Antibiotic-induced gut dysbiosis and cognitive, emotional, and behavioral changes in rodents: a systematic review and meta-analysis
There are previous epidemiological studies reporting associations between antibiotic use and psychiatric symptoms. Antibiotic-induced gut dysbiosis and alteration of microbiota-gut-brain axis communication has been proposed to play a role in this association. In this systematic review and meta-analy...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-09-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2023.1237177/full |
| _version_ | 1827854706740822016 |
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| author | Shivdeep S. Hayer Shivdeep S. Hayer Shivdeep S. Hayer Shivdeep S. Hayer Soonjo Hwang Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton |
| author_facet | Shivdeep S. Hayer Shivdeep S. Hayer Shivdeep S. Hayer Shivdeep S. Hayer Soonjo Hwang Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton |
| author_sort | Shivdeep S. Hayer |
| collection | DOAJ |
| description | There are previous epidemiological studies reporting associations between antibiotic use and psychiatric symptoms. Antibiotic-induced gut dysbiosis and alteration of microbiota-gut-brain axis communication has been proposed to play a role in this association. In this systematic review and meta-analysis, we reviewed published articles that have presented results on changes in cognition, emotion, and behavior in rodents (rats and mice) after antibiotic-induced gut dysbiosis. We searched three databases—PubMed, Web of Science, and SCOPUS to identify such articles using dedicated search strings and extracted data from 48 articles. Increase in anxiety and depression-like behavior was reported in 32.7 and 40.7 percent of the study-populations, respectively. Decrease in sociability, social novelty preference, recognition memory and spatial cognition was found in 18.1, 35.3, 26.1, and 62.5 percent of the study-populations, respectively. Only one bacterial taxon (increase in gut Proteobacteria) showed statistically significant association with behavioral changes (increase in anxiety). There were no consistent findings with statistical significance for the potential biomarkers [Brain-derived neurotrophic factor (BDNF) expression in the hippocampus, serum corticosterone and circulating IL-6 and IL-1β levels]. Results of the meta-analysis revealed a significant association between symptoms of negative valence system (including anxiety and depression) and cognitive system (decreased spatial cognition) with antibiotic intake (p < 0.05). However, between-study heterogeneity and publication bias were statistically significant (p < 0.05). Risk of bias was evaluated to be high in the majority of the studies. We identified and discussed several reasons that could contribute to the heterogeneity between the results of the studies examined. The results of the meta-analysis provide promising evidence that there is indeed an association between antibiotic-induced gut dysbiosis and psychopathologies. However, inconsistencies in the implemented methodologies make generalizing these results difficult. Gut microbiota depletion using antibiotics may be a useful strategy to evaluate if and how gut microbes influence cognition, emotion, and behavior, but the heterogeneity in methodologies used precludes any definitive interpretations for a translational impact on clinical practice. |
| first_indexed | 2024-03-12T11:26:40Z |
| format | Article |
| id | doaj.art-d3633e85b8f048f6994b35b8618e6452 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-03-12T11:26:40Z |
| publishDate | 2023-09-01 |
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| series | Frontiers in Neuroscience |
| spelling | doaj.art-d3633e85b8f048f6994b35b8618e64522023-09-01T07:51:55ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-09-011710.3389/fnins.2023.12371771237177Antibiotic-induced gut dysbiosis and cognitive, emotional, and behavioral changes in rodents: a systematic review and meta-analysisShivdeep S. Hayer0Shivdeep S. Hayer1Shivdeep S. Hayer2Shivdeep S. Hayer3Soonjo Hwang4Jonathan B. Clayton5Jonathan B. Clayton6Jonathan B. Clayton7Jonathan B. Clayton8Jonathan B. Clayton9Jonathan B. Clayton10Department of Biology, University of Nebraska at Omaha, Omaha, NE, United StatesCallitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, United StatesNebraska Food for Health Center, University of Nebraska-Lincoln, Lincoln, NE, United StatesDepartment of Population Medicine, University of Guelph, Guelph, ON, CanadaDepartment of Psychiatry, University of Nebraska