Age-Related Changes in the Nasopharyngeal Microbiome Are Associated With Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Infection and Symptoms Among Children, Adolescents, and Young Adults
Abstract Background Children are less susceptible to SARS-CoV-2 infection and typically have milder illness courses than adults, but the factors underlying these age-associated differences are not well understood. The upper respiratory microbiome undergoes substantial shifts during childhood and is...
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| Veröffentlicht in: | Clinical infectious diseases 2022-08, Vol.75 (1), p.e928-e937 |
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| creator | Hurst, Jillian H McCumber, Alexander W Aquino, Jhoanna N Rodriguez, Javier Heston, Sarah M Lugo, Debra J Rotta, Alexandre T Turner, Nicholas A Pfeiffer, Trevor S Gurley, Thaddeus C Moody, M Anthony Denny, Thomas N Rawls, John F Clark, James S Woods, Christopher W Kelly, Matthew S |
| description | Abstract
Background
Children are less susceptible to SARS-CoV-2 infection and typically have milder illness courses than adults, but the factors underlying these age-associated differences are not well understood. The upper respiratory microbiome undergoes substantial shifts during childhood and is increasingly recognized to influence host defense against respiratory pathogens. Thus, we sought to identify upper respiratory microbiome features associated with SARS-CoV-2 infection susceptibility and illness severity.
Methods
We collected clinical data and nasopharyngeal swabs from 285 children, adolescents, and young adults ( |
| doi_str_mv | 10.1093/cid/ciac184 |
| format | Article |
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Background
Children are less susceptible to SARS-CoV-2 infection and typically have milder illness courses than adults, but the factors underlying these age-associated differences are not well understood. The upper respiratory microbiome undergoes substantial shifts during childhood and is increasingly recognized to influence host defense against respiratory pathogens. Thus, we sought to identify upper respiratory microbiome features associated with SARS-CoV-2 infection susceptibility and illness severity.
Methods
We collected clinical data and nasopharyngeal swabs from 285 children, adolescents, and young adults (<21 years) with documented SARS-CoV-2 exposure. We used 16S ribosomal RNA gene sequencing to characterize the nasopharyngeal microbiome and evaluated for age-adjusted associations between microbiome characteristics and SARS-CoV-2 infection status and respiratory symptoms.
Results
Nasopharyngeal microbiome composition varied with age (PERMANOVA, P < .001; R2 = 0.06) and between SARS-CoV-2–infected individuals with and without respiratory symptoms (PERMANOVA, P = .002; R2 = 0.009). SARS-CoV-2–infected participants with Corynebacterium/Dolosigranulum-dominant microbiome profiles were less likely to have respiratory symptoms than infected participants with other nasopharyngeal microbiome profiles (OR: .38; 95% CI: .18–.81). Using generalized joint attributed modeling, we identified 9 bacterial taxa associated with SARS-CoV-2 infection and 6 taxa differentially abundant among SARS-CoV-2–infected participants with respiratory symptoms; the magnitude of these associations was strongly influenced by age.
Conclusions
We identified interactive relationships between age and specific nasopharyngeal microbiome features that are associated with SARS-CoV-2 infection susceptibility and symptoms in children, adolescents, and young adults. Our data suggest that the upper respiratory microbiome may be a mechanism by which age influences SARS-CoV-2 susceptibility and illness severity.
