Prenatal Stress Alters Bacterial Colonization of the Gut in Infant Monkeys
Open accessAbstract
Objective The hypothesis that prenatal stress lowers the levels of protective microflora and increases the risk for postpartum Gram-negative pathogens was tested in infant monkeys. Methods Female monkeys were left undisturbed or were stressed during pregnancy using an acoustical startle paradigm for 6 weeks either early or late in their 24-week gestation. Several types of intestinal microflora were repeatedly enumerated by fecal culture while infants were reared normally by their mothers. Results Significant changes in microflora concentrations occurred during the first 6 months of life. The profile of total aerobes and facultative anaerobes was biphasic, with peak concentrations occurring between 2 and 16 weeks of age. The numbers of bifidobacteria and lactobacilli were low at 2 days after birth but rapidly increased to a peak between 8 and 16 weeks of age. Although similar temporal patterns were evident in all infants, prenatal stress reduced the overall numbers of bifidobacteria and lactobacilli. Conclusions Moderate disturbance during pregnancy was sufficient to alter the intestinal microflora in the newborn infant. These alterations could result in enhanced susceptibility to infection and suggest a mechanism for some effects of maternal pregnancy conditions on infant health.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Both prenatal and postnatal stress were associated with transient reductions in the levels of the enteric microbiota in rhesus monkeys.
“Both pre natal17 and postnatal stress16 were associated with transient reductions in the levels of the enteric microbiota in rhesus monkeys.”
From Principles and clinical implications of the brain-gut-enteric microbiota axis (2009) · cites this paper as [17]
Cites
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170 · see citing works
Stark, P. L., & Lee, A. (1982) · Journal of Medical Microbiology · doi:10.1099/00222615-15-2-189 · Cited by 616 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
Gut/brain axis and the microbiota
Mayer, E. A., Tillisch, K., & Gupta, A. (2015) · Journal of Clinical Investigation · doi:10.1172/jci76304 · Cited by 1,503 · see citing works
Principles and clinical implications of the brain-gut-enteric microbiota axis
Rhee, S. H., Pothoulakis, C., & Mayer, E. A. (2009) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2009.35 · Cited by 1,342 · see citing works
Messaoudi, M., Lalonde, R., Violle, N., Javelot, H., Desor, D., Nejdi, A., Bisson, J.-F., Rougeot, C., Pichelin, M., Cazaubiel, M., et al. (2011) · British Journal of Nutrition · doi:10.1017/s0007114510004319 · Cited by 1,324 · 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
Bailey, M. T., Dowd, S. E., Galley, J. D., Hufnagle, A. R., Allen, R. G., & Lyte, M. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.10.023 · Cited by 1,123 · see citing works
Self-citationEffects of the probiotic Bifidobacterium infantis in the maternal separation model of depression
Desbonnet, L., Garrett, L., Clarke, G., Kiely, B., Cryan, J. F., & Dinan, T. G. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.005 · Cited by 999 · see citing works
Brain-gut-microbe communication in health and disease
Grenham, S., Clarke, G., Cryan, J. F., & Dinan, T. G. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2011.00094 · Cited by 952 · see citing works
Petra, A. I., Panagiotidou, S., Hatziagelaki, E., Stewart, J. M., Conti, P., & Theoharides, T. C. (2015) · Clinical Therapeutics · doi:10.1016/j.clinthera.2015.04.002 · Cited by 592 · see citing works
Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology
Dinan, T. G., & Cryan, J. F. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.03.007 · Cited by 577 · see citing works
Brain gut microbiome interactions and functional bowel disorders
Mayer, E. A., Savidge, T., & Shulman, R. J. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.02.037 · Cited by 496 · see citing works
Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys
Coe, C. L., Kramer, M., Czéh, B., Gould, E., Reeves, A. J., Kirschbaum, C., & Fuchs, E. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00698-x · Cited by 477 · see citing works
Self-citationGareau, M. G., Jury, J., MacQueen, G., Sherman, P. M., & Perdue, M. H. (2007) · Gut · doi:10.1136/gut.2006.117176 · Cited by 472 · see citing works
The role of the microbiome for human health: From basic science to clinical applications
Mohajeri, M. H., Brummer, R. J. M., Rastall, R. A., Weersma, R. K., Harmsen, H. J. M., Faas, M., & Eggersdorfer, M. (2018) · European Journal of Nutrition · doi:10.1007/s00394-018-1703-4 · Cited by 440 · see citing works
Maternal prenatal stress is associated with the infant intestinal microbiota
Zijlmans, M. A. C., Korpela, K., Riksen-Walraven, J. M., de Vos, W. M., & de Weerth, C. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.01.006 · Cited by 438 · see citing works
Microbiota-Gut-Brain Axis: New Therapeutic Opportunities
Long-Smith, C., O'Riordan, K. J., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2020) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010919-023628 · Cited by 419 · 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
Agorastos, A., Pervanidou, P., Chrousos, G. P., & Baker, D. G. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00118 · Cited by 385 · see citing works
“Stress-related disruption of the dynamic host-microbe interaction at these critical periods can lead to alterations of the bacterial colonization of the gut in early life and vice versa (242, 243).”
