The DOI matches its Crossref record; 90 of the 91 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The gut microbiota shapes intestinal immune responses during health and disease
Round, J. L., & Mazmanian, S. K. (2009) · Nature Reviews Immunology · doi:10.1038/nri2515 · Cited by 5,029
Dominguez-Bello, M. G., Costello, E. K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., & Knight, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002601107 · Cited by 4,774
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
Cryan, J. F., & Dinan, T. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3346 · Cited by 4,572
Vaginal microbiome of reproductive-age women
Ravel, J., Gajer, P., Abdo, Z., Schneider, G. M., Koenig, S. S. K., McCulle, S. L., Karlebach, S., Gorle, R., Russell, J., Tacket, C. O., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002611107 · Cited by 4,254
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., Codelli, J. A., Chow, J., Reisman, S. E., Petrosino, J. F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.024 · Cited by 3,283
Normal gut microbiota modulates brain development and behavior
Heijtz, R. D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H., & Pettersson, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010529108 · Cited by 3,228
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X., Kubo, C., & Koga, Y. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063388 · Cited by 2,735
Succession of microbial consortia in the developing infant gut microbiome
Koenig, J. E., Spor, A., Scalfone, N., Fricker, A. D., Stombaugh, J., Knight, R., Angenent, L. T., & Ley, R. E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000081107 · Cited by 2,540
The gut microbiota influences blood-brain barrier permeability in mice
Braniste, V., Al-Asmakh, M., Kowal, C., Anuar, F., Abbaspour, A., Tóth, M., Korecka, A., Bakocevic, N., Ng, L. G., Kundu, P., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009759 · Cited by 2,530
Orthogonal projections to latent structures (O‐PLS)
Trygg, J., & Wold, S. (2002) · Journal of Chemometrics · doi:10.1002/cem.695 · Cited by 2,523
Flagged first, then by citations
1 of the 91 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Items 101–200 of 330
Kelly, J. R., Keane, V. O., Cryan, J. F., Clarke, G., & Dinan, T. G. (2019) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2019.04.006 · Cited by 65
“Under the Skin” and into the Gut: Social Epidemiology of the Microbiome
Dowd, J. B., & Renson, A. (2018) · Current Epidemiology Reports · doi:10.1007/s40471-018-0167-7 · Cited by 66
The role of the commensal microbiota in adaptive and maladaptive stressor-induced immunomodulation
Mackos, A. R., Maltz, R. M., & Bailey, M. T. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.10.006 · Cited by 63
Immune recognition and response to the intestinal microbiome in type 1 diabetes
Paun, A., Yau, C., & Danska, J. S. (2016) · Journal of Autoimmunity · doi:10.1016/j.jaut.2016.02.004 · Cited by 67
Fuochi, V., Cardile, V., Petronio, G. P., & Furneri, P. M. (2018) · Journal of Applied Microbiology · doi:10.1111/jam.14164 · Cited by 62
Homberg, J. R., Kyzar, E. J., Scattoni, M. L., Norton, W., Pittman, J. T., Gaikwad, S., Nguyen, M., Poudel, M. K., Ullmann, J. F. P., Diamond, D. M., et al. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.04.015 · Cited by 67
The microbiome and disorders of the central nervous system
Felice, V. D., & O'Mahony, S. M. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.016 · Cited by 60
Microbiota of newborn meconium is associated with maternal anxiety experienced during pregnancy
