Low-Dose Penicillin in Early Life Induces Long-Term Changes in Murine Gut Microbiota, Brain Cytokines and Behavior

Leclercq, Sophie; Mian, Firoz M.; Stanisz, Andrew M.; Bindels, Laure B.; Cambier, Emmanuel; Ben-Amram, Hila; Koren, Omry; Forsythe, Paul; Bienenstock, John

doi:10.1038/ncomms15062

Cited by 435Gut microbiota and healthTryptophan and brain disordersProbiotics and Fermented Foods

Low-Dose Penicillin in Early Life Induces Long-Term Changes in Murine Gut Microbiota, Brain Cytokines and Behavior

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Leclercq, Sophie, Mian, Firoz M., Stanisz, Andrew M., Bindels, Laure B., Cambier, Emmanuel, Ben-Amram, Hila, Koren, Omry, Forsythe, Paul +1 more·2017·Nature Communications

DOI 10.1038/ncomms15062PMC PMC5382287

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Abstract

There is increasing concern about potential long-term effects of antibiotics on children's health. Epidemiological studies have revealed that early-life antibiotic exposure can increase the risk of developing immune and metabolic diseases, and rodent studies have shown that administration of high doses of antibiotics has long-term effects on brain neurochemistry and behaviour. Here we investigate whether low-dose penicillin in late pregnancy and early postnatal life induces long-term effects in the offspring of mice. We find that penicillin has lasting effects in both sexes on gut microbiota, increases cytokine expression in frontal cortex, modifies blood-brain barrier integrity and alters behaviour. The antibiotic-treated mice exhibit impaired anxiety-like and social behaviours, and display aggression. Concurrent supplementation with Lactobacillus rhamnosus JB-1 prevents some of these alterations. These results warrant further studies on the potential role of early-life antibiotic use in the development of neuropsychiatric disorders, and the possible attenuation of these by beneficial bacteria.

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Strong preclinical evidence indicates that early-life disruption of the microbiota alters a wide range of behavioral and neural outcomes both during development and later in life.
“Such investigations are becoming more widespread based on strong preclinical evidence that early-life disruption of the microbiota alters a wide range of behavioral and neural outcomes both during development and later in life (Clarke et al., 2013;Diaz Heijtz et al., 2011;Leclercq et al., 2017;Minter et al., 2017;O'Mahony et al., 2014;Olszak et al., 2012;Stilling et al., 2015).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Leclercq et al., 2017
The Abstract and Discussion report that perinatal penicillin exposure in mice was followed by lasting changes in brain cytokines, blood–brain barrier integrity, and several behaviors. The paper supports the later-life portion of the claim, but the cited passages do not report behavioral or neural outcomes measured during development. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Mice with gut microbiota depleted by antibiotics show disorders in social behavior.
“Some studies show that mice with gut microbiota depleted by antibiotics also show disorders in social behavior [109,110].”
From Unraveling the Connections: Eating Issues, Microbiome, and Gastrointestinal Symptoms in Autism Spectrum Disorder (2025) · cites this paper as [109]

