Alterations in the Vaginal Microbiome by Maternal Stress Are Associated With Metabolic Reprogramming of the Offspring Gut and Brain
Open accessAbstract
The neonate is exposed to the maternal vaginal microbiota during parturition, providing the primary source for normal gut colonization, host immune maturation, and metabolism. These early interactions between the host and microbiota occur during a critical window of neurodevelopment, suggesting early life as an important period of cross talk between the developing gut and brain. Because perturbations in the prenatal environment such as maternal stress increase neurodevelopmental disease risk, disruptions to the vaginal ecosystem could be a contributing factor in significant and long-term consequences for the offspring. Therefore, to examine the hypothesis that changes in the vaginal microbiome are associated with effects on the offspring gut microbiota and on the developing brain, we used genomic, proteomic and metabolomic technologies to examine outcomes in our mouse model of early prenatal stress. Multivariate modeling identified broad proteomic changes to the maternal vaginal environment that influence offspring microbiota composition and metabolic processes essential for normal neurodevelopment. Maternal stress altered proteins related to vaginal immunity and abundance of Lactobacillus, the prominent taxa in the maternal vagina. Loss of maternal vaginal Lactobacillus resulted in decreased transmission of this bacterium to offspring. Further, altered microbiota composition in the neonate gut corresponded with changes in metabolite profiles involved in energy balance, and with region- and sex-specific disruptions of amino acid profiles in the developing brain. Taken together, these results identify the vaginal microbiota as a novel factor by which maternal stress may contribute to reprogramming of the developing brain that may predispose individuals to neurodevelopmental disorders.
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Animal models demonstrate microbiome changes in response to maternal stress are passed onto offspring at birth, setting in motion microbial dysbiosis that persists into adulthood.
“Animal models demonstrate that microbiome changes in response to maternal stress are passed onto offspring at birth, setting in motion microbial dysbiosis that persists into adulthood (105–107).”
From Emerging Roles for the Gut Microbiome in Autism Spectrum Disorder (2017) · cites this paper as [106]
Prenatal stress induced depressive-like behavior in adulthood mice, which led to long-lasting change of enteric microbiota composition associated with exaggerated HPA axis response to stress.
“Prenatal stress induced depressive-like behavior in adulthood mice, which led to a long-lasting change of the enteric microbiota composition associated with an exaggerated HPA axis response to stress [353][354][355].”
From Anxiety, depression, and the microbiome: A role for gut peptides (2018) · cites this paper as [353]
Jašarević et al. demonstrated changes in the microbiome of offspring and alterations in the metabolome of the gut and brain.
“Jašarević et al. demonstrated changes in the microbiome of these offspring, as well as alterations in the metabolome of the gut and brain (343).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [343]
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The central nervous system and the gut microbiome
Sharon, G., Sampson, T. R., Geschwind, D. H., & Mazmanian, S. K. (2016) · Cell · doi:10.1016/j.cell.2016.10.027 · Cited by 1,513 · see citing works
Van den Bergh, B. R. H., van den Heuvel, M. I., Lahti, M., Braeken, M., de Rooij, S. R., Entringer, S., Hoyer, D., Roseboom, T., Räikkönen, K., King, S., et al. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.07.003 · Cited by 1,181 · see citing works
Stress & the gut-brain axis: Regulation by the microbiome
Foster, J. A., Rinaman, L., & Cryan, J. F. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.03.001 · Cited by 1,150 · see citing works
Kelly, J. R., Kennedy, P. J., Cryan, J. F., Dinan, T. G., Clarke, G., & Hyland, N. P. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00392 · Cited by 1,110 · see citing works
From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways
