Stress and the Commensal Microbiota: Importance in Parturition and Infant Neurodevelopment

The body is colonized by an enormous array of microbes that are collectively called the microbiota. During quiescent periods, microbial communities within the gut are relatively resistant to change. However, several factors that disrupt homeostasis can also significantly change gut microbial community structure. One factor that has been shown to change the composition of the gut microbiota is exposure to psychological stressors. Studies demonstrate that the commensal microbiota are involved in stressor-induced immunomodulation, but other biological effects are not yet known. This review discusses emerging evidence that the microbiota can impact the brain and behavior and indicates that stressor-induced alterations in the composition of gut microbial communities contribute to stressor-induced behavioral changes. This review will also discuss the evidence that such effects are most evident early in life, where both stress and the microbiota have been linked to birth outcomes, such as prematurity, and neurodevelopment. When considered together, a paradigm emerges in which stressor-induced alterations in commensal microbial populations significantly impact parturition and infant neurodevelopment.

• Publication year

  2015

• Venue

  Frontiers in Psychiatry

• Publication date

  2015-02-02

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.3389/fpsyt.2015.00005PMID 25698977PMCID 4313583
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Microbiota and neurodevelopmental windows: implications for brain disorders.

  2014cited by this paper
• Neuroendocrine regulation of inflammation.

  2014cited by this paper
• Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats.

  2014cited by this paper
• The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain

  2014cited by this paper
• The Placenta Harbors a Unique Microbiome

  2014cited by this paper
• Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota

  2014cited by this paper
• A novel role for maternal stress and microbial transmission in early life programming and neurodevelopment

  2014cited by this paper
• Microbial genes, brain & behaviour – epigenetic regulation of the gut–brain axis

  2014cited by this paper
• Microbiota is essential for social development in the mouse

  2013cited by this paper
• Lack of association between maternal periodontal status and adverse pregnancy outcomes: a multicentric epidemiologic study

  2013cited by this paper
• Mom Knows Best: The Universality of Maternal Microbial Transmission

  2013cited by this paper
• The inflammasome and danger associated molecular patterns (DAMPs) are implicated in cytokine and chemokine responses following stressor exposure.

  2013cited by this paper
• Psychosocial stress in pregnancy and preterm birth: associations and mechanisms

  2013cited by this paper
• Melancholic microbes: a link between gut microbiota and depression?

  2013cited by this paper
• Stress-evoked sterile inflammation, danger associated molecular patterns (DAMPs), microbial associated molecular patterns (MAMPs) and the inflammasome

  2013cited by this paper
• The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner

  2013cited by this paper
• Pathogenic Mechanisms Linking Periodontal Diseases With Adverse Pregnancy Outcomes

  2012cited by this paper
• Effects of a high-fat diet during pregnancy and lactation are modulated by E. coli in rat offspring

  2012cited by this paper
• The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery.

  2012cited by this paper
• Long term effects of pre- and early postnatal nutrition and environment on the gut.

  2012cited by this paper
• Diversity of microbes in amniotic fluid.

  2012cited by this paper
• Commensal Bacteria and MAMPs Are Necessary for Stress-Induced Increases in IL-1β and IL-18 but Not IL-6, IL-10 or MCP-1

  2012cited by this paper
• Effect of Milk Formula Protein Content on Intestinal Barrier Function in a Porcine Model of LBW Neonates

  2011cited by this paper
• Normal gut microbiota modulates brain development and behavior

  2011cited by this paper
• Mucosal immunosuppression and epithelial barrier defects are key events in murine psychosocial stress-induced colitis.

  2011cited by this paper
• Inflammation-associated depression: from serotonin to kynurenine.

  2011cited by this paper
• Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation.

  2011cited by this paper
• In vitro measurement of the impact of human milk oligosaccharides on the faecal microbiota of weaned formula‐fed infants compared to a mixture of prebiotic fructooligosaccharides and galactooligosaccharides

  2011cited by this paper
• Effects on weight gain and gut microbiota in rats given bacterial supplements and a high-energy-dense diet from fetal life through to 6 months of age.

  2011cited by this paper
• Probiotics function mechanistically as delivery vehicles for neuroactive compounds: Microbial endocrinology in the design and use of probiotics

  2011cited by this paper
• Phenotypic and genotypic analyses of lactic acid bacteria in local fermented food, breast milk and faeces of mothers and their babies.

  2011cited by this paper
• Faculty of 1000 evaluation for Probiotics function mechanistically as delivery vehicles for neuroactive compounds: Microbial endocrinology in the design and use of probiotics.

