Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition

Digestive disorders of gut-brain interaction (DGBI) are very common, predominant in females, and usually associated with intestinal barrier dysfunction, dysbiosis, and stress. We previously found that females have increased susceptibility to intestinal barrier dysfunction in response to acute stress...

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Published inFrontiers in microbiology Vol. 15; p. 1441126
Main Authors Rodiño-Janeiro, Bruno K., Khannous-Lleiffe, Olfat, Pigrau, Marc, Willis, Jesse R., Salvo-Romero, Eloísa, Nieto, Adoración, Expósito, Elba, Fortea, Marina, Pardo-Camacho, Cristina, Albert-Bayo, Mercé, González-Castro, Ana María, Guagnozzi, Danila, Martínez, Cristina, Lobo, Beatriz, Vicario, María, Santos, Javier, Gabaldón, Toni, Alonso-Cotoner, Carmen
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 15.01.2025
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ISSN1664-302X
1664-302X
DOI10.3389/fmicb.2024.1441126

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Abstract Digestive disorders of gut-brain interaction (DGBI) are very common, predominant in females, and usually associated with intestinal barrier dysfunction, dysbiosis, and stress. We previously found that females have increased susceptibility to intestinal barrier dysfunction in response to acute stress. However, whether this is associated with changes in the small bowel microbiota remains unknown. We have evaluated changes in the small intestinal microbiota in response to acute stress to better understand stress-induced intestinal barrier dysfunction. Jejunal biopsies were obtained at baseline and 90 min after cold pain or sham stress. Autonomic (blood pressure and heart rate), hormonal (plasma cortisol and adrenocorticotropic hormone) and psychological (Subjective Stress Rating Scale) responses to cold pain and sham stress were monitored. Microbial DNA from the biopsies was analyzed using a 16S metabarcoding approach before and after cold pain stress and sham stress. Differences in diversity and relative abundance of microbial taxa were examined. Cold pain stress was associated with a significant decrease in alpha diversity ( = 0.015), which was more pronounced in females, along with significant sex differences in the abundance of specific taxa and the overall microbiota composition. Microbiota alterations significantly correlated with changes in psychological responses, hormones, and gene expression in the intestinal mucosal. Cold pain stress was also associated with activation of autonomic, hormonal and psychological response, with no differences between sexes. Acute stress elicits rapid alterations in bacterial composition in the jejunum of healthy subjects and these changes are more pronounced in females. Our results may contribute to the understanding of female predominance in DGBI.
AbstractList Background/aimsDigestive disorders of gut-brain interaction (DGBI) are very common, predominant in females, and usually associated with intestinal barrier dysfunction, dysbiosis, and stress. We previously found that females have increased susceptibility to intestinal barrier dysfunction in response to acute stress. However, whether this is associated with changes in the small bowel microbiota remains unknown. We have evaluated changes in the small intestinal microbiota in response to acute stress to better understand stress-induced intestinal barrier dysfunction.MethodsJejunal biopsies were obtained at baseline and 90 min after cold pain or sham stress. Autonomic (blood pressure and heart rate), hormonal (plasma cortisol and adrenocorticotropic hormone) and psychological (Subjective Stress Rating Scale) responses to cold pain and sham stress were monitored. Microbial DNA from the biopsies was analyzed using a 16S metabarcoding approach before and after cold pain stress and sham stress. Differences in diversity and relative abundance of microbial taxa were examined.ResultsCold pain stress was associated with a significant decrease in alpha diversity (P = 0.015), which was more pronounced in females, along with significant sex differences in the abundance of specific taxa and the overall microbiota composition. Microbiota alterations significantly correlated with changes in psychological responses, hormones, and gene expression in the intestinal mucosal. Cold pain stress was also associated with activation of autonomic, hormonal and psychological response, with no differences between sexes.ConclusionsAcute stress elicits rapid alterations in bacterial composition in the jejunum of healthy subjects and these changes are more pronounced in females. Our results may contribute to the understanding of female predominance in DGBI.