Rogers, G. B., Keating, D. J., Young, R. L., Wong, M.-L., Licinio, J., & Wesselingh, S. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.50 · Cited by 969 · see citing works
Kynurenine pathway metabolism and the microbiota-gut-brain axis
Kennedy, P. J., Cryan, J. F., Dinan, T. G., & Clarke, G. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.07.002 · Cited by 724 · see citing works
Banks, W. A., Gray, A. M., Erickson, M. A., Salameh, T. S., Damodarasamy, M., Sheibani, N., Meabon, J. S., Wing, E. E., Morofuji, Y., Cook, D. G., et al. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0434-1 · Cited by 636 · see citing works
Emerging Roles for the Gut Microbiome in Autism Spectrum Disorder
Vuong, H. E., & Hsiao, E. Y. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.08.024 · Cited by 595 · see citing works
Anxiety, depression, and the microbiome: A role for gut peptides
Lach, G., Schellekens, H., Dinan, T. G., & Cryan, J. F. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0585-0 · Cited by 573 · see citing works
The Gut–Brain Axis and the Microbiome: Mechanisms and Clinical Implications
Osadchiy, V., Martin, C. R., & Mayer, E. A. (2019) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2018.10.002 · Cited by 555 · see citing works
Wang, H.-X., & Wang, Y.-P. (2016) · Chinese Medical Journal · doi:10.4103/0366-6999.190667 · Cited by 546 · see citing works
The microbiome and host behavior
Vuong, H. E., Yano, J. M., Fung, T. C., & Hsiao, E. Y. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031347 · Cited by 537 · see citing works
The Microbiota–Gut–Brain Axis in Psychiatric Disorders
Góralczyk-Bińkowska, A., Szmajda‐Krygier, D., & Kozłowska, E. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231911245 · Cited by 534 · see citing works
Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
Rusch, J. A., Layden, B. T., & Dugas, L. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1130689 · Cited by 415 · see citing works
Walker, C., Bath, K. G., Joëls, M., Kőrösi, A., Larauche, M. H., Lucassen, P. J., Morris, M. J., Raineki, C., Roth, T. L., Sullivan, R. M., et al. (2017) · Stress · doi:10.1080/10253890.2017.1343296 · Cited by 402 · see citing works
Prenatal developmental origins of future psychopathology: mechanisms and pathways
Monk, C., Lugo-Candelas, C., & Trumpff, C. (2019) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050718-095539 · Cited by 388 · see citing works
Relationship between the gut microbiome and brain function
Mohajeri, M. H., La Fata, G., Steinert, R. E., & Weber, P. (2018) · Nutrition Reviews · doi:10.1093/nutrit/nuy009 · Cited by 376 · see citing works
Microbiota alteration is associated with the development of stress-induced despair behavior
Marin, I. A., Goertz, J. E., Ren, T., Rich, S. S., Onengut-Gumuscu, S., Farber, E., Wu, M., Overall, C. C., Kipnis, J., & Gaultier, A. (2017) · Scientific Reports · doi:10.1038/srep43859 · Cited by 369 · see citing works
Thomas, S., Izard, J., Walsh, E. K., Batich, K. A., Chongsathidkiet, P., Clarke, G. A., Sela, D. A., Muller, A. J., Mullin, J. M., Albert, K., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-2929 · Cited by 369 · see citing works
The Role of the Microbiome in the Developmental Origins of Health and Disease
Stiemsma, L. T., & Michels, K. B. (2018) · PEDIATRICS · doi:10.1542/peds.2017-2437 · Cited by 361 · see citing works
Brown, R. G., Marchesi, J. R., Lee, Y. S., Smith, A., Lehne, B., Kindinger, L. M., Terzidou, V., Holmes, E., Nicholson, J. K., Bennett, P. R., et al. (2018) · BMC Medicine · doi:10.1186/s12916-017-0999-x · Cited by 295 · see citing works
Sex differences in the gut microbiome–brain axis across the lifespan
Jašarević, E., Morrison, K. E., & Bale, T. L. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0122 · Cited by 294 · see citing works
Self-citationThe prenatal gut microbiome: are we colonized with bacteria in utero ?
Walker, R. W., Clemente, J. C., Peter, I., & Loos, R. J. F. (2017) · Pediatric Obesity · doi:10.1111/ijpo.12217 · Cited by 294 · see citing works
Cross talk: the microbiota and neurodevelopmental disorders
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G., & Dinan, T. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00490 · Cited by 271 · see citing works
Why do lactobacilli dominate the human vaginal microbiota?