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Synergistic Interactions between Cytokines and AVP at the Blood-CSF Barrier Result in Increased Chemokine Production and Augmented Influx of Leukocytes after Brain Injury
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The Impact of Prulifloxacin on Vaginal Lactobacillus Microflora: AnIn VivoStudy
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The Microbiota-Gut-Brain Axis
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
The gut microbiota–brain axis in behaviour and brain disorders
Morais, L. H., Schreiber, H. L., & Mazmanian, S. K. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-020-00460-0 · Cited by 2,149 · see citing works
The gut microbiome in neurological disorders
Cryan, J. F., O'Riordan, K. J., Sandhu, K., Peterson, V., & Dinan, T. G. (2020) · The Lancet Neurology · doi:10.1016/s1474-4422(19)30356-4 · Cited by 1,336 · see citing works
Negative association of antibiotics on clinical activity of immune checkpoint inhibitors in patients with advanced renal cell and non-small-cell lung cancer
Derosa, L., Hellmann, M. D., Spaziano, M., Halpenny, D., Fidelle, M., Rizvi, H., Long, N., Plodkowski, A. J., Arbour, K. C., Chaft, J. E., et al. (2018) · Annals of Oncology · doi:10.1093/annonc/mdy103 · Cited by 908 · see citing works
Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder
Sgritta, M., Dooling, S. W., Buffington, S. A., Momin, E. N., Francis, M. B., Britton, R. A., & Costa-Mattioli, M. (2019) · Neuron · doi:10.1016/j.neuron.2018.11.018 · Cited by 865 · see citing works
The blood-brain barrier in aging and neurodegeneration
Knox, E. G., Aburto, M. R., Clarke, G., Cryan, J. F., & O’Driscoll, C. M. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01511-z · Cited by 738 · see citing works
“In another study mice treated with low-dose penicillin in early life, however, have increased mRNA and protein expression of tight junction proteins in the hippocampus [149].”
Impact of microbiota on central nervous system and neurological diseases: the gut-brain axis
Ma, Q., Xing, C., Long, W., Wang, H. Y., Liu, Q., & Wang, R. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1434-3 · Cited by 752 · see citing works
Dysbiosis of gut microbiota and microbial metabolites in Parkinson's disease
Sun, M.-F., & Shen, Y.-Q. (2018) · Ageing Research Reviews · doi:10.1016/j.arr.2018.04.004 · Cited by 445 · see citing works
Mechanisms of Blood–Brain Barrier Protection by Microbiota-Derived Short-Chain Fatty Acids
Fock, E. M., & Parnova, R. G. (2023) · Cells · doi:10.3390/cells12040657 · Cited by 418 · see citing works
Maternal Polystyrene Microplastic Exposure during Gestation and Lactation Altered Metabolic Homeostasis in the Dams and Their F1 and F2 Offspring
Luo, T., Wang, C., Pan, Z., Jin, C., Fu, Z., & Jin, Y. (2019) · Environmental Science & Technology · doi:10.1021/acs.est.9b03191 · Cited by 388 · see citing works
Gut microbial molecules in behavioural and neurodegenerative conditions
Needham, B. D., Kaddurah-Daouk, R., & Mazmanian, S. K. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-00381-0 · Cited by 379 · see citing works
Intestinal Lactobacillus in health and disease, a driver or just along for the ride?
Heeney, D. D., Gareau, M. G., & Marco, M. L. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2017.08.004 · Cited by 367 · see citing works
Gastrointestinal and brain barriers: unlocking gates of communication across the microbiota–gut–brain axis
Aburto, M. R., & Cryan, J. F. (2024) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-023-00890-0 · Cited by 391 · see citing works
Management of Infants at Risk for Group B Streptococcal Disease
Puopolo, K. M., Lynfield, R., Cummings, J. J., Hand, I. L., Adams-Chapman, I. S., Poindexter, B. B., Stewart, D. L., Aucott, S. W., Goldsmith, J. P., Mowitz, M. E., et al. (2019) · PEDIATRICS · doi:10.1542/peds.2019-1881 · Cited by 318 · see citing works
