Evolution of the facial skin microbiome during puberty in normal and acne skin
Background The composition of the skin microbiome varies from infancy to adulthood and becomes most stable in adulthood. Adult acne patients harbour an ‘acne microbiome’ dominated by specific strains of Cutibacterium acnes. However, the precise timing of skin microbiome evolution, the development of...
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| Veröffentlicht in: | Journal of the European Academy of Dermatology and Venereology 2023-01, Vol.37 (1), p.166-175 |
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| container_title | Journal of the European Academy of Dermatology and Venereology |
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| creator | Schneider, Andrea M. Nolan, Zachary T. Banerjee, Kalins Paine, Allison R. Cong, Zhaoyuan Gettle, Samantha L. Longenecker, Amy L. Zhan, Xiang Agak, George W. Nelson, Amanda M. |
| description | Background
The composition of the skin microbiome varies from infancy to adulthood and becomes most stable in adulthood. Adult acne patients harbour an ‘acne microbiome’ dominated by specific strains of Cutibacterium acnes. However, the precise timing of skin microbiome evolution, the development of the acne microbiome, and the shift to virulent C. acnes strain composition during puberty is unknown.
Objectives
We performed a cross‐sectional pilot study in a paediatric population to understand how and when the skin microbiome composition transitions during puberty and whether a distinct ‘acne microbiome’ emerges in paediatric subjects.
Methods
Forty‐eight volunteers including males and females, ages 7–17 years, with and without acne were enrolled and evaluated for pubertal development using the Tanner staging criteria. Sebum levels were measured, and skin microbiota were collected by sterile swab on the subject's forehead. DNA was sequenced by whole genome shotgun sequencing.
Results
A significant shift in microbial diversity emerged between early (T1‐T2) and late (T3‐T5) stages of puberty, coinciding with increased sebum production on the face. The overall relative abundance of C. acnes in both normal and acne skin increased during puberty and individual C. acnes strains were uniquely affected by pubertal stage and the presence of acne. Further, an acne microbiome signature associated with unique C. acnes strain composition and metabolic activity emerges in late puberty in those with acne. This unique C. acnes strain composition is predicted to have increased porphyrin production, which may contribute to skin inflammation.
Conclusions
Our data suggest that the stage of pubertal development influences skin microbiome composition. As children mature, a distinct acne microbiome composition emerges in those with acne. Understanding how both puberty and acne influence the microbiome may support novel therapeutic strategies to combat acne in the paediatric population. |
| doi_str_mv | 10.1111/jdv.18616 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11134479</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2718643673</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4166-a3dc89713421891b218329e4ec16fb2935c387e7ba116cd0cdb555cd6391f3c63</originalsourceid><addsrcrecordid>eNp1kU1PxCAQhonR6Ppx8A8YjnroypSWlpMx6_qVjV7UK6GUKtrCCu2a_feiq0YPcoDDPDwzeQehfSBjiOf4uV6MoWTA1tAIMlYmlJR0HY0IT1nCec630HYIz4QQgLzcRFs0sjkj2QjdTBeuHXrjLHYN7p80bqQyssXhxVjcGeVdZVyncT14Yx_xfKi075c4Fq3zXQSlrbFUVn_-2EUbjWyD3vt6d9D9-fRucpnMbi-uJqezRGXAWCJprUpeAM1SKDlU8aYp15lWwJoq5TRXtCx0UUkApmqi6irPc1UzyqGhitEddLLyxnk6XSttey9bMfemk34pnDTib8WaJ_HoFiLGRbOs4NFw-GXw7nXQoRedCUq3rbTaDUGkRUw0o6ygET1aoTGMELxufvoA-RCCiAsQnwuI7MHvwX7I78QjcLwC3kyrl_-bxPXZw0r5DjXykDo</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2718643673</pqid></control><display><type>article</type><title>Evolution of the facial skin microbiome during puberty in normal and acne skin</title><source>MEDLINE</source><source>Wiley Online Library Journals Frontfile Complete</source><creator>Schneider, Andrea M. ; Nolan, Zachary T. ; Banerjee, Kalins ; Paine, Allison R. ; Cong, Zhaoyuan ; Gettle, Samantha L. ; Longenecker, Amy L. ; Zhan, Xiang ; Agak, George W. ; Nelson, Amanda M.</creator><creatorcontrib>Schneider, Andrea M. ; Nolan, Zachary T. ; Banerjee, Kalins ; Paine, Allison R. ; Cong, Zhaoyuan ; Gettle, Samantha L. ; Longenecker, Amy L. ; Zhan, Xiang ; Agak, George W. ; Nelson, Amanda M.</creatorcontrib><description>Background
The composition of the skin microbiome varies from infancy to adulthood and becomes most stable in adulthood. Adult acne patients harbour an ‘acne microbiome’ dominated by specific strains of Cutibacterium acnes. However, the precise timing of skin microbiome evolution, the development of the acne microbiome, and the shift to virulent C. acnes strain composition during puberty is unknown.