  2011cited by this paper
• Intestinal Microbiota of 6-week-old Infants Across Europe: Geographic Influence Beyond Delivery Mode, Breast-feeding, and Antibiotics

  2010cited by this paper
• Early life programming and neurodevelopmental disorders.

  2010cited by this paper
• Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns

  2010cited by this paper
• Stressor Exposure Disrupts Commensal Microbial Populations in the Intestines and Leads to Increased Colonization by Citrobacter rodentium

  2010cited by this paper
• Mode of delivery affects the bacterial community in the newborn gut.

  2010cited by this paper
• Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life.

  2010cited by this paper
• Norepinephrine Augments Salmonella enterica-Induced Enteritis in a Manner Associated with Increased Net Replication but Independent of the Putative Adrenergic Sensor Kinases QseC and QseE

  2009cited by this paper
• Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses.

  2009cited by this paper
• Microbial manipulation of the rat dam changes bacterial colonization and alters properties of the gut in her offspring.

  2008cited by this paper
• Microbial endocrinology: how stress influences susceptibility to infection.

  2008cited by this paper
• A meta‐analysis of the association between Caesarean section and childhood asthma

  2008cited by this paper
• From inflammation to sickness and depression: when the immune system subjugates the brain

  2008cited by this paper
• Investigating the role of perceived stress on bacterial flora activity and salivary cortisol secretion: a possible mechanism underlying susceptibility to illness.

  2008cited by this paper
• Epigenetic regulation in psychiatric disorders

  2007cited by this paper
• Neonatal Maternal Separation Causes Colonic Dysfunction in Rat Pups Including Impaired Host Resistance

  2006cited by this paper
• Stress induces the translocation of cutaneous and gastrointestinal microflora to secondary lymphoid organs of C57BL/6 mice.

  2006cited by this paper
• Could peripartum antibiotics have delayed health consequences for the infant?

  2006cited by this paper
• Microbial endocrinology and infectious disease in the 21st century.

  2004cited by this paper
• Elective cesarean section vs. spontaneous delivery: a comparative study of birth experience

  2003cited by this paper
• How stress influences the immune response.

  2003cited by this paper
• Stimulation of Staphylococcus epidermidis growth and biofilm formation by catecholamine inotropes.

  2003cited by this paper
• Intrauterine infection and prematurity.

  2002cited by this paper
• Maternal periodontitis and prematurity. Part II: Maternal infection and fetal exposure.

  2001cited by this paper
• The role of infection in preterm labour and delivery.

  2001cited by this paper
• Intrauterine infection and preterm delivery.

  2000cited by this paper
• Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys.

  1999cited by this paper
• Psychological impact of emergency cesarean section in comparison with elective cesarean section, instrumental and normal vaginal delivery.

  1998cited by this paper
• Alteration of Escherichia coli O157:H7 growth and molecular fingerprint by the neuroendocrine hormone noradrenaline.

  1997cited by this paper
• Induction of gram-negative bacterial growth by neurochemical containing banana (Musa x paradisiaca) extracts.

  1997cited by this paper
• Norepinephrine induced growth and expression of virulence associated factors in enterotoxigenic and enterohemorrhagic strains of Escherichia coli.

  1997cited by this paper
• Norepinephrine-induced expression of the K99 pilus adhesin of enterotoxigenic Escherichia coli.

  1997cited by this paper
• Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma.

  1997cited by this paper
• Production of Shiga-like toxins by Escherichia coli O157:H7 can be influenced by the neuroendocrine hormone norepinephrine.

  1996cited by this paper
• Biological correlates of mental stress related to anticipated caesarean section

  1990cited by this paper
• Maternal stress response associated with caesarean delivery under general and epidural anaesthesia.

  1987cited by this paper
• Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales.

  1986cited by this paper
• Influences of Dietary and Environmental Stress on Microbial Populations in the Murine Gastrointestinal Tract

  1974cited by this paper
• PREVENTION OF ACCIDENTS

  1938cited by this paper

• Nutritional Management of Schizophrenia: Gut-Brain Axis Mechanisms and Dietary Interventions

  2026cites this paper
• Getting Over It: Maternal Stress and Gut Microbiome Manipulations Do Not Affect Rates of Offspring Habituation During Long Bouts of Stress.