We demonstrate that the nasopharyngeal microbiome undergoes marked shifts in composition with age during childhood and adolescence, and age-associated changes in nasopharyngeal microbiome composition are associated with SARS-CoV-2 infection and SARS-CoV-2–associated respiratory symptoms among children, adolescents, and young adults.</description><identifier>ISSN: 1058-4838</identifier><identifier>EISSN: 1537-6591</identifier><identifier>DOI: 10.1093/cid/ciac184</identifier><identifier>PMID: 35247047</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Adolescent ; Bacteria - genetics ; Child ; COVID-19 ; Humans ; Major ; Microbiota - genetics ; Nasopharynx - microbiology ; SARS-CoV-2 ; Young Adult</subject><ispartof>Clinical infectious diseases, 2022-08, Vol.75 (1), p.e928-e937</ispartof><rights>The Author(s) 2022. Published by Oxford University Press for the Infectious Diseases Society of America. 2022</rights><rights>The Author(s) 2022. Published by Oxford University Press for the Infectious Diseases Society of America.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-f4449058942ecf258e67e1acfa6dca4945f74d8d99a9c882dfdcb53b459c34113</citedby><cites>FETCH-LOGICAL-c412t-f4449058942ecf258e67e1acfa6dca4945f74d8d99a9c882dfdcb53b459c34113</cites><orcidid>0000-0001-5079-9920</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,1578,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35247047$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hurst, Jillian H</creatorcontrib><creatorcontrib>McCumber, Alexander W</creatorcontrib><creatorcontrib>Aquino, Jhoanna N</creatorcontrib><creatorcontrib>Rodriguez, Javier</creatorcontrib><creatorcontrib>Heston, Sarah M</creatorcontrib><creatorcontrib>Lugo, Debra J</creatorcontrib><creatorcontrib>Rotta, Alexandre T</creatorcontrib><creatorcontrib>Turner, Nicholas A</creatorcontrib><creatorcontrib>Pfeiffer, Trevor S</creatorcontrib><creatorcontrib>Gurley, Thaddeus C</creatorcontrib><creatorcontrib>Moody, M Anthony</creatorcontrib><creatorcontrib>Denny, Thomas N</creatorcontrib><creatorcontrib>Rawls, John F</creatorcontrib><creatorcontrib>Clark, James S</creatorcontrib><creatorcontrib>Woods, Christopher W</creatorcontrib><creatorcontrib>Kelly, Matthew S</creatorcontrib><title>Age-Related Changes in the Nasopharyngeal Microbiome Are Associated With Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Infection and Symptoms Among Children, Adolescents, and Young Adults</title><title>Clinical infectious diseases</title><addtitle>Clin Infect Dis</addtitle><description>Abstract
Background
Children are less susceptible to SARS-CoV-2 infection and typically have milder illness courses than adults, but the factors underlying these age-associated differences are not well understood. The upper respiratory microbiome undergoes substantial shifts during childhood and is increasingly recognized to influence host defense against respiratory pathogens. Thus, we sought to identify upper respiratory microbiome features associated with SARS-CoV-2 infection susceptibility and illness severity.
Methods
We collected clinical data and nasopharyngeal swabs from 285 children, adolescents, and young adults (<21 years) with documented SARS-CoV-2 exposure. We used 16S ribosomal RNA gene sequencing to characterize the nasopharyngeal microbiome and evaluated for age-adjusted associations between microbiome characteristics and SARS-CoV-2 infection status and respiratory symptoms.
Results
Nasopharyngeal microbiome composition varied with age (PERMANOVA, P < .001; R2 = 0.06) and between SARS-CoV-2–infected individuals with and without respiratory symptoms (PERMANOVA, P = .002; R2 = 0.009). SARS-CoV-2–infected participants with Corynebacterium/Dolosigranulum-dominant microbiome profiles were less likely to have respiratory symptoms than infected participants with other nasopharyngeal microbiome profiles (OR: .38; 95% CI: .18–.81). Using generalized joint attributed modeling, we identified 9 bacterial taxa associated with SARS-CoV-2 infection and 6 taxa differentially abundant among SARS-CoV-2–infected participants with respiratory symptoms; the magnitude of these associations was strongly influenced by age.
Conclusions
We identified interactive relationships between age and specific nasopharyngeal microbiome features that are associated with SARS-CoV-2 infection susceptibility and symptoms in children, adolescents, and young adults. Our data suggest that the upper respiratory microbiome may be a mechanism by which age influences SARS-CoV-2 susceptibility and illness severity.
