The DOI matches its Crossref record; 105 of the 106 references it cites were found in a registry or an index.
Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats
Abstract
Disruption of bacterial colonization during the early postnatal period is increasingly being linked to adverse health outcomes. Indeed, there is a growing appreciation that the gut microbiota plays a role in neurodevelopment. However, there is a paucity of information on the consequences of early-life manipulations of the gut microbiota on behavior. To this end we administered an antibiotic (vancomycin) from postnatal days 4-13 to male rat pups and assessed behavioral and physiological measures across all aspects of the brain-gut axis. In addition, we sought to confirm and expand the effects of early-life antibiotic treatment using a different antibiotic strategy (a cocktail of pimaricin, bacitracin, neomycin; orally) during the same time period in both female and male rat pups. Vancomycin significantly altered the microbiota, which was restored to control levels by 8 weeks of age. Notably, vancomycin-treated animals displayed visceral hypersensitivity in adulthood without any significant effect on anxiety responses as assessed in the elevated plus maze or open field tests. Moreover, cognitive performance in the Morris water maze was not affected by early-life dysbiosis. Immune and stress-related physiological responses were equally unaffected. The early-life antibiotic-induced visceral hypersensitivity was also observed in male rats given the antibiotic cocktail. Both treatments did not alter visceral pain perception in female rats. Changes in visceral pain perception in males were paralleled by distinct decreases in the transient receptor potential cation channel subfamily V member 1, the α-2A adrenergic receptor and cholecystokinin B receptor. In conclusion, a temporary disruption of the gut microbiota in early-life results in very specific and long-lasting changes in visceral sensitivity in male rats, a hallmark of stress-related functional disorders of the brain-gut axis such as irritable bowel disorder.
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“Fourthly, preclinical studies with antibiotic administration, either in early life (O'Mahony et al., 2014) or adulthood (Verdu et al., 2008), have shown long-lasting effects on brain, spinal cord, and the ENS.”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as O'Mahony et al., 2014
In the citing paper
“While chronic antibiotic treatment impaired spatial memory in the Morris Water Maze in adult rats (Hoban et al., 2016a;Wang et al., 2015) acute treatments did not affect this type of memory when administered in early life in rats (O'Mahony et al., 2014), nor when administered during adulthood in mice and tested in the Barnes maze (Frohlich et al., 2016).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as O'Mahony et al., 2014
In the citing paper
“Disruption of the gut microbiota in early-life also has been associated with longterm changes in visceral sensitivity, emphasizing the importance of the gut microbiome in neurodevelopment of pain pathways68.”
From The gut Microbiome in adult and pediatric functional gastrointestinal disorders (2019) · cites this paper as [68]
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“Below, we will discuss how each pathway suggests a link between the”
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“Studies in germ-free mice and antibiotic-treated animals suggested that the gut microbiota may play a role in pain perception (Luczynski et al., 2017; O’Mahony et al., 2014; Verdu et al., 2006).”
BackgroundImpact of prebiotics on metabolic and behavioral alterations in a mouse model of metabolic syndrome
de Cossío, L. F., Fourrier, C., Sauvant, J., Everard, A., Capuron, L., Cani, P. D., Layé, S., & Castanon, N. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.12.022 · Cited by 108
Gutsy Moves: The Amygdala as a Critical Node in Microbiota to Brain Signaling
Cowan, C. S. M., Hoban, A. E., Ventura‐Silva, A. P., Dinan, T. G., Clarke, G. A., & Cryan, J. F. (2017) · BioEssays · doi:10.1002/bies.201700172 · Cited by 110
Self-citationEarly exposure to antibiotic drugs and risk for psychiatric disorders: a population-based study
Lavebratt, C., Yang, L. L., Giacobini, M., Forsell, Y., Schalling, M., Partonen, T., & Gissler, M. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0653-9 · Cited by 107
Visceral pain: gut microbiota, a new hope?