  2026cites this paper
• Microbiome and Brain Development: A Tale of Two Systems

  2025cites this paper
• Maternal Stress and Maternal Microbiome Manipulations Remodel Offspring Medial Prefrontal Cortex in a Sex‐Dependent Manner

  2025cites this paper
• Pregnancy during COVID 19 pandemic associated with differential gut microbiome composition as compared to pre-pandemic

  2024cites this paper
• Gut Microbiota and Symptom Expression and Severity in Neonatal Abstinence Syndrome

  2024cites this paper
• Cesarean birth is associated with lower motor and language development scores during early childhood: a longitudinal analysis of two cohorts

  2024cites this paper
• Exploring the effect of prenatal maternal stress on the microbiomes of mothers and infants: A systematic review.

  2023cites this paper
• Maternal Vertical Microbial Transmission During Skin-to-Skin Care

  2023cites this paper
• An updated overview on the relationship between human gut microbiome dysbiosis and psychiatric and psychological disorders.

  2023cites this paper
• The effect of physical and psychological stress on the oral microbiome

  2023cites this paper
• Mitochondrial Dysfunction and mTOR in Autism Spectrum Disorders

  2023cites this paper
• Chronic Stress and Depression in Periodontitis and Peri-Implantitis: A Narrative Review on Neurobiological, Neurobehavioral and Immune–Microbiome Interplays and Clinical Management Implications

  2022cites this paper
• The social microbiome: The missing mechanism mediating the sociality-fitness nexus?

  2022cites this paper
• Maternal stress and the maternal microbiome have sex-specific effects on offspring development and aggressive behavior in Siberian hamsters (Phodopus sungorus).

  2022cites this paper
• Discrete role for maternal stress and gut microbes in shaping maternal and offspring immunity

  2022cites this paper
• Cortisol Promotes Surface Translocation of Porphyromonas gingivalis

  2022cites this paper
• Immune System Alterations and Postpartum Mental Illness: Evidence From Basic and Clinical Research

  2022cites this paper
• Role of Brain-Gut-Microbiota Axis in Depression: Emerging Therapeutic Avenues.

  2022cites this paper
• Neurobiological, Behavioral, and Immune–Microbiome Interactions of Chronic Stress and Depression in Periodontitis and Peri-Implantitis: A Narrative Review with Clinical Management Insights

  2022cites this paper
• The Oral-Microbiome-Brain Axis and Neuropsychiatric Disorders: An Anthropological Perspective

  2022cites this paper
• Breastfeeding, maternal psychopathological symptoms, and infant problem behaviors among low-income mothers returning to work.

  2021cites this paper
• Fundamental Clock of Biological Aging: Convergence of Molecular, Neurodegenerative, Cognitive and Psychiatric Pathways: Non-Equilibrium Thermodynamics Meet Psychology

  2021cites this paper
• Fundamental Clock of Biological Aging: Convergence of Molecular, Neurodegenerative, Cognitive, and Psychiatric Pathways

  2021cites this paper
• Effect of the Intake of a Traditional Mexican Beverage Fermented with Lactic Acid Bacteria on Academic Stress in Medical Students

  2021cites this paper
• Unique maternal immune and functional microbial profiles during prenatal stress

  2020cites this paper
• Gut microbiome mediated epigenetic regulation of brain disorder and application of machine learning for multi-omics data analysis.

  2020cites this paper
• Microbes and the womb: does it matter?

  2020cites this paper
• The gut microbiota may be a novel pathogenic mechanism in loosening of orthopedic implants in rats

  2020cites this paper
• Gutted! Unraveling the Role of the Microbiome in Major Depressive Disorder.

  2020cites this paper
• Oral microbiome composition, but not diversity, is associated with adolescent anxiety and depression symptoms.

  2020cites this paper
• Integrative Review of Gut Microbiota and Expression of Symptoms Associated with Neonatal Abstinence Syndrome.

  2020cites this paper
• Prenatal stress causes intrauterine inflammation and serotonergic dysfunction, and long-term behavioral deficits through microbe- and CCL2-dependent mechanisms

  2020cites this paper
• INTERACTION OF THE SYMBIOTIC MICROBIOTA OF THE GASTRO-INTESTINAL TRACT WITH THE NERVOUS SYSTEM OF THE HOST ORGANISM

  2019cites this paper
• Prenatal stress disrupts social behavior, cortical neurobiology and commensal microbes in adult male offspring

  2019cites this paper
• Stress and the gut microbiota-brain axis

  2019cites this paper
• Microbiota of newborn meconium is associated with maternal anxiety experienced during pregnancy.