Hu, J., Ly, J. J., Zhang, W., Huang, Y., Glover, V. A. S., Peter, I., Hurd, Y. L., & Nomura, Y. (2019) · Developmental Psychobiology · doi:10.1002/dev.21837 · Cited by 59
A Revolutionizing Approach to Autism Spectrum Disorder Using the Microbiome
Johnson, D., Letchumanan, V., Thurairajasingam, S., & Lee, L. (2020) · Nutrients · doi:10.3390/nu12071983 · Cited by 64
At the crux of maternal immune activation: Viruses, microglia, microbes, and IL‐17A
Otero, A. M., & Antonson, A. M. (2022) · Immunological Reviews · doi:10.1111/imr.13125 · Cited by 57
What’s bugging your teen?—The microbiota and adolescent mental health
McVey Neufeld, K.-A., Luczynski, P., Seira Oriach, C., Dinan, T. G., & Cryan, J. F. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.06.005 · Cited by 56
O’Callaghan, T. F., Ross, R. P., Stanton, C., & Clarke, G. A. (2016) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2016.05.003 · Cited by 56
The Role of the Gut Microbiota in the Development of Ischemic Stroke
Wang, J., Zhang, H., He, J., & Xiong, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.845243 · Cited by 56
Callaghan, B. L., Cowan, C. S. M., & Richardson, R. (2016) · Psychological Science · doi:10.1177/0956797616653103 · Cited by 55
Early‐life adversity, epigenetics, and visceral hypersensitivity
Liu, S., Hagiwara, S., & Bhargava, A. (2017) · Neurogastroenterology & Motility · doi:10.1111/nmo.13170 · Cited by 55
Cervicovaginal Microbiome Composition Is Associated with Metabolic Profiles in Healthy Pregnancy
Oliver, A. S., LaMere, B. J., Weihe, C., Wandro, S., Lindsay, K. L., Wadhwa, P. D., Mills, D. A., Pride, D. T., Fiehn, O., Northen, T. R., et al. (2020) · mBio · doi:10.1128/mbio.01851-20 · Cited by 56
Prenatal Maternal Stress and the Risk of Asthma in Children
Douros, K., Moustaki, M., Tsabouri, S., Papadopoulou, A., Papadopoulos, M., & Priftis, K. Ν. (2017) · Frontiers in Pediatrics · doi:10.3389/fped.2017.00202 · Cited by 55
Ntranos, A., & Casaccia, P. (2017) · Neurotherapeutics · doi:10.1007/s13311-017-0597-9 · Cited by 52
Ortega, V. A., Mercer, E. M., Giesbrecht, G. F., & Arrieta, M. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.634539 · Cited by 55
Jahnke, H. R., Roach, J. M., Azcárate-Peril, M. A., & Thompson, A. L. (2021) · PLoS ONE · doi:10.1371/journal.pone.0251782 · Cited by 56
MicroRNA Cross-Involvement in Autism Spectrum Disorders and Atopic Dermatitis: A Literature Review
Tonacci, A., Bagnato, G., Pandolfo, G., Billeci, L., Sansone, F., Conte, R., & Gangemi, S. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8010088 · Cited by 51
Korach-Rechtman, H., Freilich, S., Gerassy-Vainberg, S., Buhnik‐Rosenblau, K., Danin‐Poleg, Y., Bar, H., & Kashi, Y. (2019) · Applied and Environmental Microbiology · doi:10.1128/aem.00826-19 · Cited by 51
The microbiome and childhood diseases: Focus on brain‐gut axis
O’Mahony, S. M., Stilling, R. M., Dinan, T. G., & Cryan, J. F. (2015) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.21118 · Cited by 53
Neonatal microbiome – a brief review
Singh, A., & Mittal, M. (2019) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2019.1583738 · Cited by 50
He, J., Zheng, W., Tao, C., Guo, H., Xue, Y., Zhao, R., & Yao, W. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.115111 · Cited by 50
Long‐Term Vegan Meditation Improved Human Gut Microbiota
Jia, W., Zhen, J., Liu, A., Yuan, J., Wu, X.-L., Zhao, P., Zhao, L., Li, X., Liu, Q., Huang, G., et al. (2020) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2020/9517897 · Cited by 52
Prenatal stress impacts foetal neurodevelopment: Temporal windows of gestational vulnerability
Collins, J. M., Keane, J. M., Deady, C., Khashan, A. S., McCarthy, F. P., O’Keeffe, G. W., Clarke, G. A., Cryan, J. F., Caputi, V., & O’Mahony, S. M. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105793 · Cited by 52