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The gut microbiota–brain axis in neurological disorder
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Lewis, F. M. T., Bernstein, K. T., & Aral, S. O. (2017) · Obstetrics & Gynecology · doi:10.1097/aog.0000000000001932 · Cited by 248 · see citing works
Transfer of maternal psychosocial stress to the fetus
Rakers, F., Rupprecht, S., Dreiling, M., Bergmeier, C., Witte, O. W., & Schwab, M. G. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.019 · Cited by 231 · see citing works
The Microbiome in Psychology and Cognitive Neuroscience
Sarkar, A., Harty, S., Lehto, S. M., Moeller, A. H., Dinan, T. G., Dunbar, R., Cryan, J. F., & Burnet, P. W. J. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.04.006 · Cited by 231 · see citing works
The tantalizing links between gut microbes and the brain
Smith, P. A. (2015) · Nature · doi:10.1038/526312a · Cited by 221 · see citing works
Simon, E., Călinoiu, L. F., Mitrea, L., & Vodnar, D. C. (2021) · Nutrients · doi:10.3390/nu13062112 · Cited by 224 · see citing works
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Gur, T. L., Shay, L., Palkar, A. V., Fisher, S., Varaljay, V. A., Dowd, S., & Bailey, M. T. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.12.021 · Cited by 213 · see citing works
A gut (microbiome) feeling about the brain
Sherwin, E., Rea, K., Dinan, T. G., & Cryan, J. F. (2016) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000244 · Cited by 206 · see citing works
Early-life adversity and brain development: Is the microbiome a missing piece of the puzzle?
O’Mahony, S. M., Clarke, G., Dinan, T. G., & Cryan, J. F. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.068 · Cited by 203 · see citing works
You’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
Brain-gut-microbiota axis: challenges for translation in psychiatry
Kelly, J. R., Clarke, G. A., Cryan, J. F., & Dinan, T. G. (2016) · Annals of Epidemiology · doi:10.1016/j.annepidem.2016.02.008 · Cited by 200 · see citing works
Programming Bugs: Microbiota and the Developmental Origins of Brain Health and Disease
Codagnone, M. G., Spichak, S., O’Mahony, S. M., O’Leary, O. F., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.014 · Cited by 198 · see citing works
Heijtz, R. D. (2016) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2016.04.012 · Cited by 193 · see citing works
Jašarević, E., Howard, C. D., Morrison, K., Misic, A., Weinkopff, T., Scott, P., Hunter, C., Beiting, D., & Bale, T. L. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0182-5 · Cited by 189 · see citing works
Self-citationImmune dysfunction and neuroinflammation in autism spectrum disorder
Bjørklund, G., Saad, K., Chirumbolo, S., Kern, J. K., Geier, D. A., Geier, M. R., & Urbina, M. A. (2016) · Acta Neurobiologiae Experimentalis · doi:10.21307/ane-2017-025 · Cited by 188 · see citing works
Harnessing Gut Microbes for Mental Health: Getting From Here to There
Bruce‐Keller, A. J., Salbaum, J. M., & Berthoud, H. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.08.014 · Cited by 188 · see citing works
Do bacteria shape our development? Crosstalk between intestinal microbiota and HPA axis
de Weerth, C. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.09.016 · Cited by 181 · see citing works
Cowan, C. S. M., Dinan, T. G., & Cryan, J. F. (2020) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13156 · Cited by 176 · see citing works
The Role of Gut Dysbiosis in the Pathophysiology of Neuropsychiatric Disorders
Anand, N., Gorantla, V. R., & Chidambaram, S. B. (2022) · Cells · doi:10.3390/cells12010054 · Cited by 185 · see citing works
From Probiotics to Psychobiotics: Live Beneficial Bacteria Which Act on the Brain-Gut Axis
Bermúdez‐Humarán, L. G., Salinas, E., Ortíz, G. G., Ramírez-Jirano, L. J., Morales, J. A., & Bitzer-Quintero, O. K. (2019) · Nutrients · doi:10.3390/nu11040890 · Cited by 172 · see citing works
Multifaceted origins of sex differences in the brain
McCarthy, M. (2016) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0106 · Cited by 166 · see citing works
The contribution of the gut microbiome to neurodevelopment and neuropsychiatric disorders
