Stress and depression-associated shifts in gut microbiota: A pilot study of human pregnancy
Background: Psychosocial stress and mood-related disorders, such as depression, are prevalent and vulnerability to these conditions is heightened during pregnancy. Psychosocial stress induces consequences via several mechanisms including the gut microbiota-brain axis and associated signaling pathway...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-03-01
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| Series: | Brain, Behavior, & Immunity - Health |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2666354624000085 |
| _version_ | 1797271239685832704 |
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| author | Therese A. Rajasekera Jeffrey D. Galley Amy R. Mackos Helen J. Chen Justin G. Mitchell Joshua J. Kleinman Paige Cappelucci Lauren Mashburn-Warren Christian L. Lauber Michael T. Bailey Brett L. Worly Tamar L. Gur |
| author_facet | Therese A. Rajasekera Jeffrey D. Galley Amy R. Mackos Helen J. Chen Justin G. Mitchell Joshua J. Kleinman Paige Cappelucci Lauren Mashburn-Warren Christian L. Lauber Michael T. Bailey Brett L. Worly Tamar L. Gur |
| author_sort | Therese A. Rajasekera |
| collection | DOAJ |
| description | Background: Psychosocial stress and mood-related disorders, such as depression, are prevalent and vulnerability to these conditions is heightened during pregnancy. Psychosocial stress induces consequences via several mechanisms including the gut microbiota-brain axis and associated signaling pathways. Previous preclinical work indicates that prenatal stress alters maternal gut microbial composition and impairs offspring development. Importantly, although the fecal and vaginal microenvironments undergo alterations across pregnancy, we lack consensus regarding which shifts are adaptive or maladaptive in the presence of prenatal stress and depression. Clinical studies interrogating these relationships have identified unique taxa but have been limited in study design. Methods: We conducted a prospective cohort study of pregnant individuals consisting of repeated administration of psychometrics (Perceived Stress Scale (PSS) and Center for Epidemiological Studies Depression Scale (CES-D)) and collection of fecal and vaginal microbiome samples. Fecal and vaginal microbial community composition across psychometric responses were interrogated using full-length 16S rRNA sequencing followed by α and β-diversity metrics and taxonomic abundance. Results: Early pregnancy stress was associated with increased abundance of fecal taxa not previously identified in related studies, and stress from late pregnancy through postpartum was associated with increased abundance of typical vaginal taxa and opportunistic pathogens in the fecal microenvironment. Additionally, in late pregnancy, maternal stress and depression scores were associated with each other and with elevated maternal C–C motif chemokine ligand 2 (CCL2) concentrations. At delivery, concordant with previous literature, umbilical CCL2 concentration was negatively correlated with relative abundance of maternal fecal Lactobacilli. Lastly, participants with more severe depressive symptoms experienced steeper decreases in prenatal vaginal α-diversity. Conclusion: These findings a) underscore previous preclinical and clinical research demonstrating the effects of prenatal stress on maternal microbiome composition, b) suggest distinct biological pathways for the consequences of stress versus depression and c) extend the literature by identifying several taxa which may serve critical roles in mediating this relationship. Thus, further interrogation of the role of specific maternal microbial taxa in relation to psychosocial stress and its sequelae is warranted. |
| first_indexed | 2024-03-07T13:58:55Z |
| format | Article |
| id | doaj.art-33c85d6cd0594ddc9d07005da7070ac9 |
| institution | Directory Open Access Journal |
| issn | 2666-3546 |
| language | English |
| last_indexed | 2024-03-07T13:58:55Z |
| publishDate | 2024-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Brain, Behavior, & Immunity - Health |
| spelling | doaj.art-33c85d6cd0594ddc9d07005da7070ac92024-03-07T05:30:17ZengElsevierBrain, Behavior, & Immunity - Health2666-35462024-03-0136100730Stress and depression-associated shifts in gut microbiota: A pilot study of human pregnancyTherese A. Rajasekera0Jeffrey D. Galley1Amy R. Mackos2Helen J. Chen3Justin G. Mitchell4Joshua J. Kleinman5Paige Cappelucci6Lauren Mashburn-Warren7Christian L. Lauber8Michael T. Bailey9Brett L. Worly10Tamar L. Gur11Department of Psychiatry and Behavioral Health, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Institute for Behavioral Medicine Research, The Ohio State University Wexner Medical Center, Columbus, OH, USADepartment of Psychiatry and Behavioral Health, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Institute for Behavioral Medicine Research, The Ohio State University Wexner Medical Center, Columbus, OH, USACollege of Nursing, The Ohio State University, Columbus, OH, USADepartment of Psychiatry and Behavioral Health, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Institute for Behavioral Medicine Research, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Medical Scientist Training Program, The Ohio State University, Columbus, OH, USA; Department of Neuroscience, The Ohio State University, Columbus, OH, USACollege