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Gut microbiota develop towards an adult profile in a sex-specific manner during puberty

Accumulating evidence indicates that gut microbiota may regulate sex-hormone levels in the host, with effects on reproductive health. Very little is known about the development of intestinal microbiota during puberty in humans. To assess the connection between pubertal timing and fecal microbiota, a...

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Autores principales: Korpela, Katri, Kallio, Sampo, Salonen, Anne, Hero, Matti, Kukkonen, Anna Kaarina, Miettinen, Päivi J., Savilahti, Erkki, Kohva, Ella, Kariola, Laura, Suutela, Maria, Tarkkanen, Annika, de Vos, Willem M., Raivio, Taneli, Kuitunen, Mikael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8640005/
https://www.ncbi.nlm.nih.gov/pubmed/34857814
http://dx.doi.org/10.1038/s41598-021-02375-z
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author Korpela, Katri
Kallio, Sampo
Salonen, Anne
Hero, Matti
Kukkonen, Anna Kaarina
Miettinen, Päivi J.
Savilahti, Erkki
Kohva, Ella
Kariola, Laura
Suutela, Maria
Tarkkanen, Annika
de Vos, Willem M.
Raivio, Taneli
Kuitunen, Mikael
author_facet Korpela, Katri
Kallio, Sampo
Salonen, Anne
Hero, Matti
Kukkonen, Anna Kaarina
Miettinen, Päivi J.
Savilahti, Erkki
Kohva, Ella
Kariola, Laura
Suutela, Maria
Tarkkanen, Annika
de Vos, Willem M.
Raivio, Taneli
Kuitunen, Mikael
author_sort Korpela, Katri
collection PubMed
description Accumulating evidence indicates that gut microbiota may regulate sex-hormone levels in the host, with effects on reproductive health. Very little is known about the development of intestinal microbiota during puberty in humans. To assess the connection between pubertal timing and fecal microbiota, and to assess how fecal microbiota develop during puberty in comparison with adult microbiota, we utilized a Finnish allergy-prevention-trial cohort (Flora). Data collected at 13-year follow-up were compared with adult data from a different Finnish cohort. Among the 13-year-old participants we collected questionnaire information, growth data from school-health-system records and fecal samples from 148 participants. Reference adult fecal samples were received from the Health and Early Life Microbiota (HELMi) cohort (n = 840). Fecal microbiota were analyzed using 16S rRNA gene amplicon sequencing; the data were correlated with pubertal timing and compared with data on adult microbiota. Probiotic intervention in the allergy-prevention-trial cohort was considered as a confounding factor only. The main outcome was composition of the microbiota in relation to pubertal timing (time to/from peak growth velocity) in both sexes separately, and similarity to adult microbiota. In girls, fecal microbiota became more adult-like with pubertal progression (p = 0.009). No such development was observed in boys (p = 0.9). Both sexes showed a trend towards increasing relative abundance of estrogen-metabolizing Clostridia and decreasing Bacteroidia with pubertal development, but this was statistically significant in girls only (p = 0.03). In girls, pubertal timing was associated positively with exposure to cephalosporins prior to the age of 10. Our data support the hypothesis that gut microbiota, particularly members of Ruminococcaceae, may affect pubertal timing, possibly via regulating host sex-hormone levels. Trial registration The registration number for the allergy-prevention-trial cohort: ClinicalTrials.gov, NCT00298337, registered 1 March 2006—Retrospectively registered, https://clinicaltrials.gov/show/NCT00298337. The adult-comparison cohort (HELMi) is NCT03996304.
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spelling pubmed-86400052021-12-06 Gut microbiota develop towards an adult profile in a sex-specific manner during puberty Korpela, Katri Kallio, Sampo Salonen, Anne Hero, Matti Kukkonen, Anna Kaarina Miettinen, Päivi J. Savilahti, Erkki Kohva, Ella Kariola, Laura Suutela, Maria Tarkkanen, Annika de Vos, Willem M. Raivio, Taneli Kuitunen, Mikael Sci Rep Article Accumulating evidence indicates that gut microbiota may regulate sex-hormone levels in the host, with effects on reproductive health. Very little is known about the development of intestinal microbiota during puberty in humans. To assess the connection between pubertal timing and fecal microbiota, and to assess how fecal microbiota develop during puberty in comparison with adult microbiota, we utilized a Finnish allergy-prevention-trial cohort (Flora). Data collected at 13-year follow-up were compared with adult data from a different Finnish cohort. Among the 13-year-old participants we collected questionnaire information, growth data from school-health-system records and fecal samples from 148 participants. Reference adult fecal samples were received from the Health and Early Life Microbiota (HELMi) cohort (n = 840). Fecal microbiota were analyzed using 16S rRNA gene amplicon sequencing; the data were correlated with pubertal timing and compared with data on adult microbiota. Probiotic intervention in the allergy-prevention-trial cohort was considered as a confounding factor only. The main outcome was composition of the microbiota in relation to pubertal timing (time to/from peak growth velocity) in both sexes separately, and similarity to adult microbiota. In girls, fecal microbiota became more adult-like with pubertal progression (p = 0.009). No such development was observed in boys (p = 0.9). Both sexes showed a trend towards increasing relative abundance of estrogen-metabolizing Clostridia and decreasing Bacteroidia with pubertal development, but this was statistically significant in girls only (p = 0.03). In girls, pubertal timing was associated positively with exposure to cephalosporins prior to the age of 10. Our data support the hypothesis that gut microbiota, particularly members of Ruminococcaceae, may affect pubertal timing, possibly via regulating host sex-hormone levels. Trial registration The registration number for the allergy-prevention-trial cohort: ClinicalTrials.gov, NCT00298337, registered 1 March 2006—Retrospectively registered, https://clinicaltrials.gov/show/NCT00298337. The adult-comparison cohort (HELMi) is NCT03996304. Nature Publishing Group UK 2021-12-02 /pmc/articles/PMC8640005/ /pubmed/34857814 http://dx.doi.org/10.1038/s41598-021-02375-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Korpela, Katri
Kallio, Sampo
Salonen, Anne
Hero, Matti
Kukkonen, Anna Kaarina
Miettinen, Päivi J.
Savilahti, Erkki
Kohva, Ella
Kariola, Laura
Suutela, Maria
Tarkkanen, Annika
de Vos, Willem M.
Raivio, Taneli
Kuitunen, Mikael
Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
title Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
title_full Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
title_fullStr Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
title_full_unstemmed Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
title_short Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
title_sort gut microbiota develop towards an adult profile in a sex-specific manner during puberty
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8640005/
https://www.ncbi.nlm.nih.gov/pubmed/34857814
http://dx.doi.org/10.1038/s41598-021-02375-z
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