S pyogenes</em> events and 0·74 (0·3–1·2) for <em>emm</em>-linked <em>S pyogenes</em> events. Of the 204 carriage and disease events, <em>emm</em> types were available for 179 (88%). Only 18 <em>emm</em>-linked between-visit household transmission events were identified. Pyoderma was the most common source of <em>S pyogenes</em> household transmissions in 11 (61%) of 18 <em>emm</em>-linked transmissions. Both pharynx to skin and skin to pharynx transmission events were observed.</p></div><div><h3>Interpretation</h3><p><em>S pyogenes</em> carriage and infection are common in The Gambia, particularly in children. Most events are non-household acquisitions, but skin carriage and pyoderma have an important role in <em>S pyogenes</em> household transmission and bidirectional transmission between skin and pharynx occurs.</p></div><div><h3>Funding</h3><p>Wellcome Trust, Chadwick Trust, Fonds National de la Recherche Scientifique (Belgium), European Society for Paediatric Infectious Diseases, and Medical Research Council (UK).</p></div>","PeriodicalId":46633,"journal":{"name":"Lancet Microbe","volume":null,"pages":null},"PeriodicalIF":20.9000,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S2666524724000466/pdfft?md5=bc8389712029b740af2e4fb87875e5e4&pid=1-s2.0-S2666524724000466-main.pdf","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Lancet Microbe","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S2666524724000466","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"INFECTIOUS DISEASES","Score":null,"Total":0}
引用次数: 0

Abstract

Background

Streptococcus pyogenes causes more than 500 000 deaths per year globally, which occur disproportionately in low-income and middle-income countries. The roles of S pyogenes skin and pharyngeal carriage in transmission are unclear. We aimed to investigate the clinical epidemiology and household transmission dynamics of both S pyogenes asymptomatic carriage and infection in a high-burden setting.

Methods

We did a 1-year prospective, longitudinal, household cohort study, recruiting healthy participants from households in Sukuta, The Gambia. Households were eligible if they comprised at least three members, including one child younger than 18 years, and were excluded if more than half of household members declined to participate. Households were identified by random GPS coordinates derived from census data. At monthly visits, pharyngeal and normal skin swabs were collected for S pyogenes culture, and sociodemographic data were recorded by interview. Incident pharyngitis and pyoderma infections were captured. Cultured isolates underwent emm genotyping. The primary outcome measures were incidence of S pyogenes carriage and disease. Additional outcomes were prevalence of S pyogenes skin and pharyngeal carriage, S pyogenes skin and pharyngeal clearance time, S pyogenes emm type, risk factors for carriage and disease events, household secondary attack rate, and emm-linked household transmission events. The study is registered on ClinicalTrials.gov, NCT05117528.

Findings

Between July 27, 2021, and Sept 28, 2022, 442 participants were enrolled from 44 households. The median age was 15 years (IQR 6–28) and 233 (53%) were female. We identified 17 pharyngitis and 99 pyoderma events and 49 pharyngeal and 39 skin S pyogenes carriage acquisition events. Mean monthly prevalence was 1·4% (95% CI 1·1–1·9) for S pyogenes pharyngeal carriage and 1·2% (0·9–1·6) for S pyogenes skin carriage. Incidence was 120 per 1000 person-years (95% CI 87–166) for S pyogenes pharyngeal carriage, 124 per 1000 person-years (90–170) for S pyogenes skin carriage, 51 per 1000 person-years (31–84) for S pyogenes pharyngitis, and 263 per 1000 person-years (212–327) for S pyogenes pyoderma. Pharyngeal carriage risk was higher during the rainy season (HR 5·67, 95% CI 2·19–14·69) and in larger households (per additional person: 1·03, 1·00–1·05), as was pharyngitis risk (rainy season: 3·00, 1·10–8·22; household size: 1·04, 1·02–1·07). Skin carriage risk was not affected by season or household size, but was lower in female than in male participants (0·45, 0·22–0·92) and highest in children younger than 5 years compared with adults (22·69, 3·08–167·21), with similar findings for pyoderma (female sex: 0·34, 0·19–0·61; age <5 years: 7·00, 2·78–17·64). Median clearance time after carriage acquisition was 4·0 days for both skin (IQR 3·5–7·0) and pharynx (3·5–7·3). The mean household secondary attack rate was 4·9 (95% CI 3·5–6·3) for epidemiologically linked S pyogenes events and 0·74 (0·3–1·2) for emm-linked S pyogenes events. Of the 204 carriage and disease events, emm types were available for 179 (88%). Only 18 emm-linked between-visit household transmission events were identified. Pyoderma was the most common source of S pyogenes household transmissions in 11 (61%) of 18 emm-linked transmissions. Both pharynx to skin and skin to pharynx transmission events were observed.