The role of the gut microbiota in development, function and disorders of the central nervous system and the enteric nervous system
Heiss, C. N., & Olofsson, L. E. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12684 · Cited by 304 · see citing works
Blood–Brain Barrier Dynamics to Maintain Brain Homeostasis
Segarra, M., Aburto, M. R., & Acker‐Palmer, A. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2020.12.002 · Cited by 304 · see citing works
Cross talk: the microbiota and neurodevelopmental disorders
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G., & Dinan, T. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00490 · Cited by 271 · see citing works
Antibiotics in early life: dysbiosis and the damage done
Neuman, H., Forsythe, P., Uzan-Yulzari, A., Avni, O., & Koren, O. (2018) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuy018 · Cited by 258 · see citing works
Gut reactions: how the blood-brain barrier connects the microbiome and the brain
Logsdon, A. F., Erickson, M. A., Rhea, E. M., Salameh, T. S., & Banks, W. A. (2018) · Experimental Biology and Medicine · doi:10.1177/1535370217743766 · Cited by 235 · see citing works
The Microbiome in Psychology and Cognitive Neuroscience
Sarkar, A., Harty, S., Lehto, S. M., Moeller, A. H., Dinan, T. G., Dunbar, R., Cryan, J. F., & Burnet, P. W. J. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.04.006 · Cited by 233 · see citing works
The role of the gut microbiota in dietary interventions for depression and anxiety
Bear, T. L. K., Dalziel, J. E., Coad, J., Roy, N. C., Butts, C. A., & Gopal, P. K. (2020) · Advances in Nutrition · doi:10.1093/advances/nmaa016 · Cited by 229 · see citing works
Role of Inflammatory Mechanisms in Major Depressive Disorder: From Etiology to Potential Pharmacological Targets
Kouba, B. R., Borba, L. A., de Souza, P. B., Gil‐Mohapel, J., & Rodrigues, A. L. S. (2024) · Cells · doi:10.3390/cells13050423 · Cited by 232 · see citing works
Neuroimmune circuits in inter-organ communication
Huh, J. R., & Veiga‐Fernandes, H. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0247-z · Cited by 216 · see citing works
Gut microbiota modulate neurobehavior through changes in brain insulin sensitivity and metabolism
Soto, M., Herzog, C., Pacheco, J. A., Fujisaka, S., Bullock, K., Clish, C. B., & Kahn, C. R. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0086-5 · Cited by 216 · see citing works
Gut microbiota in patients with Alzheimer’s disease spectrum: a systematic review and meta-analysis
Hung, C.-C., Chang, C., Huang, C.-W., Nouchi, R., & Cheng, C. (2022) · Aging · doi:10.18632/aging.203826 · Cited by 217 · see citing works
Antibiotic-induced gut dysbiosis and barrier disruption and the potential protective strategies
Duan, H., Yu, L., Tian, F., Zhai, Q., Fan, L., & Chen, W. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2020.1843396 · Cited by 215 · see citing works
You’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
Emerging role of gut microbiota in modulation of neuroinflammation and neurodegeneration with emphasis on Alzheimer's disease
Goyal, D., Ali, S. A., & Singh, R. K. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110112 · Cited by 205 · see citing works
Programming Bugs: Microbiota and the Developmental Origins of Brain Health and Disease
Codagnone, M. G., Spichak, S., O’Mahony, S. M., O’Leary, O. F., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.014 · Cited by 198 · see citing works
Psychobiotics: Mechanisms of Action, Evaluation Methods and Effectiveness in Applications with Food Products
Toro-Barbosa, M. D., Hurtado‐Romero, A., García-Amezquita, L. E., & García‐Cayuela, T. (2020) · Nutrients · doi:10.3390/nu12123896 · Cited by 195 · see citing works
Evidence for interplay among antibacterial-induced gut microbiota disturbance, neuro-inflammation, and anxiety in mice
Jang, H.-M., Lee, H.-J., Jang, S.-E., Han, M. J., & Kim, D.-H. (2018) · Mucosal Immunology · doi:10.1038/s41385-018-0042-3 · Cited by 181 · see citing works