BackgroundThe gut microbiome and diet in psychiatry: focus on depression
Dash, S., Clarke, G., Berk, M., & Jacka, F. N. (2015) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000117 · Cited by 369 · see citing works
Bailey, M. T., Dowd, S. E., Parry, N. M. A., Galley, J. D., Schauer, D. B., & Lyte, M. (2010) · Infection and Immunity · doi:10.1128/iai.00862-09 · Cited by 335 · see citing works
Self-citationJašarević, E., Howerton, C. L., Howard, C. D., & Bale, T. L. (2015) · Endocrinology · doi:10.1210/en.2015-1177 · Cited by 329 · see citing works
The neuroendocrinology of the microbiota-gut-brain axis: a behavioural perspective
Cussotto, S., Sandhu, K. V., Dinan, T. G., & Cryan, J. F. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.04.002 · Cited by 326 · see citing works
Entringer, S., Buss, C., & Wadhwa, P. D. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.08.019 · Cited by 324 · see citing works
Irritable bowel syndrome: a gut microbiota-related disorder?
Bhattarai, Y., Muniz Pedrogo, D. A., & Kashyap, P. C. (2017) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00338.2016 · Cited by 294 · see citing works
Tarr, A. J., Galley, J. D., Fisher, S. E., Chichlowski, M., Berg, B. M., & Bailey, M. T. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.06.025 · Cited by 284 · see citing works
Self-citationGolubeva, A. V., Crampton, S., Desbonnet, L., Edge, D., O'Sullivan, O., Lomasney, K. W., Zhdanov, A. V., Crispie, F., Moloney, R. D., Borre, Y. E., et al. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.06.002 · Cited by 283 · see citing works
The intestinal microbiome, probiotics and prebiotics in neurogastroenterology
Saulnier, D. M., Ringel, Y., Heyman, M. B., Foster, J. A., Bercik, P., Shulman, R. J., Versalovic, J., Verdu, E. F., Dinan, T. G., Hecht, G., et al. (2013) · Gut Microbes · doi:10.4161/gmic.22973 · Cited by 248 · see citing works
Prenatal programming of postnatal plasticity?
Pluess, M., & Belsky, J. (2011) · Development and Psychopathology · doi:10.1017/s0954579410000623 · Cited by 235 · see citing works
The human gut microbiome in health: Establishment and resilience of microbiota over a lifetime
Greenhalgh, K., Meyer, K. M., Aagaard, K. M., & Wilmes, P. (2016) · Environmental Microbiology · doi:10.1111/1462-2920.13318 · Cited by 218 · see citing works
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
Self-citationMind-altering with the gut: Modulation of the gut-brain axis with probiotics
Kim, N., Yun, M., Oh, Y. J., & Choi, H.-J. (2018) · Journal of Microbiology · doi:10.1007/s12275-018-8032-4 · Cited by 210 · see citing works
Nutritionally Mediated Programming of the Developing Immune System
Palmer, A. C. (2011) · Advances in Nutrition · doi:10.3945/an.111.000570 · Cited by 198 · see citing works
Knowles, S. R., Nelson, E. A., & Palombo, E. A. (2008) · Biological Psychology · doi:10.1016/j.biopsycho.2007.09.010 · Cited by 192 · 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
Gut Microbiota: The Brain Peacekeeper
Mu, C., Yang, Y., & Zhu, W. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00345 · Cited by 188 · see citing works
Raison, C. L., Lowry, C. A., & Rook, G. A. W. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.161 · Cited by 169 · see citing works
Marques, A. H., Bjørke-Monsen, A.-L., Teixeira, A. L., & Silverman, M. N. (2015) · Brain Research · doi:10.1016/j.brainres.2014.10.051 · Cited by 166 · see citing works
Gut inflammation in chronic fatigue syndrome
Lakhan, S. E., & Kirchgessner, A. (2010) · Nutrition & Metabolism · doi:10.1186/1743-7075-7-79 · Cited by 143 · 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
Bailey, M. T., Engler, H., & Sheridan, J. F. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2005.09.008 · Cited by 133 · see citing works
Self-citationPosttraumatic stress disorder: does the gut microbiome hold the key?