We demonstrate that the nasopharyngeal microbiome undergoes marked shifts in composition with age during childhood and adolescence, and age-associated changes in nasopharyngeal microbiome composition are associated with SARS-CoV-2 infection and SARS-CoV-2–associated respiratory symptoms among children, adolescents, and young adults.</description><subject>Adolescent</subject><subject>Bacteria - genetics</subject><subject>Child</subject><subject>COVID-19</subject><subject>Humans</subject><subject>Major</subject><subject>Microbiota - genetics</subject><subject>Nasopharynx - microbiology</subject><subject>SARS-CoV-2</subject><subject>Young Adult</subject><issn>1058-4838</issn><issn>1537-6591</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp9kU2P0zAQhiMEYpeFE3fkE1rEBuLYSe0LUhTxsdICUsuHOFmuPWmMEjvYTqX-RX4VDi0ruHAY2Ro_88543ix7jIsXuODkpTI6hVSY0TvZOa7IKq8rju-me1GxnDLCzrIHIXwvCoxZUd3PzkhV0lVBV-fZz2YH-RoGGUGjtpd2BwEZi2IP6IMMbuqlP6SkHNB7o7zbGjcCanyKEFxqu9R9NbFHG9jDklZzBLSGMBkvo_MHtDlY7Zeq1nln5d74OaASXW6a9SZv3Ze8fIaubQcqGmeRtDpVjFN0Y0DN6OwujWUG7cFeoUa7AYICG8PVb_KbmxPQ6HmI4WF2r5NDgEen8yL7_Ob1p_ZdfvPx7XXb3OSK4jLmHaWUp8VwWoLqyopBvQIsVSdrrSTltOpWVDPNueSKsVJ3Wm0rsqUVV4RiTC6yV0fdad6OoJdpvBzE5M2YdiWcNOLfF2t6sXN7wXhBaE2SwOVJwLsfM4QoRpM-NQzSgpuDKGtS44ryskzo8yOaVh-Ch-62DS7E4r5I7ouT-4l-8vdkt-wfuxPw9Ai4efqv0i8Zobzm</recordid><startdate>20220824</startdate><enddate>20220824</enddate><creator>Hurst, Jillian H</creator><creator>McCumber, Alexander W</creator><creator>Aquino, Jhoanna N</creator><creator>Rodriguez, Javier</creator><creator>Heston, Sarah M</creator><creator>Lugo, Debra J</creator><creator>Rotta, Alexandre T</creator><creator>Turner, Nicholas A</creator><creator>Pfeiffer, Trevor S</creator><creator>Gurley, Thaddeus C</creator><creator>Moody, M Anthony</creator><creator>Denny, Thomas N</creator><creator>Rawls, John F</creator><creator>Clark, James S</creator><creator>Woods, Christopher W</creator><creator>Kelly, Matthew S</creator><general>Oxford University Press</general><scope>TOX</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5079-9920</orcidid></search><sort><creationdate>20220824</creationdate><title>Age-Related Changes in the Nasopharyngeal Microbiome Are Associated With Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Infection and Symptoms Among Children, Adolescents, and Young Adults</title><author>Hurst, Jillian H ; McCumber, Alexander W ; Aquino, Jhoanna N ; Rodriguez, Javier ; Heston, Sarah M ; Lugo, Debra J ; Rotta, Alexandre T ; Turner, Nicholas A ; Pfeiffer, Trevor S ; Gurley, Thaddeus C ; Moody, M Anthony ; Denny, Thomas N ; Rawls, John F ; Clark, James S ; Woods, Christopher W ; Kelly, Matthew S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-f4449058942ecf258e67e1acfa6dca4945f74d8d99a9c882dfdcb53b459c34113</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Adolescent</topic><topic>Bacteria - genetics</topic><topic>Child</topic><topic>COVID-19</topic><topic>Humans</topic><topic>Major</topic><topic>Microbiota - genetics</topic><topic>Nasopharynx - microbiology</topic><topic>SARS-CoV-2</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hurst, Jillian H</creatorcontrib><creatorcontrib>McCumber, Alexander W</creatorcontrib><creatorcontrib>Aquino, Jhoanna N</creatorcontrib><creatorcontrib>Rodriguez, Javier</creatorcontrib><creatorcontrib>Heston, Sarah M</creatorcontrib><creatorcontrib>Lugo, Debra J</creatorcontrib><creatorcontrib>Rotta, Alexandre T</creatorcontrib><creatorcontrib>Turner, Nicholas A</creatorcontrib><creatorcontrib>Pfeiffer, Trevor S</creatorcontrib><creatorcontrib>Gurley, Thaddeus C</creatorcontrib><creatorcontrib>Moody, M Anthony</creatorcontrib><creatorcontrib>Denny, Thomas N</creatorcontrib><creatorcontrib>Rawls, John F</creatorcontrib><creatorcontrib>Clark, James S</creatorcontrib><creatorcontrib>Woods, Christopher W</creatorcontrib><creatorcontrib>Kelly, Matthew S</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Clinical infectious diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hurst, Jillian H</au><au>McCumber, Alexander W</au><au>Aquino, Jhoanna