Objectives
We performed a cross‐sectional pilot study in a paediatric population to understand how and when the skin microbiome composition transitions during puberty and whether a distinct ‘acne microbiome’ emerges in paediatric subjects.
Methods
Forty‐eight volunteers including males and females, ages 7–17 years, with and without acne were enrolled and evaluated for pubertal development using the Tanner staging criteria. Sebum levels were measured, and skin microbiota were collected by sterile swab on the subject's forehead. DNA was sequenced by whole genome shotgun sequencing.
Results
A significant shift in microbial diversity emerged between early (T1‐T2) and late (T3‐T5) stages of puberty, coinciding with increased sebum production on the face. The overall relative abundance of C. acnes in both normal and acne skin increased during puberty and individual C. acnes strains were uniquely affected by pubertal stage and the presence of acne. Further, an acne microbiome signature associated with unique C. acnes strain composition and metabolic activity emerges in late puberty in those with acne. This unique C. acnes strain composition is predicted to have increased porphyrin production, which may contribute to skin inflammation.
Conclusions
Our data suggest that the stage of pubertal development influences skin microbiome composition. As children mature, a distinct acne microbiome composition emerges in those with acne. Understanding how both puberty and acne influence the microbiome may support novel therapeutic strategies to combat acne in the paediatric population.</description><identifier>ISSN: 0926-9959</identifier><identifier>EISSN: 1468-3083</identifier><identifier>DOI: 10.1111/jdv.18616</identifier><identifier>PMID: 36165604</identifier><language>eng</language><publisher>England</publisher><subject>Acne Vulgaris - drug therapy ; Adolescent ; Adult ; Child ; Cross-Sectional Studies ; Female ; Humans ; Male ; Microbiota - genetics ; Pilot Projects ; Propionibacterium acnes - genetics ; Puberty ; Skin - microbiology</subject><ispartof>Journal of the European Academy of Dermatology and Venereology, 2023-01, Vol.37 (1), p.166-175</ispartof><rights>2022 European Academy of Dermatology and Venereology.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4166-a3dc89713421891b218329e4ec16fb2935c387e7ba116cd0cdb555cd6391f3c63</citedby><cites>FETCH-LOGICAL-c4166-a3dc89713421891b218329e4ec16fb2935c387e7ba116cd0cdb555cd6391f3c63</cites><orcidid>0000-0001-9650-143X ; 0000-0002-5471-8670 ; 0000-0002-3804-2789 ; 0000-0002-9725-4634 ; 0000-0003-4314-5114 ; 0000-0001-9881-8203 ; 0000-0003-3064-2058 ; 0000-0001-6375-8706 ; 0000-0001-9895-2912 ; 0000-0002-3356-9864</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fjdv.18616$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fjdv.18616$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36165604$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Schneider, Andrea M.</creatorcontrib><creatorcontrib>Nolan, Zachary T.</creatorcontrib><creatorcontrib>Banerjee, Kalins</creatorcontrib><creatorcontrib>Paine, Allison R.</creatorcontrib><creatorcontrib>Cong, Zhaoyuan</creatorcontrib><creatorcontrib>Gettle, Samantha L.</creatorcontrib><creatorcontrib>Longenecker, Amy L.</creatorcontrib><creatorcontrib>Zhan, Xiang</creatorcontrib><creatorcontrib>Agak, George W.</creatorcontrib><creatorcontrib>Nelson, Amanda M.</creatorcontrib><title>Evolution of the facial skin microbiome during puberty in normal and acne skin</title><title>Journal of the European Academy of Dermatology and Venereology</title><addtitle>J Eur Acad Dermatol Venereol</addtitle><description>Background
The composition of the skin microbiome varies from infancy to adulthood and becomes most stable in adulthood. Adult acne patients harbour an ‘acne microbiome’ dominated by specific strains of Cutibacterium acnes. However, the precise timing of skin microbiome evolution, the development of the acne microbiome, and the shift to virulent C. acnes strain composition during puberty is unknown.
Objectives
We performed a cross‐sectional pilot study in a paediatric population to understand how and when the skin microbiome composition transitions during puberty and whether a distinct ‘acne microbiome’ emerges in paediatric subjects.