  2019cites this paper
• Early-life stress, microbiota, and brain development: probiotics reverse the effects of maternal separation on neural circuits underpinning fear expression and extinction in infant rats

  2019cites this paper
• The “ Healthy ” Microbiome

  2019cites this paper
• The Microbiota-Gut-Brain Axis.

  2019cites this paper
• Microbiome and Mental Health, Specifically as It Relates to Adolescents

  2019cites this paper
• The role of the brain–gut–microbiota axis in psychology: The importance of considering gut microbiota in the development, perpetuation, and treatment of psychological disorders

  2019cites this paper
• The effect of the stress hormone cortisol on the metatranscriptome of the oral microbiome

  2018cites this paper
• Evolution of the nasopharyngeal bacterial microbiota of beef calves from spring processing to 40 days after feedlot arrival.

  2018cites this paper
• The Role and Influence of the Mother in the Development of the Fetus: Comparative Study of Qur’an, Hadiths, and Modern Medical Perspectives

  2018cites this paper
• Making Sense of … the Microbiome in Psychiatry

  2018cites this paper
• Gut-Brain Psychology: Rethinking Psychology From the Microbiota–Gut–Brain Axis

  2018influential citation
• Recognizing Depression from the Microbiota–Gut–Brain Axis

  2018cites this paper
• Impacts of Early Life Adversity on Microbiota and Immune Functioning in Individuals with Major Depressive Disorder

  2018cites this paper
• Dysbiosis of Oral Microflora: A Review

  2018cites this paper
• Relationships Among Airborne Microbial Communities, Urban Land Uses and Vegetation Cover: Implications for Urban Planning and Human Health

  2018cites this paper
• Resilience priming: Translational models for understanding resiliency and adaptation to early life adversity

  2018cites this paper
• The skin microbiome: impact of modern environments on skin ecology, barrier integrity, and systemic immune programming

  2017cites this paper
• Prenatal stress affects placental cytokines and neurotrophins, commensal microbes, and anxiety-like behavior in adult female offspring.

  2017cites this paper
• Childhood body mass is positively associated with cesarean birth in Yucatec Maya subsistence farmers

  2017cites this paper
• Gut microbiota, epigenetic modification and colorectal cancer

  2017cites this paper
• Toward a Biopsychosocial Ecology of the Human Microbiome, Brain-Gut Axis, and Health

  2017influential citation
• Effects of Stress on Commensal Microbes and Immune System Activity.

  2016cites this paper
• Probiotic supplementation can positively affect anxiety and depressive symptoms: a systematic review of randomized controlled trials.

  2016cites this paper
• Cultural Epigenetics

  2016influential citation
• Role of the Intestinal Microbiota in Host Responses to Stressor Exposure.

  2016cites this paper
• Therapy-induced microenvironmental changes in cancer

  2016cites this paper
• The Effect of Probiotic Supplementation on Self-Reported Sleep Quality

  2016cites this paper
• Argon as a potential strategy against the neurotoxicity of nitrous oxide and perinatal hypoxia/ischemia induced brain injury

  2016cites this paper
• Cultural epigenetics: Cultural epigenetics

  2016cites this paper
• The Role of the Microbial Metabolites Including Tryptophan Catabolites and Short Chain Fatty Acids in the Pathophysiology of Immune-Inflammatory and Neuroimmune Disease

  2016cites this paper
• Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health

  2016cites this paper
• Gut-Microbiota-Brain Axis and Its Effect on Neuropsychiatric Disorders With Suspected Immune Dysregulation.

  2015cites this paper
• STUDY OF ORAL MICROBIOTA IN OLDER PEOPLE OF VALENCIA AND ITS RELATION TO AGE, A COGNITIVE IMPARIMENT AND DIET

  2015cites this paper
• The neurotoxic effects of ampicillin-associated gut bacterial imbalances compared to those of orally administered propionic acid in the etiology of persistent autistic features in rat pups: effects of various dietary regimens

  2015cites this paper
• Alterations in the Vaginal Microbiome by Maternal Stress Are Associated With Metabolic Reprogramming of the Offspring Gut and Brain.

  2015cites this paper
• Prenatal stress-induced alterations in major physiological systems correlate with gut microbiota composition in adulthood.

  2015cites this paper
• A Vagina Monologue: Mom's Stress, Bugs, and Baby's Brain.

  2015cites this paper
• C H A P T E R 1 1 Stress in Pregnancy Impacts on Mother and Child

  year unknowncites this paper