Human microbiome restoration and safety
Daliri, E. B., Tango, C. N., Lee, B. H., & Oh, D. (2018) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2018.05.002 · Cited by 50
Animal Models for Functional Gastrointestinal Disorders
Accarie, A., & Vanuytsel, T. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.509681 · Cited by 51
Zhang, Z., Li, N., Chen, R., Lee, T., Gao, Y.-X., Yuan, Z., Nie, Y., & Sun, T. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100333 · Cited by 51
Maternal effects in mammals: Broadening our understanding of offspring programming
Edwards, P. D., Lavergne, S. G., McCaw, L. K., Wijenayake, S., Boonstra, R., McGowan, P. O., & Holmes, M. M. (2021) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2021.100924 · Cited by 49
Prenatal Maternal Stress Exacerbates Experimental Colitis of Offspring in Adulthood
Sun, Y., Xie, R., Lü, L., Jin, G., Zhou, B., Huang, H., Li, M., Yang, Y., Liu, X., Cao, X., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.700995 · Cited by 49
Decoding the neurocircuitry of gut feelings: Region-specific microbiome-mediated brain alterations
Sharvin, B. L., Aburto, M. R., & Cryan, J. F. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106033 · Cited by 51
Framing the discussion of microorganisms as a facet of social equity in human health
Ishaq, S. L., Rapp, M., Byerly, R., McClellan, L. S., O’Boyle, M. R., Nykanen, A., Fuller, P. J., Aas, C., Stone, J. M., Killpatrick, S., et al. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000536 · Cited by 50
Querdasi, F. R., Enders, C. K., Karnani, N., Broekman, B. F. P., Seng, C. Y., Gluckman, P. D., Daniel, L. M., Yap, F. K. P., Eriksson, J. G., Cai, S., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2213768120 · Cited by 47
Probiotics in human mental health and diseases—A minireview
Sivamaruthi, B. S., Prasanth, M. I., Kesika, P., & Chaiyasut, C. (2021) · Tropical Journal of Pharmaceutical Research · doi:10.4314/tjpr.v18i4.29 · Cited by 44
Social and population health science approaches to understand the human microbiome
Herd, P., Palloni, A., Rey, F. E., & Dowd, J. B. (2018) · Nature Human Behaviour · doi:10.1038/s41562-018-0452-y · Cited by 45
Maternal depressive symptoms linked to reduced fecal Immunoglobulin A concentrations in infants
Kang, L. J., Koleva, P. T., Field, C. J., Giesbrecht, G. F., Wine, E., Becker, A. B., Mandhane, P. J., Turvey, S. E., Subbarao, P., Sears, M. R., et al. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.10.007 · Cited by 43
Abecia, L., Martínez, G., Waddams, K. E., Martín-García, A. I., Pinloche, E., Creevey, C. J., Denman, S. E., Newbold, C. J., & Yáñez-Ruíz, D. R. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02227 · Cited by 48
Thomann, A., Mak, J. W. Y., Zhang, J., Wüstenberg, T., Ebert, M. P., Sung, J. J. �., Bernstein, C. N., Reindl, W., & Ng, S. C. (2020) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.15787 · Cited by 44
Stress in the microbiome-immune crosstalk
Beurel, E. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2327409 · Cited by 48
Smith, L. K., & Wissel, E. F. (2019) · Perspectives on Psychological Science · doi:10.1177/1745691618809379 · Cited by 46
Inflammation in Mental Disorders: Is the Microbiota the Missing Link?
Marin, S., Hé, Y., Butler, K., & Tsuang, M. T. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00535-1 · Cited by 44
Malnutrition and the microbiome as modifiers of early neurodevelopment
Coley, E. J. L., & Hsiao, E. Y. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.06.004 · Cited by 40
Is the role of human female reproductive tract microbiota underestimated?