Warner, B. B. (2018) · Pediatric Research · doi:10.1038/s41390-018-0191-9 · Cited by 168 · see citing works
Understanding the gut microbiome of dairy calves: Opportunities to improve early-life gut health
Malmuthuge, N., & Guan, L. L. (2017) · Journal of Dairy Science · doi:10.3168/jds.2016-12239 · Cited by 167 · see citing works
Heim, C. M., Entringer, S., & Buss, C. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.12.011 · Cited by 158 · see citing works
Childhood adversity impact on gut microbiota and inflammatory response to stress during pregnancy
Hantsoo, L., Jašarević, E., Criniti, S., McGeehan, B., Tanes, C., Sammel, M. D., Elovitz, M. A., Compher, C., Wu, G., & Epperson, C. N. (2019) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.11.005 · Cited by 156 · see citing works
Self-citationA gut feeling: Microbiome-brain-immune interactions modulate social and affective behaviors
Sylvia, K. E., & Demas, G. E. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.02.001 · Cited by 151 · see citing works
Host contributes to longitudinal diversity of fecal microbiota in swine selected for lean growth
Lu, D., Tiezzi, F., Schillebeeckx, C., McNulty, N. P., Schwab, C. R., Shull, C. M., & Maltecca, C. (2018) · Microbiome · doi:10.1186/s40168-017-0384-1 · Cited by 149 · see citing works
Socioeconomic Status and the Gut Microbiome: A TwinsUK Cohort Study
Bowyer, R. C. E., Jackson, M. A., Le Roy, C. I., Ni Lochlainn, M., Spector, T. D., Dowd, J. B., & Steves, C. J. (2019) · Microorganisms · doi:10.3390/microorganisms7010017 · Cited by 150 · see citing works
Targeting gut microbiome: a novel and potential therapy for autism
Yang, Y., Tian, J., & Yang, B. (2018) · Life Sciences · doi:10.1016/j.lfs.2017.12.027 · Cited by 140 · see citing works
The role of the microbiome in the neurobiology of social behaviour
Sarkar, A., Harty, S., Johnson, K. V. ‐., Moeller, A. H., Carmody, R. N., Lehto, S. M., Erdman, S. E., Dunbar, R. I. M., & Burnet, P. W. J. (2020) · Biological Reviews · doi:10.1111/brv.12603 · Cited by 135 · see citing works
Moussaoui, N., Jacobs, J. P., Larauche, M. H., Biraud, M., Million, M., Mayer, E. A., & Taché, Y. (2016) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm16105 · Cited by 133 · see citing works
Gur, T. L., Palkar, A. V., Rajasekera, T., Allen, J., Niraula, A., Godbout, J., & Bailey, M. T. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.06.025 · Cited by 127 · see citing works
Prenatal and postnatal contributions of the maternal microbiome on offspring programming
Jašarević, E., & Bale, T. L. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100797 · Cited by 127 · see citing works
Self-citationThe female reproductive tract microbiotas, inflammation, and gynecological conditions
Gholiof, M., Luca, E. A.-D., & Wessels, J. M. (2022) · Frontiers in Reproductive Health · doi:10.3389/frph.2022.963752 · Cited by 131 · see citing works
Galley, J. D., Mashburn‐Warren, L., Blalock, L. C., Lauber, C. L., Carroll, J., Ross, K. M., Hobel, C. J., Coussons‐Read, M. E., Schetter, C. D., & Gur, T. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.10.005 · Cited by 120 · see citing works
Cattane, N., Richetto, J., & Cattaneo, A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.001 · Cited by 118 · see citing works
Roles of the Microbiota of the Female Reproductive Tract in Gynecological and Reproductive Health
Zhu, B., Tao, Z., Edupuganti, L., Serrano, M. G., & Buck, G. A. (2022) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00181-21 · Cited by 123 · see citing works
Inflammatory Bowel Disease: A Stressed “Gut/Feeling”
Oligschlaeger, Y., Yadati, T., Houben, T., Oliván, C. M. C., & Shiri‐Sverdlov, R. (2019) · Cells · doi:10.3390/cells8070659 · Cited by 116 · see citing works
Role of the Astroglial Glutamate Exchanger xCT in Ventral Hippocampus in Resilience to Stress
Nasca, C., Bigio, B., Zelli, D., de Angelis, P., Lau, T., Okamoto, M., Soya, H., Ni, J., Brichta, L., Greengard, P., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.020 · Cited by 113 · see citing works
Commensal bacteria‐immunity crosstalk shapes mucosal homeostasis in teleost fish
Yu, Y., Ding, L., Huang, Z., Xu, H., & Xu, Z. (2021) · Reviews in Aquaculture · doi:10.1111/raq.12570 · Cited by 114 · see citing works