Pusceddu, M. M., & Gareau, M. G. (2018) · Journal of Biomedical Science · doi:10.1186/s12929-018-0476-7 · Cited by 101
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
“Several studies in germ-free rats have shown that the absence of gut microbiota leads to stress and anxiety (Crumeyrolle-Arias et al., 2014; O'Mahony et al., 2014).”
BackgroundResultThe gut microbiota as a key regulator of visceral pain
O’Mahony, S. M., Dinan, T. G., & Cryan, J. F. (2016) · Pain · doi:10.1097/j.pain.0000000000000779 · Cited by 104
Self-citationNeufeld, K. M., O’Mahony, S. M., Hoban, A. E., Waworuntu, R. V., Berg, B. M., Dinan, T. G., & Cryan, J. F. (2017) · Nutritional Neuroscience · doi:10.1080/1028415x.2017.1397875 · Cited by 98
Self-citationMicrobiome: Bacterial broadband
Eisenstein, M. (2016) · Nature · doi:10.1038/533s104a · Cited by 95
Gut Microbiota: A Modulator of Brain Plasticity and Cognitive Function in Ageing
Leung, K., & Thuret, S. (2015) · Healthcare · doi:10.3390/healthcare3040898 · Cited by 94
“Increasing insights into the role of the gut-brain axis on cognitive function in humans and animals with inflammatory bowel disease and IBS is further evidence of this influence [37].”
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 97
Self-citationMeynier, M., Baudu, E., Rolhion, N., Defaye, M., Straube, M., Daugey, V., Modoux, M., Wawrzyniak, I., Delbac, F., Villéger, R., et al. (2022) · Gut Microbes · doi:10.1080/19490976.2021.2022997 · Cited by 90
The Microbiota–Gut–Brain Axis and Neurological Disorders: A Comprehensive Review
Nakhal, M. M., Yassin, L. K., Alyaqoubi, R., Saeed, S., Alderei, A., Alhammadi, A., Alshehhi, M., Almehairbi, A., Houqani, S. A., BaniYas, S., et al. (2024) · Life · doi:10.3390/life14101234 · Cited by 136
Alcohol, microbiome, and their effect on psychiatric disorders
Hillemacher, T., Bachmann, O. P., Kahl, K. G., & Frieling, H. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.04.015 · Cited by 90
“, 2015) anxiety disorders,(Lurie et al., 2015; Foster and McVey Neufeld, 2013; Luna and Foster, 2015; O'Mahony et al., 2014) schizophrenia,(Nemani et al.”
Morshedi, M., Saghafi‐Asl, M., & Hosseinifard, E.-S. (2020) · Journal of Translational Medicine · doi:10.1186/s12967-019-02169-y · Cited by 81
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 82
Chronic Visceral Pain: New Peripheral Mechanistic Insights and Resulting Treatments
Ford, A. C., Vanner, S. J., Kashyap, P., & Nasser, Y. (2024) · Gastroenterology · doi:10.1053/j.gastro.2024.01.045 · Cited by 87
O’Mahony, S. M., Neufeld, K. M., Waworuntu, R. V., Pusceddu, M. M., Manurung, S., Murphy, K., Strain, C., Laguna, M. C., Peterson, V. L., Stanton, C., et al. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14514 · Cited by 82
“While MS is just one model of early‐life adversity, other studies have shown that other stressors including early‐life antibiotics (O'Mahony et al., 2014), neonatal colonic inflammation (Al‐Chaer, Kawasaki, & Pasricha, 2000) and repeated neonatal colorectal distension (Lin & Al‐Chaer, 2003) during this early stage of…”
BackgroundMethodInfluentialSelf-citationPaneth cell defects induce microbiota dysbiosis in mice and promote visceral hypersensitivity
Riba, A., Olier, M., Lacroix-Lamandé, S., Lencina, C., Bacquié, V., Harkat, C., Gillet, M., Baron, M., Sommer, C., Mallet, V., et al. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.08.044 · Cited by 78