Methods
Forty‐eight volunteers including males and females, ages 7–17 years, with and without acne were enrolled and evaluated for pubertal development using the Tanner staging criteria. Sebum levels were measured, and skin microbiota were collected by sterile swab on the subject's forehead. DNA was sequenced by whole genome shotgun sequencing.
Results
A significant shift in microbial diversity emerged between early (T1‐T2) and late (T3‐T5) stages of puberty, coinciding with increased sebum production on the face. The overall relative abundance of C. acnes in both normal and acne skin increased during puberty and individual C. acnes strains were uniquely affected by pubertal stage and the presence of acne. Further, an acne microbiome signature associated with unique C. acnes strain composition and metabolic activity emerges in late puberty in those with acne. This unique C. acnes strain composition is predicted to have increased porphyrin production, which may contribute to skin inflammation.
Conclusions
Our data suggest that the stage of pubertal development influences skin microbiome composition. As children mature, a distinct acne microbiome composition emerges in those with acne. Understanding how both puberty and acne influence the microbiome may support novel therapeutic strategies to combat acne in the paediatric population.</description><subject>Acne Vulgaris - drug therapy</subject><subject>Adolescent</subject><subject>Adult</subject><subject>Child</subject><subject>Cross-Sectional Studies</subject><subject>Female</subject><subject>Humans</subject><subject>Male</subject><subject>Microbiota - genetics</subject><subject>Pilot Projects</subject><subject>Propionibacterium acnes - genetics</subject><subject>Puberty</subject><subject>Skin - microbiology</subject><issn>0926-9959</issn><issn>1468-3083</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kU1PxCAQhonR6Ppx8A8YjnroypSWlpMx6_qVjV7UK6GUKtrCCu2a_feiq0YPcoDDPDwzeQehfSBjiOf4uV6MoWTA1tAIMlYmlJR0HY0IT1nCec630HYIz4QQgLzcRFs0sjkj2QjdTBeuHXrjLHYN7p80bqQyssXhxVjcGeVdZVyncT14Yx_xfKi075c4Fq3zXQSlrbFUVn_-2EUbjWyD3vt6d9D9-fRucpnMbi-uJqezRGXAWCJprUpeAM1SKDlU8aYp15lWwJoq5TRXtCx0UUkApmqi6irPc1UzyqGhitEddLLyxnk6XSttey9bMfemk34pnDTib8WaJ_HoFiLGRbOs4NFw-GXw7nXQoRedCUq3rbTaDUGkRUw0o6ygET1aoTGMELxufvoA-RCCiAsQnwuI7MHvwX7I78QjcLwC3kyrl_-bxPXZw0r5DjXykDo</recordid><startdate>202301</startdate><enddate>202301</enddate><creator>Schneider, Andrea M.</creator><creator>Nolan, Zachary T.</creator><creator>Banerjee, Kalins</creator><creator>Paine, Allison R.</creator><creator>Cong, Zhaoyuan</creator><creator>Gettle, Samantha L.</creator><creator>Longenecker, Amy L.</creator><creator>Zhan, Xiang</creator><creator>Agak, George W.</creator><creator>Nelson, Amanda M.</creator><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/0000-0001-9650-143X</orcidid><orcidid>https://orcid.org/0000-0002-5471-8670</orcidid><orcidid>https://orcid.org/0000-0002-3804-2789</orcidid><orcidid>https://orcid.org/0000-0002-9725-4634</orcidid><orcidid>https://orcid.org/0000-0003-4314-5114</orcidid><orcidid>https://orcid.org/0000-0001-9881-8203</orcidid><orcidid>https://orcid.org/0000-0003-3064-2058</orcidid><orcidid>https://orcid.org/0000-0001-6375-8706</orcidid><orcidid>https://orcid.org/0000-0001-9895-2912</orcidid><orcidid>https://orcid.org/0000-0002-3356-9864</orcidid></search><sort><creationdate>202301</creationdate><title>Evolution of the facial skin microbiome during puberty in normal and acne skin</title><author>Schneider, Andrea M. ; Nolan, Zachary T. ; Banerjee, Kalins ; Paine, Allison R. ; Cong, Zhaoyuan ; Gettle, Samantha L. ; Longenecker, Amy L. ; Zhan, Xiang ; Agak, George W. ; Nelson, Amanda M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4166-a3dc89713421891b218329e4ec16fb2935c387e7ba116cd0cdb555cd6391f3c63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Acne Vulgaris - drug therapy</topic><topic>Adolescent</topic><topic>Adult</topic><topic>Child</topic><topic>Cross-Sectional Studies</topic><topic>Female</topic><topic>Humans</topic><topic>Male</topic><topic>Microbiota - genetics</topic><topic>Pilot Projects</topic><topic>Propionibacterium acnes - genetics</topic><topic>Puberty</topic><topic>Skin - microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Schneider, Andrea M.</creatorcontrib><creatorcontrib>Nolan, Zachary T.</creatorcontrib><creatorcontrib>Banerjee, Kalins</creatorcontrib><creatorcontrib>Paine, Allison R.