Gut microbiota profiles in treatment-naïve children with attention deficit hyperactivity disorder
Jiang, H.-Y., Zhou, Y.-Y., Zhou, G.-L., Li, Y.-C., Yuan, J., Li, X.-H., & Ruan, B. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.03.036 · Cited by 164 · see citing works
The Impact of Gut Microbiota Disorders on the Blood–Brain Barrier
Wei, T., Zhu, H., Feng, Y., Guo, R., & Wan, D. (2020) · Infection and Drug Resistance · doi:10.2147/idr.s254403 · Cited by 163 · see citing works
The communication mechanism of the gut-brain axis and its effect on central nervous system diseases: A systematic review
Lu, S., Zhao, Q., Yu, G., Sun, Z., Li, W., Guo, S., & Zhang, A. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.117207 · Cited by 182 · see citing works
Risk and Protective Environmental Factors Associated with Autism Spectrum Disorder: Evidence-Based Principles and Recommendations
Gialloreti, L. E., Mazzone, L., Benvenuto, A., Fasano, A., García-Alcón, A., Kraneveld, A. D., Moavero, R., Raz, R., Riccio, M. P., Siracusano, M., et al. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8020217 · Cited by 157 · see citing works
Gut microbiota composition is associated with temperament traits in infants
Aatsinki, A.-K., Lahti, L., Uusitupa, H.-M., Munukka, E., Keskitalo, A., Nolvi, S., O'Mahony, S., Pietilä, S., Elo, L. L., Eerola, E., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.05.035 · Cited by 148 · see citing works
Perinatal Interactions between the Microbiome, Immunity, and Neurodevelopment
Pronovost, G. N., & Hsiao, E. Y. (2019) · Immunity · doi:10.1016/j.immuni.2018.11.016 · Cited by 146 · see citing works
Gut-Brain-Microbiota Axis: Antibiotics and Functional Gastrointestinal Disorders
Karakan, T., Özkul, C., Akkol, E. K., Bilici, S., Sobarzo‐Sánchez, E., & Capasso, R. (2021) · Nutrients · doi:10.3390/nu13020389 · Cited by 155 · see citing works
Physiology and molecular biology of barrier mechanisms in the fetal and neonatal brain
Saunders, N. R., Dzięgielewska, K. M., Møllgård, K., & Habgood, M. D. (2018) · The Journal of Physiology · doi:10.1113/jp275376 · Cited by 151 · see citing works
Case-Control Study of the Effects of Gut Microbiota Composition on Neurotransmitter Metabolic Pathways in Children With Attention Deficit Hyperactivity Disorder
Wan, L., Ge, W., Zhang, S., Sun, Y.-L., Wang, B., & Yang, G. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00127 · Cited by 149 · see citing works
Myelin as a regulator of development of the microbiota-gut-brain axis
Keogh, C. E., Kim, D. H. J., Pusceddu, M. M., Knotts, T. A., Rabasa, G., Sladek, J. A., Hsieh, M. T., Honeycutt, M., Brust-Mascher, I., Barboza, M., et al. (2021) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.11.001 · Cited by 137 · see citing works
Comparative Evaluation of Microbiota Engraftment Following Fecal Microbiota Transfer in Mice Models: Age, Kinetic and Microbial Status Matter
Roy, T. L., Debédat, J., Marquet, F., Da-Cunha, C., Ichou, F., Guerre-Millo, M., Kapel, N., Aron‐Wisnewsky, J., & Clément, K. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.03289 · Cited by 143 · see citing works
Influence of the microbiota-gut-brain axis on behavior and welfare in farm animals: A review
Kraïmi, N., Dawkins, M. S., Gebhardt‐Henrich, S. G., Velge, P., Rychlı́k, I., Volf, J., Créach, P., Smith, A. L., Colles, F. M., & Leterrier, C. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.112658 · Cited by 145 · see citing works
Pathophysiological and neurobehavioral characteristics of a propionic acid-mediated autism-like rat model
Choi, J., Lee, S., Won, J., Jin, Y., Hong, Y., Hur, T.-Y., Kim, J.-H., Lee, S.-R., & Hong, Y. (2018) · PLOS ONE · doi:10.1371/journal.pone.0192925 · Cited by 139 · see citing works
A review of antibiotics, depression, and the gut microbiome
Hao, W., Li, X., Zhang, P.-W., & Chen, J. (2019) · Psychiatry Research · doi:10.1016/j.psychres.2019.112691 · Cited by 144 · see citing works