Maltz, R. M., Keirsey, J. K., Kim, S. C., Mackos, A. R., Gharaibeh, R. Z., Moore, C. C., Xu, J., Somogyi, Á., & Bailey, M. T. (2018) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000002226 · Cited by 81
Microbiota: a novel regulator of pain
Defaye, M., Gervason, S., Altier, C., Berthon, J., Ardid, D., Filaire, E., & Carvalho, F. A. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02083-z · Cited by 81
Pusceddu, M. M., Kelly, P. M., Ariffin, N., Cryan, J. F., Clarke, G. A., & Dinan, T. G. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.04.015 · Cited by 79
Self-citationIrritable Bowel Syndrome and Stress-Related Psychiatric Co-morbidities: Focus on Early Life Stress
O’Mahony, S. M., Clarke, G. A., Dinan, T. G., & Cryan, J. F. (2017) · Handbook of experimental pharmacology · doi:10.1007/164_2016_128 · Cited by 82
Self-citationMicrobiome in brain function and mental health
Kennedy, P. J., Murphy, A., Cryan, J. F., Ross, R. P., Dinan, T. G., & Stanton, C. (2016) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2016.05.001 · Cited by 81
“It is noteworthy that in rodents, perturbing the gut microbiota with antibiotic treatment in early life can induce visceral hypersensitivity (O'Mahony et al., 2014), whilst probiotic strains such as Bifidobacteria infantis 35624 can alleviate hypersensitivity (McKernan, Fitzgerald, Dinan, & Cryan, 2010).”
BackgroundSelf-citationMicrobiota 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 74
Self-citationAntibiotics and the nervous system: More than just the microbes?
Champagne-Jorgensen, K., Kunze, W. A., Forsythe, P., Bienenstock, J., & McVey Neufeld, K.-A. (2019) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.12.014 · Cited by 92
Stress and the Commensal Microbiota: Importance in Parturition and Infant Neurodevelopment
Gur, T., Worly, B. L., & Bailey, M. T. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00005 · Cited by 69
Luk, B., Horvath, T. D., Engevik, K. A., Ruan, W. H., Haidacher, S. J., Hoch, K. M., Oezguen, N., Spinler, J. K., Haag, A. M., Versalovic, J. A., et al. (2021) · Biomolecules · doi:10.3390/biom11081091 · Cited by 67
Microbiome to Brain: Unravelling the Multidirectional Axes of Communication
Aidy, S. E., Stilling, R. M., Dinan, T. G., & Cryan, J. F. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-20215-0_15 · Cited by 65
“…as an early-life stressor in rats it was demonstrated that postnatal adversity, next to its effects on anxiety-and depressive-like behaviours, changes the composition the intestinal microbiota and induces visceral hypersensitivity later in life (O’Mahony et al. 2009 , 2014 ; Hyland et al. 2015 ).”
BackgroundSelf-citationKentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64
“In rodents, early life maternal separation disrupts the offspring's microbiota (O'Mahony et al., 2009).”
Self-citationColitis-Induced Microbial Perturbation Promotes Postinflammatory Visceral Hypersensitivity
Esquerre, N., Basso, L., Defaye, M., Vicentini, F., Cluny, N. L., Bihan, D. G., Hirota, S. A., Schick, A., Jijon, H. B., Lewis, I. A., et al. (2020) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2020.04.003 · Cited by 67
“In a study where neonatal mice were treated with 10 days of Abx, animals developed persistent visceral pain at 10 weeks of age.(60) Interestingly, this was associated with decreased TRPV1 expression in the lumbosacral spinal cord; no evidence of inflammation was seen.”