Kamińska, D., & Gajęcka, M. (2017) · Beneficial Microbes · doi:10.3920/bm2015.0174 · Cited by 39
Sex Difference of Gut Microbiota
Kim, N. (2022) · Springer eBooks · doi:10.1007/978-981-19-0120-1_22 · Cited by 42
Stress and the Microbiota-Gut-Brain Axis
Cryan, J. F. (2016) · The Canadian Journal of Psychiatry · doi:10.1177/0706743716635538 · Cited by 40
Mitchell, E. J., Klein, S. L., Argyropoulos, K. V., Sharma, A., Chan, R., Toth, J. G., Barboza, L., Bavley, C. C., Bortolozzi, A. A., Chen, Q., et al. (2016) · Nature Communications · doi:10.1038/ncomms11492 · Cited by 38
Prenatal stress-induced disruptions in microbial and host tryptophan metabolism and transport
Galley, J. D., Chen, H. J., Antonson, A. M., & Gur, T. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113471 · Cited by 47
ADHD-originating in the gut? The emergence of a new explanatory model
Sandgren, A. M., & Brummer, R. J. (2018) · Medical Hypotheses · doi:10.1016/j.mehy.2018.08.022 · Cited by 40
Family SES Is Associated with the Gut Microbiome in Infants and Children
Lewis, C. R., Bonham, K. S., McCann, S., Volpe, A. R., D’Sa, V. A., Naymik, M., Both, M. D. D., Huentelman, M. J., Lemery‐Chalfant, K., Highlander, S. K., et al. (2021) · Microorganisms · doi:10.3390/microorganisms9081608 · Cited by 36
Prenatal programming of environmental sensitivity
Hartman, S., Belsky, J., & Pluess, M. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02461-y · Cited by 45
Contribution of Epithelial Cells to Defense Mechanisms in the Human Vagina
Linhares, I. M., Sisti, G., Minis, E. E., de Freitas, G. B., Moron, A. F., & Witkin, S. S. (2019) · Current Infectious Disease Reports · doi:10.1007/s11908-019-0686-5 · Cited by 37
How gut microbiota may impact ocular surface homeostasis and related disorders
Labétoulle, M., Baudouin, C., del Castillo, J. M. B., Rolando, M., Rescigno, M., Messmer, E. S. B. M., & Aragona, P. (2024) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2024.101250 · Cited by 38
Bushby, E. V., Friel, M., Goold, C. M., Gray, H. E., Smith, L., & Collins, L. (2018) · Frontiers in Veterinary Science · doi:10.3389/fvets.2018.00193 · Cited by 42
Hong, M., Zhang, R., Liu, Y., Wu, Z., & Weng, P. (2021) · Journal of Food Biochemistry · doi:10.1111/jfbc.13870 · Cited by 35
Vogel, S. C., Brito, N. H., & Callaghan, B. L. (2020) · Current Psychiatry Reports · doi:10.1007/s11920-020-01186-9 · Cited by 32
Haq, S. U., Bhat, U. A., & Kumar, A. (2021) · Journal of Biosciences · doi:10.1007/s12038-021-00153-7 · Cited by 37
Menichini, D., Chiossi, G., Monari, F., Seta, F. D., & Facchinetti, F. (2022) · Nutrients · doi:10.3390/nu14214520 · Cited by 33
Role of microbiota function during early life on child's neurodevelopment
Cerdó, T., Garcia-Valdes, L., Altmäe, S., Ruiz-Rodriguez, A., Suárez, A., & Campoy, C. (2016) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2016.08.007 · Cited by 33
Immune-Kynurenine Pathways and the Gut Microbiota-Brain Axis in Anxiety Disorders
Evrensel, A., Ünsalver, B. Ö., & Ceylan, M. E. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-981-32-9705-0_10 · Cited by 35
Abu, Y. F., Singh, S., Tao, J., Chupikova, I., Singh, P. K., Meng, J., & Roy, S. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2292224 · Cited by 32
Castro-Quintas, A., Palma-Gudiel, H., Martín-González, N. S., Caso, J., Leza, J., & Fañanás, L. (2023) · Frontiers in neuroendocrinology (Print) · doi:10.1016/j.yfrne.2023.101083 · Cited by 29