Interpretation

S pyogenes carriage and infection are common in The Gambia, particularly in children. Most events are non-household acquisitions, but skin carriage and pyoderma have an important role in S pyogenes household transmission and bidirectional transmission between skin and pharynx occurs.

Funding

Wellcome Trust, Chadwick Trust, Fonds National de la Recherche Scientifique (Belgium), European Society for Paediatric Infectious Diseases, and Medical Research Council (UK).

冈比亚家庭内化脓性链球菌携带和感染情况:纵向队列研究。
背景:化脓性链球菌每年在全球造成 50 多万人死亡,其中大部分发生在低收入和中等收入国家。化脓性链球菌皮肤和咽部携带在传播中的作用尚不清楚。我们的目的是调查化脓性链球菌无症状携带和感染在高负担环境中的临床流行病学和家庭传播动态:我们进行了一项为期 1 年的前瞻性纵向家庭队列研究,从冈比亚苏库塔的家庭中招募健康参与者。如果家庭中至少有三名成员,其中包括一名18岁以下的儿童,则该家庭符合条件;如果有一半以上的家庭成员拒绝参与,则该家庭不符合条件。根据人口普查数据得出的随机 GPS 坐标确定住户。每月访问一次,采集咽部和正常皮肤拭子进行化脓性链球菌培养,并通过访谈记录社会人口学数据。咽炎和脓疱疮感染病例也被记录在案。对培养分离物进行emm基因分型。主要结果指标是化脓性链球菌携带率和发病率。其他结果包括化脓性链球菌皮肤和咽部携带率、化脓性链球菌皮肤和咽部清除时间、化脓性链球菌emm类型、携带和疾病事件的风险因素、家庭二次发病率以及与emm相关的家庭传播事件。该研究已在 ClinicalTrials.gov 上注册,编号为 NCT05117528:2021 年 7 月 27 日至 2022 年 9 月 28 日期间,44 个家庭的 442 名参与者参加了研究。中位年龄为 15 岁(IQR 6-28),233 人(53%)为女性。我们发现了 17 起咽炎和 99 起脓疱疮事件,以及 49 起咽部和 39 起皮肤化脓性链球菌携带感染事件。化脓性链球菌咽部携带的月平均流行率为 1-4%(95% CI 1-1-1-9),化脓性链球菌皮肤携带的月平均流行率为 1-2%(0-9-1-6)。化脓性链球菌咽部携带的发病率为每千人年 120 例(95% CI 87-166),化脓性链球菌皮肤携带的发病率为每千人年 124 例(90-170),化脓性链球菌咽炎的发病率为每千人年 51 例(31-84),化脓性链球菌脓皮病的发病率为每千人年 263 例(212-327)。咽部带菌风险在雨季更高(HR 5-67,95% CI 2-19-14-69),在人口较多的家庭更高(每增加一人:1-03,1-00-1-05),咽炎风险也更高(雨季:3-00,1-10-8-22;家庭人口:1-04,1-02-1-07)。皮肤携带风险不受季节或家庭规模的影响,但女性参与者的皮肤携带风险低于男性(0-45,0-22-0-92),5 岁以下儿童的皮肤携带风险高于成人(22-69,3-08-167-21):化脓性链球菌携带和感染在冈比亚很常见,尤其是在儿童中。大多数情况是非家庭感染,但皮肤带菌和脓皮病在化脓性链球菌家庭传播中起着重要作用,皮肤和咽部之间的双向传播也时有发生:资金来源:惠康基金会、查德威克基金会、比利时国家科学研究基金会、欧洲儿科传染病学会和英国医学研究理事会。
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 求助全文
来源期刊
Lancet Microbe
Lancet Microbe Multiple-
CiteScore
27.20
自引率
0.80%
发文量
278
审稿时长
6 weeks
期刊介绍: The Lancet Microbe is a gold open access journal committed to publishing content relevant to clinical microbiologists worldwide, with a focus on studies that advance clinical understanding, challenge the status quo, and advocate change in health policy.
×
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
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
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 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信