BackgroundVisceral Pain and Gastrointestinal Microbiome
Chichlowski, M., & Rudolph, C. (2015) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm15025 · Cited by 66
“Disruption of the microbiome during early life by administration of vancomycin for postnatal day 4-13 led to visceral hypersensitivity to colorectal distension in the adult rats, even though the dysbiosis had resolved.(57) Interestingly, vancomycin treatment did not impact cognitive or anxiety-related behaviors, growt…”
Wheezing and infantile colic are associated with neonatal antibiotic treatment
Oosterloo, B. C., van Elburg, R. M., Rutten, N. B. M. M., Bunkers, C. M., Crijns, C. E., Meijssen, C. B., Oudshoorn, J. H., Rijkers, G. T., van der Ent, C. K., & Vlieger, A. M. (2018) · Pediatric Allergy and Immunology · doi:10.1111/pai.12857 · Cited by 62
How poverty affects diet to shape the microbiota and chronic disease
Harrison, C. A., & TAREN, D. L. (2017) · Nature reviews. Immunology · doi:10.1038/nri.2017.121 · Cited by 65
From Dysbiosis to Neurodegenerative Diseases through Different Communication Pathways: An Overview
Intili, G., Paladino, L., Rappa, F., Alberti, G., Plicato, A., Calabrò, F., Fucarino, A., Cappello, F., Bucchieri, F., Tomasello, G., et al. (2023) · Biology · doi:10.3390/biology12020195 · Cited by 66
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
“Moreover, we have recently shown that a temporary disruption of the gut microbiota in rat pups following earlylife antibiotic administration results in very specific and long-lasting changes in visceral sensitivity in male rats (S. O'Mahony et al. 2014).”
Self-citationWang, P., Tu, K., Cao, P., Yang, Y., Zhang, H., Qiu, X.-T., Zhang, M., Wu, X., Yang, H., & Chen, T. (2021) · Molecular Brain · doi:10.1186/s13041-021-00759-w · Cited by 60
Exploring the microbiota-gut-brain axis: impact on brain structure and function
Yassin, L. K., Nakhal, M. M., Alderei, A., Almehairbi, A., Mydeen, A. B., Akour, A. A., & Hamad, M. I. K. (2025) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2025.1504065 · Cited by 64
Metadata
- Authors
- O’Mahony, S. M., Felice, V. D., Nally, K., Savignac, H. M., Claesson, M. J., Scully, P., Woznicki, J., Hyland, N. P., Shanahan, F., Quigley, E. M., Marchesi, J. R., O’Toole, P. W., Dinan, T. G., & Cryan, J. F.
- Affiliations
- University College Cork (IE)
- ORCID
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2014-09
- Volume
- 277
- Pages
- 885-901
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2055122111
- Cited by
- 272
- References
- 106
- Citations by year
- 2026: 7 · 2025: 13 · 2024: 24 · 2023: 15 · 2022: 18 · 2021: 42 · 2020: 24 · 2019: 26 · 2018: 23 · 2017: 25 · 2016: 34 · 2015: 16 · 2014: 5
- FWCI
- 10.93
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Funders
- Science Foundation Ireland (02/CE/B124, 07/CE/B1368)
- GlaxoSmithKline
- European Community’s Seventh Framework Programme (FP7/2007-2013)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Medicine › Physiology (medical) › Pain Mechanisms and Treatments
- Keywords
- gut microbiota, early-life antibiotic exposure, vancomycin, visceral hypersensitivity, visceral pain, gut-brain axis, brain development, anxiety-like behavior, cognitive performance, sex differences, TRPV1, alpha2A-adrenergic receptor, cholecystokinin B receptor, irritable bowel syndrome
- MeSH terms
- Animals, Animals, Newborn, Anti-Bacterial Agents, Anxiety, Bacitracin, Behavior, Animal, Cognition, Female, Hyperalgesia, Male, Neomycin, Natamycin, Vancomycin, Rats, Sprague-Dawley, Gastrointestinal Tract, Visceral Pain, Microbiota
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