N</au><au>Rodriguez, Javier</au><au>Heston, Sarah M</au><au>Lugo, Debra J</au><au>Rotta, Alexandre T</au><au>Turner, Nicholas A</au><au>Pfeiffer, Trevor S</au><au>Gurley, Thaddeus C</au><au>Moody, M Anthony</au><au>Denny, Thomas N</au><au>Rawls, John F</au><au>Clark, James S</au><au>Woods, Christopher W</au><au>Kelly, Matthew S</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Age-Related Changes in the Nasopharyngeal Microbiome Are Associated With Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Infection and Symptoms Among Children, Adolescents, and Young Adults</atitle><jtitle>Clinical infectious diseases</jtitle><addtitle>Clin Infect Dis</addtitle><date>2022-08-24</date><risdate>2022</risdate><volume>75</volume><issue>1</issue><spage>e928</spage><epage>e937</epage><pages>e928-e937</pages><issn>1058-4838</issn><eissn>1537-6591</eissn><abstract>Abstract
Background
Children are less susceptible to SARS-CoV-2 infection and typically have milder illness courses than adults, but the factors underlying these age-associated differences are not well understood. The upper respiratory microbiome undergoes substantial shifts during childhood and is increasingly recognized to influence host defense against respiratory pathogens. Thus, we sought to identify upper respiratory microbiome features associated with SARS-CoV-2 infection susceptibility and illness severity.
Methods
We collected clinical data and nasopharyngeal swabs from 285 children, adolescents, and young adults (<21 years) with documented SARS-CoV-2 exposure. We used 16S ribosomal RNA gene sequencing to characterize the nasopharyngeal microbiome and evaluated for age-adjusted associations between microbiome characteristics and SARS-CoV-2 infection status and respiratory symptoms.
Results
Nasopharyngeal microbiome composition varied with age (PERMANOVA, P < .001; R2 = 0.06) and between SARS-CoV-2–infected individuals with and without respiratory symptoms (PERMANOVA, P = .002; R2 = 0.009). SARS-CoV-2–infected participants with Corynebacterium/Dolosigranulum-dominant microbiome profiles were less likely to have respiratory symptoms than infected participants with other nasopharyngeal microbiome profiles (OR: .38; 95% CI: .18–.81). Using generalized joint attributed modeling, we identified 9 bacterial taxa associated with SARS-CoV-2 infection and 6 taxa differentially abundant among SARS-CoV-2–infected participants with respiratory symptoms; the magnitude of these associations was strongly influenced by age.
Conclusions
We identified interactive relationships between age and specific nasopharyngeal microbiome features that are associated with SARS-CoV-2 infection susceptibility and symptoms in children, adolescents, and young adults. Our data suggest that the upper respiratory microbiome may be a mechanism by which age influences SARS-CoV-2 susceptibility and illness severity.
We demonstrate that the nasopharyngeal microbiome undergoes marked shifts in composition with age during childhood and adolescence, and age-associated changes in nasopharyngeal microbiome composition are associated with SARS-CoV-2 infection and SARS-CoV-2–associated respiratory symptoms among children, adolescents, and young adults.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>35247047</pmid><doi>10.1093/cid/ciac184</doi><orcidid>https://orcid.org/0000-0001-5079-9920</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Clinical infectious diseases, 2022-08, Vol.75 (1), p.e928-e937 |
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| source | Oxford University Press Journals All Titles (1996-Current); MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection |
| subjects | Adolescent Bacteria - genetics Child COVID-19 Humans Major Microbiota - genetics Nasopharynx - microbiology SARS-CoV-2 Young Adult |
| title | Age-Related Changes in the Nasopharyngeal Microbiome Are Associated With Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Infection and Symptoms Among Children, Adolescents, and Young Adults |
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