Medical Center, Omaha, NE, United StatesDepartment of Biology, University of Nebraska at Omaha, Omaha, NE, United StatesCallitrichid Research Center, University of Nebraska at Omaha, Omaha, NE, United StatesNebraska Food for Health Center, University of Nebraska-Lincoln, Lincoln, NE, United StatesDepartment of Food Science and Technology, University of Nebraska-Lincoln, Lincoln, NE, United StatesDepartment of Pathology and Microbiology, University of Nebraska Medical Center, Omaha, NE, United StatesPrimate Microbiome Project, University of Nebraska-Lincoln, Lincoln, NE, United StatesThere are previous epidemiological studies reporting associations between antibiotic use and psychiatric symptoms. Antibiotic-induced gut dysbiosis and alteration of microbiota-gut-brain axis communication has been proposed to play a role in this association. In this systematic review and meta-analysis, we reviewed published articles that have presented results on changes in cognition, emotion, and behavior in rodents (rats and mice) after antibiotic-induced gut dysbiosis. We searched three databases—PubMed, Web of Science, and SCOPUS to identify such articles using dedicated search strings and extracted data from 48 articles. Increase in anxiety and depression-like behavior was reported in 32.7 and 40.7 percent of the study-populations, respectively. Decrease in sociability, social novelty preference, recognition memory and spatial cognition was found in 18.1, 35.3, 26.1, and 62.5 percent of the study-populations, respectively. Only one bacterial taxon (increase in gut Proteobacteria) showed statistically significant association with behavioral changes (increase in anxiety). There were no consistent findings with statistical significance for the potential biomarkers [Brain-derived neurotrophic factor (BDNF) expression in the hippocampus, serum corticosterone and circulating IL-6 and IL-1β levels]. Results of the meta-analysis revealed a significant association between symptoms of negative valence system (including anxiety and depression) and cognitive system (decreased spatial cognition) with antibiotic intake (p < 0.05). However, between-study heterogeneity and publication bias were statistically significant (p < 0.05). Risk of bias was evaluated to be high in the majority of the studies. We identified and discussed several reasons that could contribute to the heterogeneity between the results of the studies examined. The results of the meta-analysis provide promising evidence that there is indeed an association between antibiotic-induced gut dysbiosis and psychopathologies. However, inconsistencies in the implemented methodologies make generalizing these results difficult. Gut microbiota depletion using antibiotics may be a useful strategy to evaluate if and how gut microbes influence cognition, emotion, and behavior, but the heterogeneity in methodologies used precludes any definitive interpretations for a translational impact on clinical practice.https://www.frontiersin.org/articles/10.3389/fnins.2023.1237177/fullgut microbiotabehavioranxietydepressionsocialantibiotics |
| spellingShingle | Shivdeep S. Hayer Shivdeep S. Hayer Shivdeep S. Hayer Shivdeep S. Hayer Soonjo Hwang Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton Jonathan B. Clayton Antibiotic-induced gut dysbiosis and cognitive, emotional, and behavioral changes in rodents: a systematic review and meta-analysis Frontiers in Neuroscience gut microbiota behavior anxiety depression social antibiotics |
| title | Antibiotic-induced gut dysbiosis and cognitive, emotional, and behavioral changes in rodents: a systematic review and meta-analysis |
| title_full | Antibiotic-induced gut dysbiosis and cognitive, emotional, and behavioral changes in rodents: a systematic review and meta-analysis |
| title_fullStr | Antibiotic-induced gut dysbiosis and cognitive, emotional, and behavioral changes in rodents: a systematic review and meta-analysis |
| title_full_unstemmed | Antibiotic-induced gut dysbiosis and cognitive, emotional, and behavioral changes in rodents: a systematic review and meta-analysis |
| title_short | Antibiotic-induced gut dysbiosis and cognitive, emotional, and behavioral changes in rodents: a systematic review and meta-analysis |
| title_sort | antibiotic induced gut dysbiosis and cognitive emotional and behavioral changes in rodents a systematic review and meta analysis |
| topic | gut microbiota behavior anxiety depression social antibiotics |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2023.1237177/full |
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