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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“Additionally, gut microbial dysbiosis has been implicated in various pain conditions, such as inflammatory pain [14], visceral pain [15] and neuropathic pain [16].”
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“Moreover, neonatal antibiotic treatment (vancomycin) affected visceral pain in adulthood, but did not impact cognitive or anxiety-related behaviors in male rats (O’Mahony et al., 2014).”
BackgroundThe gut microbiome and the brain
Rykalo, N. A., Riehl, L., & Kress, M. (2024) · Current Opinion in Supportive and Palliative Care · doi:10.1097/spc.0000000000000717 · Cited by 16
“The gut microbiome is disturbed by pharmacothera-pies such as frequently given antibiotics which, when given in early life, not only cause mental disorders but also visceral pain hypersensitivity in later life [86].”
Inflammasome Signaling Regulates the Microbial–Neuroimmune Axis and Visceral Pain in Mice
Aguilera, M., Rossini, V., Hickey, A., Simnica, D., Grady, F., Felice, V. D., Moloney, A., Pawley, L. C., Fanning, A., McCarthy, L., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158336 · Cited by 13
Self-citationIs Gut Dysbiosis an Epicenter of Parkinson’s Disease?
Rajput, C., Sarkar, A., Sachan, N., Rawat, N., & Singh, M. P. (2021) · Neurochemical Research · doi:10.1007/s11064-020-03187-9 · Cited by 13
Health benefits conferred by the human gut microbiota during infancy
Ventura, M., Milani, C., Lugli, G. A., & van Sinderen, D. (2018) · Microbial Biotechnology · doi:10.1111/1751-7915.13334 · Cited by 12
Gut Microbiota: A Modulator and Therapeutic Target for Chronic Pain
Lou, L., Zhou, L., & Wang, Y. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04663-x · Cited by 13
“In addition, it was found that early treatment with vancomycin could significantly change the fecal microbiota in rats, leading to the increase of Proteobacteria, Tengut, and Bacteroides, while the Firmicutes and Actinobacteria were decreased, resulting in the visceral sensitivity [36].”
Antibiotics-induced dysbiosis impacts dendritic morphology of adult mouse cortical interneurons
Nakhal, M. M., Mydeen, A. B., Yassin, L. K., Almazrouei, R., Alkamali, R., Alsulaimi, M., Elsaleh, R. I., BaniYas, S., Houqani, S. A., Al-Marzooq, F. I., et al. (2025) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2025.1557961 · Cited by 12
Microbiota in Functional Gastrointestinal Disorders in Infancy: Implications for Management
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Pain Bugs: Gut Microbiota and Pain Disorders
Rea, K., O’Mahony, S. M., Dinan, T. G., & Cryan, J. F. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.10.001 · Cited by 12
Self-citationDegree of lipid saturation affects depressive-like behaviour and gut microbiota in mice
Lee, H.-C., Lo, Y.-C., Yu, S.-C., Tung, T.-H., Lin, I., & Huang, S. (2019) · International Journal of Food Sciences and Nutrition · doi:10.1080/09637486.2019.1681380 · Cited by 12
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The role of probiotics in nutritional health: probiotics as nutribiotics
Chávarri, M., Diez-Gutiérrez, L., Marañón, I., Villarán, M. C., & Barrón, L. J. R. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-823733-5.00018-0 · Cited by 11
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Self-citationImportance of the Microbiota in Early Life and Influence on Future Health
Verdu, E. F., Hayes, C. L., & O’Mahony, S. M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802304-4.00009-8 · Cited by 10
Self-citationHigh and Mighty? Cannabinoids and the microbiome in pain
Rea, K., O’Mahony, S. M., & Cryan, J. F. (2021) · Neurobiology of Pain · doi:10.1016/j.ynpai.2021.100061 · Cited by 9
Self-citationTiwari, N., & Qiao, L. Y. (2024) · Cells · doi:10.3390/cells13100834 · Cited by 8
“The discrepancy of sex-differential outcomes in visceral pain affected by microbiota may lie in the spectrum of antibiotics used in experiments [68] and/or diverse metabolomic responses [24].”