Tochitani, S. (2020) · Neuroscience Research · doi:10.1016/j.neures.2020.11.006 · Cited by 30
Turpin, R., Slopen, N. B., Borgogna, J.-L. C., Yeoman, C. J., He, X., Miller, R. S., Klebanoff, M. A., Ravel, J., & Brotman, R. M. (2021) · American Journal of Epidemiology · doi:10.1093/aje/kwab147 · Cited by 35
Maternal psychological distress before birth influences gut immunity in mid‐infancy
Kang, L. J., Vu, K. N., Koleva, P. T., Field, C. J., Chow, A., Azad, M. B., Becker, A. B., Mandhane, P. J., Moraes, T. J., Sears, M. R., et al. (2019) · Clinical & Experimental Allergy · doi:10.1111/cea.13551 · Cited by 28
Deoni, S., D’Sa, V. A., Volpe, A. R., Beauchemin, J., Croff, J. M., Elliott, A., Pini, N., Lucchini, M., & Fifer, W. P. (2022) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2022.101059 · Cited by 29
Karczewski, J., Zielińska, A., Staszewski, R., Eder, P., Dobrowolska, A., & Souto, E. B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116145 · Cited by 27
Epigenetic Aberrations in Major Psychiatric Diseases Related to Diet and Gut Microbiome Alterations
Nohesara, S., Abdolmaleky, H. M., & Thiagalingam, S. (2023) · Genes · doi:10.3390/genes14071506 · Cited by 32
Nunn, K. L., Ridenhour, B. J., Chester, E. M., Vitzthum, V. J., Fortenberry, J. D., & Forney, L. J. (2019) · Journal of Adolescent Health · doi:10.1016/j.jadohealth.2019.01.010 · Cited by 26
Karpiński, P., Żebrowska-Różańska, P., Kujawa, D., Łaczmański, Ł., Samochowiec, J., Jabłoński, M., Plichta, P., Piotrowski, P., Bielawski, T., & Misiak, B. (2023) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2023.106335 · Cited by 30
The Interaction between Stress and Inflammatory Bowel Disease in Pediatric and Adult Patients
Belei, O., Basaca, D.-G., Olariu, L., Pantea, M., Bozgan, D., Nanu, A.-M., Sîrbu, I., Mărginean, O., & Enătescu, I. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13051361 · Cited by 30
Dietert, R. R. (2016) · Reproductive Toxicology · doi:10.1016/j.reprotox.2016.04.026 · Cited by 25
Considering the Microbiome in Stress-Related and Neurodevelopmental Trajectories to Schizophrenia
Hoffman, K. W., Lee, J. J., Corcoran, C. M., Kimhy, D., Kranz, T. M., & Malaspina, D. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00629 · Cited by 24
Role of the Intestinal Microbiota in Host Responses to Stressor Exposure
Mackos, A. R., Varaljay, V. A., Maltz, R. M., Gur, T., & Bailey, M. T. (2016) · International review of neurobiology · doi:10.1016/bs.irn.2016.08.002 · Cited by 25
Stress and the Gut-Brain Axis: Implications for Cancer, Inflammation and Sepsis
Moughnyeh, M., Brawner, K. M., Kennedy, B. A., Yeramilli, V. A., Udayakumar, N., Graham, J. A., & Martin, C. A. (2021) · Journal of Surgical Research · doi:10.1016/j.jss.2021.02.055 · Cited by 24
Innovative methods for remote assessment of neurobehavioral development
Gustafsson, H., Young, A. S., Stamos, G., Wilken, S., Brito, N. H., Thomason, M. E., Graham, A. M., Nigg, J. T., & Sullivan, E. L. (2021) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2021.101015 · Cited by 22
Should we modulate the neonatal microbiome and what should be the goal?
van Best, N., Domínguez-Bello, M. G., Hornef, M. W., Jašarević, E., Korpela, K., & Lawley, T. D. (2022) · Microbiome · doi:10.1186/s40168-022-01281-4 · Cited by 23
Self-citationRadford‐Smith, D. E., & Anthony, D. C. (2023) · Metabolites · doi:10.3390/metabo13030455 · Cited by 23
Commentary: Lactobacilli Dominance and Vaginal pH: Why Is the Human Vaginal Microbiome Unique?