The role of the gut microbiome in the development of schizophrenia
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G. A., & Dinan, T. G. (2020) · Schizophrenia Research · doi:10.1016/j.schres.2020.02.010 · Cited by 119 · see citing works
Cortisol-Related Signatures of Stress in the Fish Microbiome
Webster, T. M. U., Rodríguez‐Barreto, D., Consuegra, S., & de Leániz, C. G. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01621 · Cited by 112 · see citing works
The Potential Influence of the Bacterial Microbiome on the Development and Progression of ADHD
Bull-Larsen, S., & Mohajeri, M. H. (2019) · Nutrients · doi:10.3390/nu11112805 · Cited by 107 · see citing works
Degroote, S., Hunting, D. J., Baccarelli, A. A., & Takser, L. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.06.010 · Cited by 106 · see citing works
Gut Microbiota Interaction with the Central Nervous System throughout Life
Ojeda, J., Ávila, A., & Vidal, P. M. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10061299 · Cited by 107 · see citing works
Murphy, K., & Mitchell, C. M. (2016) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiw140 · Cited by 100 · see citing works
Pathways of Association from Stress to Obesity in Early Childhood
Miller, A. L., & Lumeng, J. C. (2018) · Obesity · doi:10.1002/oby.22155 · Cited by 100 · see citing works
Maternal Folic Acid Supplementation Mediates Offspring Health via DNA Methylation
Liu, H.-Y., Liu, S., & Zhang, Y. (2020) · Reproductive Sciences · doi:10.1007/s43032-020-00161-2 · Cited by 99 · see citing works
Sun, Q., Cheng, L., Zeng, X., Zhang, X., Wu, Z., & Weng, P. (2020) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2020.07.208 · Cited by 98 · see citing works
Neurobehavioral comorbidities of epilepsy: Role of inflammation
Mazarati, A. M., Lewis, M. L., & Pittman, Q. J. (2017) · Epilepsia · doi:10.1111/epi.13786 · Cited by 96 · see citing works
Psychosocial Stress, Cortisol Levels, and Maintenance of Vaginal Health
Amabebe, E., & Anumba, D. O. C. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00568 · Cited by 100 · see citing works
Interactions between reproductive biology and microbiomes in wild animal species
Comizzoli, P., Power, M. L., Bornbusch, S. L., & Muletz‐Wolz, C. R. (2021) · Animal Microbiome · doi:10.1186/s42523-021-00156-7 · Cited by 93 · see citing works
Intervention strategies for cesarean section–induced alterations in the microbiota-gut-brain axis
Moya-Pérez, Á., Luczynski, P., Renes, I. B., Wang, S., Borre, Y. E., Ryan, C. A., Knol, J., Stanton, C., Dinan, T. G., & Cryan, J. F. (2017) · Nutrition Reviews · doi:10.1093/nutrit/nuw069 · Cited by 95 · see citing works
The connection between microbiome and schizophrenia
Golofast, B., & Vales, K. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.12.011 · Cited by 92 · see citing works
Gut microbiota and central nervous system development
Principi, N., & Esposito, S. (2016) · Journal of Infection · doi:10.1016/j.jinf.2016.09.010 · Cited by 92 · see citing works
Probiotic, Prebiotic, and Brain Development
Cerdó, T., Ruiz-Rodriguez, A., Suárez, A., & Campoy, C. (2017) · Nutrients · doi:10.3390/nu9111247 · Cited by 94 · see citing works
Targeting the gut microbiota to influence brain development and function in early life
Wang, S., Harvey, L., Martı́n, R., van der Beek, E. M., Knol, J., Cryan, J. F., & Renes, I. B. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.002 · Cited by 92 · see citing works
Stress gets into the belly: Early life stress and the gut microbiome
Hantsoo, L. V., & Zemel, B. S. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113474 · Cited by 91 · see citing works
Maternal Immune Activation and Related Factors in the Risk of Offspring Psychiatric Disorders
Conway, F., & Brown, A. S. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00430 · Cited by 86 · see citing works
Recent Advances in Understanding the Structure and Function of the Human Microbiome
Mousa, W. K., Chehadeh, F., & Husband, S. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.825338 · Cited by 89 · see citing works
Gut-brain axis: A matter of concern in neuropsychiatric disorders…!