Digestive disorders of gut-brain interaction (DGBI) are very common, predominant in females, and usually associated with intestinal barrier dysfunction, dysbiosis, and stress. We previously found that females have increased susceptibility to intestinal barrier dysfunction in response to acute stress. However, whether this is associated with changes in the small bowel microbiota remains unknown. We have evaluated changes in the small intestinal microbiota in response to acute stress to better understand stress-induced intestinal barrier dysfunction. Jejunal biopsies were obtained at baseline and 90 min after cold pain or sham stress. Autonomic (blood pressure and heart rate), hormonal (plasma cortisol and adrenocorticotropic hormone) and psychological (Subjective Stress Rating Scale) responses to cold pain and sham stress were monitored. Microbial DNA from the biopsies was analyzed using a 16S metabarcoding approach before and after cold pain stress and sham stress. Differences in diversity and relative abundance of microbial taxa were examined. Cold pain stress was associated with a significant decrease in alpha diversity ( = 0.015), which was more pronounced in females, along with significant sex differences in the abundance of specific taxa and the overall microbiota composition. Microbiota alterations significantly correlated with changes in psychological responses, hormones, and gene expression in the intestinal mucosal. Cold pain stress was also associated with activation of autonomic, hormonal and psychological response, with no differences between sexes. Acute stress elicits rapid alterations in bacterial composition in the jejunum of healthy subjects and these changes are more pronounced in females. Our results may contribute to the understanding of female predominance in DGBI.
Digestive disorders of gut-brain interaction (DGBI) are very common, predominant in females, and usually associated with intestinal barrier dysfunction, dysbiosis, and stress. We previously found that females have increased susceptibility to intestinal barrier dysfunction in response to acute stress. However, whether this is associated with changes in the small bowel microbiota remains unknown. We have evaluated changes in the small intestinal microbiota in response to acute stress to better understand stress-induced intestinal barrier dysfunction.Background/aimsDigestive disorders of gut-brain interaction (DGBI) are very common, predominant in females, and usually associated with intestinal barrier dysfunction, dysbiosis, and stress. We previously found that females have increased susceptibility to intestinal barrier dysfunction in response to acute stress. However, whether this is associated with changes in the small bowel microbiota remains unknown. We have evaluated changes in the small intestinal microbiota in response to acute stress to better understand stress-induced intestinal barrier dysfunction.Jejunal biopsies were obtained at baseline and 90 min after cold pain or sham stress. Autonomic (blood pressure and heart rate), hormonal (plasma cortisol and adrenocorticotropic hormone) and psychological (Subjective Stress Rating Scale) responses to cold pain and sham stress were monitored. Microbial DNA from the biopsies was analyzed using a 16S metabarcoding approach before and after cold pain stress and sham stress. Differences in diversity and relative abundance of microbial taxa were examined.MethodsJejunal biopsies were obtained at baseline and 90 min after cold pain or sham stress. Autonomic (blood pressure and heart rate), hormonal (plasma cortisol and adrenocorticotropic hormone) and psychological (Subjective Stress Rating Scale) responses to cold pain and sham stress were monitored. Microbial DNA from the biopsies was analyzed using a 16S metabarcoding approach before and after cold pain stress and sham stress. Differences in diversity and relative abundance of microbial taxa were examined.Cold pain stress was associated with a significant decrease in alpha diversity (P = 0.015), which was more pronounced in females, along with significant sex differences in the abundance of specific taxa and the overall microbiota composition. Microbiota alterations significantly correlated with changes in psychological responses, hormones, and gene expression in the intestinal mucosal. Cold pain stress was also associated with activation of autonomic, hormonal and psychological response, with no differences between sexes.ResultsCold pain stress was associated with a significant decrease in alpha diversity (P = 0.015), which was more pronounced in females, along with significant sex differences in the abundance of specific taxa and the overall microbiota composition. Microbiota alterations significantly correlated with changes in psychological responses, hormones, and gene expression in the intestinal mucosal. Cold pain stress was also associated with activation of autonomic, hormonal and psychological response, with no differences between sexes.Acute stress elicits rapid alterations in bacterial composition in the jejunum of healthy subjects and these changes are more pronounced in females. Our results may contribute to the understanding of female predominance in DGBI.ConclusionsAcute stress elicits rapid alterations in bacterial composition in the jejunum of healthy subjects and these changes are more pronounced in females. Our results may contribute to the understanding of female predominance in DGBI.