BackgroundKambe, J., Usuda, K., Inoüe, R., Hirayama, K., Ito, M., Suenaga, K., Masukado, S., Liu, H., Miyata, S., Li, C., et al. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2359729 · Cited by 8
“53 Antibiotic administration only infantile period (P4–P13) has not been reported to impair spatial memory learning in the Morris water maze test, 54 possibly because of the maternal effect such as maternal microbiome and breast milk preserve infant microbiome formation from antibiotics disturbance.”
Abdullah, N. S., Bradaïa, A., Defaye, M., Ohland, C., Svendsen, K., Dickemann, A., Cuménal, M., Hassan, A., Iftinca, M., McCoy, K. D., et al. (2024) · Mucosal Immunology · doi:10.1016/j.mucimm.2024.12.002 · Cited by 8
Microbiome contributions to pain: a review of the preclinical literature
Pratt, M. L., Plumb, A. N., Manjrekar, A., Cardona, L. M., Chan, C. K., John, J. M., & Sadler, K. E. (2024) · Pain · doi:10.1097/j.pain.0000000000003376 · Cited by 9
Hull, R., Lolas, G., Makrogkikas, S., Jensen, L. D., Syrigos, K. N., Evangelou, G., Padayachy, L. C., Egbor, C., Mehrotra, R., Makhafola, T. J., et al. (2021) · Microorganisms · doi:10.3390/microorganisms9102129 · Cited by 8
“Antibiotic treatment, influences the heterogeneity of microbiota, altering the ac iv ty of the enteric nervous system and the bra n [39].”
BackgroundENVOLVIMENTO DA FLORA INTESTINAL NA MODULAÇÃO DE DOENÇAS PSIQUIÁTRICAS
Lach, G., Morais, L. H., Costa, A. P., & Hoeller, A. A. (2017) · VITTALLE - Revista de Ciências da Saúde · doi:10.14295/vittalle.v29i1.6413 · Cited by 12
The role of gut microbiota in neuropathic pain: insights into immune mechanisms
Gong, Z., Zou, J., Fang, Y., Li, J., Luo, Y., Xue, Q., Yu, B., Hua, B., & Liu, Z. (2025) · The Journal of Headache and Pain · doi:10.1186/s10194-025-02260-4 · Cited by 10
“Importantly, these alterations in nociceptive pathways are long-lasting and resistant to antibiotic treatment [42].”
Kouraki, A., Franks, S. J., Vijay, A., Kurien, T., Taylor, M. A., Smith, S. L., Smith, B. E., Kelly, T., & Valdes, A. M. (2026) · Nutrients · doi:10.3390/nu18050714 · Cited by 6
“In animal models, restoring gut microflora reduced neuropathic-like and visceral pain, as well as pain sensitisation, independent of cognitive or anxiety-like behaviours [7,35].”
Payne, E., Harrington, K., Richard, P., Brackin, R., Davis, R., Couture, S. A., Liff, J., Asmus, F., Mutina, E., Fisher, A., et al. (2021) · Journal of Pain · doi:10.1016/j.jpain.2021.05.003 · Cited by 6
Perinatal Penicillin Exposure Affects Cortical Development and Sensory Processing
Perna, J., Lu, J., Mullen, B. R., Liu, T., Tjia, M., Weiser, S. C., Ackman, J. B., & Zuo, Y. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.704219 · Cited by 7
González‐Arancibia, C., Collio, V., Silva-Olivares, F., Montaña-Collao, P., Martínez-Pinto, J., Julio‐Pieper, M., Sotomayor‐Zárate, R., & Bravo, J. A. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.837652 · Cited by 6
“Early-life exposure to broad-range non-absorbable antibiotics has been previously shown to decrease diversity and richness of gut microbiota in adult rodents (Clarke et al., 2014; O’Mahony et al., 2014), suggesting that perinatal exposure to antibiotics alters gut microbiota composition in adulthood.”
BackgroundStress and the Gastrointestinal System
Bonaz, B. L. (2016) · Springer eBooks · doi:10.1007/978-3-319-28609-9_7 · Cited by 6
Probiotics as Curators of a Healthy Gut Microbiota
Murphy, A., Dinan, T. G., Cryan, J. F., Stanton, C., & Ross, R. P. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802304-4.00005-0 · Cited by 6
Self-citation
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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