{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T11:53:43Z","timestamp":1792756423463,"version":"4.5.0"},"reference-count":62,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,12,12]],"date-time":"2022-12-12T00:00:00Z","timestamp":1670803200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003562","name":"Ministry of Environment","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100003562","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002701","name":"Ministry of Education","doi-asserted-by":"publisher","award":["(2021R1A6C101A416"],"award-info":[{"award-number":["(2021R1A6C101A416"]}],"id":[{"id":"10.13039\/501100002701","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>Androgenetic alopecia (AGA) is a non-scarring and progressive form of hair loss occurring in both men and women. Although genetic predisposition and sex steroid hormones are the main causes, many factors remain unknown, and various extrinsic factors can negatively affect the lifespan of hair. We investigated skin\u2013gut axis microorganisms as potential exogenous factors causing AGA, through comparative analyses of the scalp and gut microbiome in individuals with and without AGA in a Korean cohort. Using 16S rRNA gene sequencing, we characterized the scalp and gut microbiomes of 141 individuals divided into groups by sex and presence of AGA. Alpha diversity indices in the scalp microbiome were generally higher in individuals with AGA than in healthy controls. These indices showed a strong negative correlation with scalp-inhabitant bacteria (<jats:italic>Cutibacterium<\/jats:italic> and <jats:italic>Staphylococcus<\/jats:italic>), indicating that the appearance of non-inhabitant bacteria increases as hair loss progresses. No significant differences in diversity were observed between the gut microbiomes. However, bacterial functional differences, such as bile acid synthesis and bacterial invasion of epithelial cells, which are related to intestinal homeostasis, were observed. The networks of the scalp and gut microbiome were more complex and denser with higher values of the network topology statistic coefficient values (i.e., transitivity, density, and degree centrality) and more unique associations in individuals with AGA than in healthy controls. Our findings reveal a link between skin\u2013gut microorganisms and AGA, indicating the former\u2019s potential involvement in the latter\u2019s development. Additionally, these results provide evidence for the development of cosmetics and therapeutics using microorganisms and metabolites involved in AGA.<\/jats:p>","DOI":"10.3389\/fmicb.2022.1076242","type":"journal-article","created":{"date-parts":[[2022,12,12]],"date-time":"2022-12-12T05:37:46Z","timestamp":1670823466000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":28,"title":["Comparative analysis of scalp and gut microbiome in androgenetic alopecia: A Korean cross-sectional study"],"prefix":"10.3389","volume":"13","author":[{"given":"Da-Ryung","family":"Jung","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hye-Young","family":"Yoo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Min-Ji","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vineet","family":"Singh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sung-Ha","family":"Park","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Minsoo","family":"Jeong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Byoung-Jun","family":"Park","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jae-Ho","family":"Shin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,12,12]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1007\/s13555-018-0278-6","article-title":"The role of vitamins and minerals in hair loss: a review","volume":"9","author":"Almohanna","year":"2019","journal-title":"Dermatol. 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Gastroenterol."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"1017","DOI":"10.1517\/14656560902876368","article-title":"Treatment strategies for alopecia","volume":"10","author":"Tosti","year":"2009","journal-title":"Expert. Opin. Pharmacother."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"981","DOI":"10.1016\/S0531-5565(02)00093-1","article-title":"Molecular mechanisms of androgenetic alopecia","volume":"37","author":"Tr\u00fceb","year":"2002","journal-title":"Exp. Gerontol."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"1195","DOI":"10.1016\/j.mcna.2015.07.003","article-title":"Selected disorders of skin appendages\u2014acne, alopecia, hyperhidrosis","volume":"99","author":"Vary","year":"2015","journal-title":"Med. 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