Fuochi, V., Volti, G. L., & Furneri, P. M. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01815 · Cited by 22
Early Life Adversity, Microbiome, and Inflammatory Responses
Beurel, E., & Nemeroff, C. B. (2024) · Biomolecules · doi:10.3390/biom14070802 · Cited by 24
The microbiome as a modulator of neurological health across the maternal-offspring interface
Orchanian, S. B., & Hsiao, E. Y. (2025) · Journal of Clinical Investigation · doi:10.1172/jci184314 · Cited by 23
The Effect of Maternal Postpartum Practices on Infant Gut Microbiota: A Chinese Cohort Study
Wang, Y., Liu, Y., Bai, J., & Chen, X. (2019) · Microorganisms · doi:10.3390/microorganisms7110511 · Cited by 20
Zubcevic, J. A., Watkins, J., Lin, C., Bautista, B., Hatch, H. M., Tevosian, S. G., & Hayward, L. F. (2022) · Metabolites · doi:10.3390/metabo12080735 · Cited by 21
Sex-related patterns of the gut-microbiota-brain axis in the neuropsychiatric conditions
Manosso, L. M., Lin, J. H. X., Carlessi, A. S., Recco, K. C. C., Quevedo, J., Gonçalves, C. L., & Réus, G. Z. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.04.001 · Cited by 23
Altered stress responses in adults born by Caesarean section
Dinan, T. G., Kennedy, P. J., Morais, L. H., Murphy, A., Long-Smith, C. M., Moloney, G. M., Bastiaanssen, T. F. S., Allen, A. P., Collery, A., Mullins, D., et al. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100425 · Cited by 24
Cullen, A. E., Labad, J., Oliver, D., Al‐Diwani, A., Minichino, A., & Fusar‐Poli, P. (2023) · Current Neuropharmacology · doi:10.2174/1570159x21666230322145049 · Cited by 25
Roles of the gut microbiota in human neurodevelopment and adult brain disorders
Mallick, R., Basak, S., Das, R. K., Banerjee, A., Paul, S., Pathak, S., & Duttaroy, A. K. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1446700 · Cited by 54
Hua, H., Huang, L., Yang, B., Jiang, S., Zhang, Y., Liu, J., Yan, C., & Xu, J. (2023) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2023.114798 · Cited by 17
Hunter, S., Flaten, E., Petersen, C., Gervain, J., Werker, J. F., Trainor, L. J., & Finlay, B. B. (2023) · PLoS ONE · doi:10.1371/journal.pone.0288689 · Cited by 21
A Spectrum of Solutions: Unveiling Non-Pharmacological Approaches to Manage Autism Spectrum Disorder
Mondal, A., Sharma, R., Abiha, U., Ahmad, F., Karan, A., Jayaraj, R. L., & Sundar, V. (2023) · Medicina · doi:10.3390/medicina59091584 · Cited by 21
Banks, W. (2020) · Current pharmaceutical design · doi:10.2174/138161282601200225102049 · Cited by 7
Context‐dependent effects of glucocorticoids on the lizard gut microbiome
MacLeod, K. J., Kohl, K. D., Trevelline, B. K., & Langkilde, T. L. (2021) · Molecular Ecology · doi:10.1111/mec.16229 · Cited by 16
Edinburgh postpartum depression scores are associated with vaginal and gut microbiota in pregnancy
Nel, N. H., Marafie, A., Bassis, C. M., Sugino, K. Y., Nzerem, A. C., Knickmeyer, R. R., McKee, K. S., & Comstock, S. S. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.10.086 · Cited by 17
Cusick, J. A., Wellman, C. L., & Demas, G. E. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105146 · Cited by 17
Mattiola, I., & Diefenbach, A. (2023) · Seminars in Immunology · doi:10.1016/j.smim.2023.101724 · Cited by 17
Holcomb, L. E., Holman, J. M., Hurd, M., Lavoie, B. A., Colucci, L., Hunt, B., Hunt, T., Kinney, M. S., Pathak, J., Mawe, G. M., et al. (2023) · mSystems · doi:10.1128/msystems.00688-23 · Cited by 20
Stress and depression-associated shifts in gut microbiota: A pilot study of human pregnancy
Rajasekera, T. A., Galley, J. D., Mackos, A. R., Chen, H. J., Mitchell, J. G., Kleinman, J. J., Cappelucci, P., Mashburn‐Warren, L., Lauber, C. L., Bailey, M. T., et al. (2024) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2024.100730 · Cited by 19
Fecal Metabolomics as a Novel Noninvasive Method for Short-Term Stress Monitoring in Beef Cattle
Valerio, A., Casadei, L., Giuliani, A., & Valerio, M. (2019) · Journal of Proteome Research · doi:10.1021/acs.jproteome.9b00655 · Cited by 16
Skillington, O., Mills, S., Gupta, A., Mayer, E. A., Gill, C. I. R., Rio, D. D., O’Riordan, K. J., Cryan, J. F., Ross, R. P., & Stanton, C. (2021) · Nutrition and Healthy Aging · doi:10.3233/nha-210129 · Cited by 18
Metadata
- 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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review