Author Alonso-Cotoner, Carmen
Guagnozzi, Danila
Pardo-Camacho, Cristina
Salvo-Romero, Eloísa
Expósito, Elba
Gabaldón, Toni
Nieto, Adoración
Santos, Javier
Martínez, Cristina
Khannous-Lleiffe, Olfat
Albert-Bayo, Mercé
Vicario, María
Pigrau, Marc
González-Castro, Ana María
Rodiño-Janeiro, Bruno K.
Lobo, Beatriz
Willis, Jesse R.
Fortea, Marina
AuthorAffiliation 4 Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology , Barcelona , Spain
8 Renal Physiopathology Group, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain
6 Laboratory of Translational Mucosal Immunology, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain
1 Laboratory of Neuro-Immuno-Gastroenterology, Digestive System Research Unit, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain
5 Facultat de Medicina, Universitat Autònoma de Barcelona , Bellaterra , Spain
2 Department of Gastroenterology, Vall d'Hebron Hospital Universitari, Vall d'Hebron Barcelona Hospital Campus , Barcelona , Spain
9 Catalan Institution for Research and Advanced Studies (ICREA) , Barcelona , Spain
3 Barcelo
AuthorAffiliation_xml – name: 5 Facultat de Medicina, Universitat Autònoma de Barcelona , Bellaterra , Spain
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Copyright Copyright © 2025 Rodiño-Janeiro, Khannous-Lleiffe, Pigrau, Willis, Salvo-Romero, Nieto, Expósito, Fortea, Pardo-Camacho, Albert-Bayo, González-Castro, Guagnozzi, Martínez, Lobo, Vicario, Santos, Gabaldón and Alonso-Cotoner.
Copyright © 2025 Rodiño-Janeiro, Khannous-Lleiffe, Pigrau, Willis, Salvo-Romero, Nieto, Expósito, Fortea, Pardo-Camacho, Albert-Bayo, González-Castro, Guagnozzi, Martínez, Lobo, Vicario, Santos, Gabaldón and Alonso-Cotoner. 2025 Rodiño-Janeiro, Khannous-Lleiffe, Pigrau, Willis, Salvo-Romero, Nieto, Expósito, Fortea, Pardo-Camacho, Albert-Bayo, González-Castro, Guagnozzi, Martínez, Lobo, Vicario, Santos, Gabaldón and Alonso-Cotoner
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– notice: Copyright © 2025 Rodiño-Janeiro, Khannous-Lleiffe, Pigrau, Willis, Salvo-Romero, Nieto, Expósito, Fortea, Pardo-Camacho, Albert-Bayo, González-Castro, Guagnozzi, Martínez, Lobo, Vicario, Santos, Gabaldón and Alonso-Cotoner. 2025 Rodiño-Janeiro, Khannous-Lleiffe, Pigrau, Willis, Salvo-Romero, Nieto, Expósito, Fortea, Pardo-Camacho, Albert-Bayo, González-Castro, Guagnozzi, Martínez, Lobo, Vicario, Santos, Gabaldón and Alonso-Cotoner
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Keywords small intestine microbiota
stress
functional dyspepsia
irritable bowel syndrome
disorders of gut-brain interaction
Language English
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Edited by: Valeria D'Argenio, University of Naples Federico II, Italy
These authors share last authorship
Lorella Tripodi, Dipartimento di Medicina Molecolare e Biotecnologie Mediche (MMBM) Università Federico II di Napoli, Italy
These authors have contributed equally to this work and share first authorship
Present addresses: Bruno K. Rodiño-Janeiro, BFlow, Edificio Emprendia, Santiago de Compostela, Spain
Reviewed by: Muriel Larauche, University of California, Los Angeles, United States
María Vicario, Nestlé Institute of Health Sciences, Société des Produits Nestlé S.A., Lausanne, Switzerland
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Snippet Digestive disorders of gut-brain interaction (DGBI) are very common, predominant in females, and usually associated with intestinal barrier dysfunction,...
Background/aimsDigestive disorders of gut-brain interaction (DGBI) are very common, predominant in females, and usually associated with intestinal barrier...
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StartPage 1441126
SubjectTerms disorders of gut-brain interaction
functional dyspepsia
irritable bowel syndrome
Microbiology
small intestine microbiota
stress
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Title Acute stress triggers sex-dependent rapid alterations in the human small intestine microbiota composition
URI https://www.ncbi.nlm.nih.gov/pubmed/39881982
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Volume 15
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