Leclercq, S., Forsythe, P., & Bienenstock, J. (2016) · The Canadian Journal of Psychiatry · doi:10.1177/0706743716635535 · Cited by 121 · see citing works
Impact of stressor exposure on the interplay between commensal microbiota and host inflammation
Galley, J. D., & Bailey, M. T. (2014) · Gut Microbes · doi:10.4161/gmic.28683 · Cited by 125 · see citing works
Microbiota, immunoregulatory old friends and psychiatric disorders
Rook, G. A. W., Raison, C. L., & Lowry, C. A. (2014) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-0897-4_15 · Cited by 117 · see citing works
Hygiene and other early childhood influences on the subsequent function of the immune system
Rook, G. A. W., Lowry, C. A., & Raison, C. L. (2015) · Brain Research · doi:10.1016/j.brainres.2014.04.004 · Cited by 109 · see citing works
Ingestion of mycobacterium vaccae decreases anxiety-related behavior and improves learning in mice
Matthews, D. M., & Jenks, S. M. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2013.02.007 · Cited by 105 · see citing works
Liu, G., Chong, H.-X., Chung, F. Y.-L., Li, Y., & Liong, M.-T. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21134608 · Cited by 83 · see citing works
Mackos, A. R., Eubank, T. D., Parry, N. M. A., & Bailey, M. T. (2013) · Infection and Immunity · doi:10.1128/iai.00278-13 · Cited by 78 · see citing works
Self-citationMaslanik, T., Tannura, K., Mahaffey, L., Loughridge, A. B., Benninson, L., Ursell, L., Greenwood, B. N., Knight, R., & Fleshner, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050636 · Cited by 77 · see citing works
Flannery, J. E., Stagaman, K., Burns, A. R., Hickey, R. J., Roos, L. E., Giuliano, R. J., Fisher, P. A., & Sharpton, T. J. (2020) · mBio · doi:10.1128/mbio.02780-19 · Cited by 75 · see citing works
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 · see citing works
Ünsal, H., Balkaya, M., Ünsal, C., Bıyık, H., Başbülbül, G., & Poyrazoğlu, E. (2008) · Digestive Diseases and Sciences · doi:10.1007/s10620-007-0089-6 · Cited by 31 · see citing works
Lewis, N., Villani, A., & Lagopoulos, J. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.01.031 · Cited by 25 · see citing works
- Authors
- Bailey, M. T., Lubach, G. R., & Coe, C. L.
- Affiliations
- University of Wisconsin–Madison (US)
- Corresponding author
- Bailey, Michael T.
- Venue
- Journal of Pediatric Gastroenterology and Nutrition
- Publisher
- Wiley
- Published
- 2004-04
- Volume
- 38
- Issue
- 4
- Pages
- 414-421
- ISSN
- 0277-2116 (ISSN-L)
- OpenAlex
- W2057396462
- Cited by
- 339
- References
- 2
- Citations by year
- 2026: 3 · 2025: 18 · 2024: 11 · 2023: 19 · 2022: 17 · 2021: 13 · 2020: 20 · 2019: 29 · 2018: 29 · 2017: 23 · 2016: 22 · 2015: 22 · 2014: 24 · 2013: 17 · 2012: 12
- FWCI
- 2.02
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Pediatric Gastroenterology and Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5f31mh012458-03, AI46521)
- National Institute of Mental Health (MH 12458)
- National Institute of Allergy and Infectious Diseases (R01AI046521, AI46521)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- prenatal stress, gut microbiota, intestinal colonization, infant monkeys, Bifidobacterium, lactobacilli, Gram-negative pathogens, maternal stress, fecal microbiota
- MeSH terms
- Animals, Animals, Newborn, Bacteria, Aerobic, Bacteria, Anaerobic, Bacterial Adhesion, Bifidobacterium, Feces, Female, Hydrocortisone, Lactobacillus, Macaca mulatta, Male, Pregnancy, Stem Cells, Stress, Psychological
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