of Medicine, The Ohio State University, Columbus, OH, USACollege of Medicine, The Ohio State University, Columbus, OH, USACollege of Medicine, The Ohio State University, Columbus, OH, USAInstitute for Genomic Medicine, Nationwide Children’s Hospital, Columbus, OH, USAInstitute for Genomic Medicine, Nationwide Children’s Hospital, Columbus, OH, USAInstitute for Behavioral Medicine Research, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Center for Microbial Pathogenesis, The Research Institute, Nationwide Children’s Hospital, Columbus, OH, USA; Department of Pediatrics, The Ohio State University Wexner Medical Center, Columbus, OH, USAObstetrics and Gynecology, The Ohio State University Wexner Medical Center, Columbus, OH, USADepartment of Psychiatry and Behavioral Health, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Institute for Behavioral Medicine Research, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Medical Scientist Training Program, The Ohio State University, Columbus, OH, USA; College of Medicine, The Ohio State University, Columbus, OH, USA; Dorothy M. Davis Heart and Lung Research Institute, The Ohio State University College of Medicine and Wexner Medical Center, Columbus, OH, USA; Department of Neuroscience, The Ohio State University, Columbus, OH, USA; Corresponding author. 120A Institute for Behavioral Medicine Research, 460 Medical Center Drive, Columbus, 43210, OH, USA.Background: Psychosocial stress and mood-related disorders, such as depression, are prevalent and vulnerability to these conditions is heightened during pregnancy. Psychosocial stress induces consequences via several mechanisms including the gut microbiota-brain axis and associated signaling pathways. Previous preclinical work indicates that prenatal stress alters maternal gut microbial composition and impairs offspring development. Importantly, although the fecal and vaginal microenvironments undergo alterations across pregnancy, we lack consensus regarding which shifts are adaptive or maladaptive in the presence of prenatal stress and depression. Clinical studies interrogating these relationships have identified unique taxa but have been limited in study design. Methods: We conducted a prospective cohort study of pregnant individuals consisting of repeated administration of psychometrics (Perceived Stress Scale (PSS) and Center for Epidemiological Studies Depression Scale (CES-D)) and collection of fecal and vaginal microbiome samples. Fecal and vaginal microbial community composition across psychometric responses were interrogated using full-length 16S rRNA sequencing followed by α and β-diversity metrics and taxonomic abundance. Results: Early pregnancy stress was associated with increased abundance of fecal taxa not previously identified in related studies, and stress from late pregnancy through postpartum was associated with increased abundance of typical vaginal taxa and opportunistic pathogens in the fecal microenvironment. Additionally, in late pregnancy, maternal stress and depression scores were associated with each other and with elevated maternal C–C motif chemokine ligand 2 (CCL2) concentrations. At delivery, concordant with previous literature, umbilical CCL2 concentration was negatively correlated with relative abundance of maternal fecal Lactobacilli. Lastly, participants with more severe depressive symptoms experienced steeper decreases in prenatal vaginal α-diversity. Conclusion: These findings a) underscore previous preclinical and clinical research demonstrating the effects of prenatal stress on maternal microbiome composition, b) suggest distinct biological pathways for the consequences of stress versus depression and c) extend the literature by identifying several taxa which may serve critical roles in mediating this relationship. Thus, further interrogation of the role of specific maternal microbial taxa in relation to psychosocial stress and its sequelae is warranted.http://www.sciencedirect.com/science/article/pii/S2666354624000085Perceived stressPregnancyPeripartum stressGut microbiomeMaternal microbiome |
| spellingShingle | Therese A. Rajasekera Jeffrey D. Galley Amy R. Mackos Helen J. Chen Justin G. Mitchell Joshua J. Kleinman Paige Cappelucci Lauren Mashburn-Warren Christian L. Lauber Michael T. Bailey Brett L. Worly Tamar L. Gur Stress and depression-associated shifts in gut microbiota: A pilot study of human pregnancy Brain, Behavior, & Immunity - Health Perceived stress Pregnancy Peripartum stress Gut microbiome Maternal microbiome |
| title | Stress and depression-associated shifts in gut microbiota: A pilot study of human pregnancy |
| title_full | Stress and depression-associated shifts in gut microbiota: A pilot study of human pregnancy |
| title_fullStr | Stress and depression-associated shifts in gut microbiota: A pilot study of human pregnancy |
| title_full_unstemmed | Stress and depression-associated shifts in gut microbiota: A pilot study of human pregnancy |
| title_short | Stress and depression-associated shifts in gut microbiota: A pilot study of human pregnancy |
| title_sort | stress and depression associated shifts in gut microbiota a pilot study of human pregnancy |
| topic | Perceived stress Pregnancy Peripartum stress Gut microbiome Maternal microbiome |
| url | http://www.sciencedirect.com/science/article/pii/S2666354624000085 |
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