</creatorcontrib><creatorcontrib>Cong, Zhaoyuan</creatorcontrib><creatorcontrib>Gettle, Samantha L.</creatorcontrib><creatorcontrib>Longenecker, Amy L.</creatorcontrib><creatorcontrib>Zhan, Xiang</creatorcontrib><creatorcontrib>Agak, George W.</creatorcontrib><creatorcontrib>Nelson, Amanda M.</creatorcontrib><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>Journal of the European Academy of Dermatology and Venereology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Schneider, Andrea M.</au><au>Nolan, Zachary T.</au><au>Banerjee, Kalins</au><au>Paine, Allison R.</au><au>Cong, Zhaoyuan</au><au>Gettle, Samantha L.</au><au>Longenecker, Amy L.</au><au>Zhan, Xiang</au><au>Agak, George W.</au><au>Nelson, Amanda M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolution of the facial skin microbiome during puberty in normal and acne skin</atitle><jtitle>Journal of the European Academy of Dermatology and Venereology</jtitle><addtitle>J Eur Acad Dermatol Venereol</addtitle><date>2023-01</date><risdate>2023</risdate><volume>37</volume><issue>1</issue><spage>166</spage><epage>175</epage><pages>166-175</pages><issn>0926-9959</issn><eissn>1468-3083</eissn><abstract>Background
The composition of the skin microbiome varies from infancy to adulthood and becomes most stable in adulthood. Adult acne patients harbour an ‘acne microbiome’ dominated by specific strains of Cutibacterium acnes. However, the precise timing of skin microbiome evolution, the development of the acne microbiome, and the shift to virulent C. acnes strain composition during puberty is unknown.
Objectives
We performed a cross‐sectional pilot study in a paediatric population to understand how and when the skin microbiome composition transitions during puberty and whether a distinct ‘acne microbiome’ emerges in paediatric subjects.
Methods
Forty‐eight volunteers including males and females, ages 7–17 years, with and without acne were enrolled and evaluated for pubertal development using the Tanner staging criteria. Sebum levels were measured, and skin microbiota were collected by sterile swab on the subject's forehead. DNA was sequenced by whole genome shotgun sequencing.
Results
A significant shift in microbial diversity emerged between early (T1‐T2) and late (T3‐T5) stages of puberty, coinciding with increased sebum production on the face. The overall relative abundance of C. acnes in both normal and acne skin increased during puberty and individual C. acnes strains were uniquely affected by pubertal stage and the presence of acne. Further, an acne microbiome signature associated with unique C. acnes strain composition and metabolic activity emerges in late puberty in those with acne. This unique C. acnes strain composition is predicted to have increased porphyrin production, which may contribute to skin inflammation.
Conclusions
Our data suggest that the stage of pubertal development influences skin microbiome composition. As children mature, a distinct acne microbiome composition emerges in those with acne. Understanding how both puberty and acne influence the microbiome may support novel therapeutic strategies to combat acne in the paediatric population.</abstract><cop>England</cop><pmid>36165604</pmid><doi>10.1111/jdv.18616</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-9650-143X</orcidid><orcidid>https://orcid.org/0000-0002-5471-8670</orcidid><orcidid>https://orcid.org/0000-0002-3804-2789</orcidid><orcidid>https://orcid.org/0000-0002-9725-4634</orcidid><orcidid>https://orcid.org/0000-0003-4314-5114</orcidid><orcidid>https://orcid.org/0000-0001-9881-8203</orcidid><orcidid>https://orcid.org/0000-0003-3064-2058</orcidid><orcidid>https://orcid.org/0000-0001-6375-8706</orcidid><orcidid>https://orcid.org/0000-0001-9895-2912</orcidid><orcidid>https://orcid.org/0000-0002-3356-9864</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Journal of the European Academy of Dermatology and Venereology, 2023-01, Vol.37 (1), p.166-175 |
| issn | 0926-9959 1468-3083 |
| language | eng |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete |
| subjects | Acne Vulgaris - drug therapy Adolescent Adult Child Cross-Sectional Studies Female Humans Male Microbiota - genetics Pilot Projects Propionibacterium acnes - genetics Puberty Skin - microbiology |
| title | Evolution of the facial skin microbiome during puberty in normal and acne skin |
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