Naveed, M., Zhou, Q.-G., Chu, X., Taleb, A., Meng, F. J., Ahmed, B., Zhang, Y., Fukunaga, K., & Han, F. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110051 · Cited by 81 · see citing works
Guo, B., Zhang, J., Zhang, W., Chen, F., & Liu, B. (2023) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2023.2272769 · Cited by 84 · see citing works
Developmental responses to early‐life adversity: Evolutionary and mechanistic perspectives
Lu, A., Petrullo, L. A., Carrera, S. C., Feder, J. A., Schneider‐Crease, I. A., & Snyder‐Mackler, N. (2019) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.21791 · Cited by 75 · see citing works
Emerging literature in the Microbiota-Brain Axis and Perinatal Mood and Anxiety Disorders
Rackers, H., Thomas, S., Williamson, K., Posey, R., & Kimmel, M. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.05.020 · Cited by 74 · see citing works
Audet, M. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100772 · Cited by 79 · see citing works
Boonchooduang, N., Louthrenoo, O., Chattipakorn, N., & Chattipakorn, S. C. (2020) · European Journal of Nutrition · doi:10.1007/s00394-020-02383-1 · Cited by 76 · see citing works
Ilan, Y. (2019) · Clinical and Experimental Gastroenterology · doi:10.2147/ceg.s203823 · Cited by 76 · see citing works
Neonatal Necrotizing Enterocolitis: An Update on Pathophysiology, Treatment, and Prevention
Roberts, A. G., Younge, N. E., & Greenberg, R. G. (2024) · Pediatric Drugs · doi:10.1007/s40272-024-00626-w · Cited by 75 · see citing works
Microbiota and Neurodevelopmental Trajectories: Role of Maternal and Early-Life Nutrition
Codagnone, M. G., Stanton, C., O’Mahony, S. M., Dinan, T. G., & Cryan, J. F. (2019) · Annals of Nutrition and Metabolism · doi:10.1159/000499144 · Cited by 73 · see citing works
Intrauterine Microbiota: Missing, or the Missing Link?
Chen, H. J., & Gur, T. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.03.008 · Cited by 70 · see citing works
Oral microbiota and autism spectrum disorder (ASD)
Olsen, I., & Hicks, S. D. (2019) · Journal of Oral Microbiology · doi:10.1080/20002297.2019.1702806 · Cited by 73 · see citing works
The murine vaginal microbiota and its perturbation by the human pathogen group B Streptococcus
Vrbanac, A. F., Riestra, A. M., Coady, A. M., Knight, R. D., Nizet, V., & Patras, K. A. (2018) · BMC Microbiology · doi:10.1186/s12866-018-1341-2 · Cited by 66 · see citing works
- Authors
- Jašarević, E., Howerton, C. L., Howard, C. D., & Bale, T. L.
- Affiliations
- University of Pennsylvania (US)
- Corresponding author
- Bale, Tracy L.
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2015-06-16
- Volume
- 156
- Issue
- 9
- Pages
- 3265-3276
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- PMC
- PMC4541625
- OpenAlex
- W1906460723
- Cited by
- 329
- References
- 91
- Citations by year
- 2026: 11 · 2025: 13 · 2024: 32 · 2023: 32 · 2022: 24 · 2021: 39 · 2020: 25 · 2019: 40 · 2018: 33 · 2017: 37 · 2016: 35 · 2015: 8
- FWCI
- 16.35
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Endocrinology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Pennsylvania (P30DK19525)
- National Institutes of Health (5r01mh091258-05, MH104184, DK 19525, MH091258)
- Perelman School of Medicine, University of Pennsylvania (P30-DK19525)
- National Institute of Mental Health (P50MH099910, MH087597, MH 104184, MH 091258, R33MH104184, R01 MH-091258, R21MH104184, R01MH087597)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30 DK 19525, P30DK019525)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
- Keywords
- maternal stress, vaginal microbiota, prenatal stress, neonatal gut microbiota, Lactobacillus, brain development, brain metabolomics, amino acid metabolism, energy balance, vaginal immunity, neurodevelopmental disorders, host-microbiota interactions
- MeSH terms
- Amino Acids, Animals, Brain, Colon, Female, Male, Mice, Inbred C57BL, Pregnancy, Pregnancy, Animal, Random Allocation, Sex Characteristics, Stress, Psychological, Vagina, Mice, 129 Strain, Microbiota
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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