Critical windows of early-life microbiota disruption on behaviour, neuroimmune function, and neurodevelopment
Lynch, C. M. K., Cowan, C. S. M., Bastiaanssen, T. F. S., Moloney, G. M., Theune, N., van de Wouw, M., Florensa-Zanuy, E., Ventura‐Silva, A. P., Codagnone, M. G., Villalobos-Manríquez, F., et al. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.12.008 · Cited by 133 · see citing works
Multi-hit early life adversity affects gut microbiota, brain and behavior in a sex-dependent manner
Rincel, M., Aubert, P., Chevalier, J., Grohard, P. ‐., Basso, L., de Oliveira, C. M., Helbling, J., Lévy, É., Chevalier, G., Leboyer, M., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.03.006 · Cited by 132 · see citing works
Prenatal stress disrupts social behavior, cortical neurobiology and commensal microbes in adult male offspring
Gur, T. L., Palkar, A. V., Rajasekera, T., Allen, J., Niraula, A., Godbout, J., & Bailey, M. T. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.06.025 · Cited by 127 · see citing works
The Microbiome-Gut-Brain Axis and Resilience to Developing Anxiety or Depression under Stress
Bear, T., Dalziel, J. E., Coad, J., Roy, N. C., Butts, C. A., & Gopal, P. K. (2021) · Microorganisms · doi:10.3390/microorganisms9040723 · Cited by 132 · see citing works
Gut microbiota composition during infancy and subsequent behavioural outcomes
Loughman, A., Ponsonby, A.-L., O'Hely, M., Symeonides, C., Collier, F., Tang, M. L. K., Carlin, J., Ranganathan, S., Allen, K., Pezic, A., et al. (2020) · EBioMedicine · doi:10.1016/j.ebiom.2020.102640 · Cited by 120 · see citing works
Early-life exposure to low-dose oxidants can increase longevity via microbiome remodelling in Drosophila
Obata, F., Fons, C., & Gould, A. P. (2018) · Nature Communications · doi:10.1038/s41467-018-03070-w · Cited by 114 · see citing works
The role of the gut microbiome in the development of schizophrenia
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G. A., & Dinan, T. G. (2020) · Schizophrenia Research · doi:10.1016/j.schres.2020.02.010 · Cited by 119 · see citing works
Microbiota-brain interactions: Moving toward mechanisms in model organisms
Nagpal, J. K., & Cryan, J. F. (2021) · Neuron · doi:10.1016/j.neuron.2021.09.036 · Cited by 107 · see citing works
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 107 · see citing works
Antibiotic-Induced Gut Microbiota Dysbiosis Damages the Intestinal Barrier, Increasing Food Allergy in Adult Mice
Zhang, Q., Cheng, L., Wang, J., Hao, M., & Che, H. (2021) · Nutrients · doi:10.3390/nu13103315 · Cited by 110 · see citing works
Gut Microbiota as a Therapeutic Target to Ameliorate the Biochemical, Neuroanatomical, and Behavioral Effects of Traumatic Brain Injuries
Rice, M. W., Pandya, J. D., & Shear, D. A. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00875 · Cited by 89 · see citing works
Manipulations of the gut microbiome alter chemotherapy-induced inflammation and behavioral side effects in female mice
Grant, C. V., Loman, B. R., Bailey, M. T., & Pyter, L. M. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.04.014 · Cited by 102 · see citing works
Exposure to antibiotics in the first 24 months of life and neurocognitive outcomes at 11 years of age
Slykerman, R. F., Coomarasamy, C., Wickens, K. L., Thompson, J., Stanley, T., Barthow, C. A., Kang, J., Crane, J., & Mitchell, E. A. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05216-0 · Cited by 100 · see citing works
Role of antibiotic use, plasma citrulline and blood microbiome in advanced non-small cell lung cancer patients treated with nivolumab
Ouaknine, J., de Tauriers, P. H., Duménil, C., Neveux, N., Dumoulin, J., Giraud, V., Labrune, S., Tisserand, J. C., Julié, C., Emile, J., et al. (2019) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-019-0658-1 · Cited by 100 · see citing works
Probiotics in Treatment of Viral Respiratory Infections and Neuroinflammatory Disorders
Shahbazi, R., Yasavoli‐Sharahi, H., Alsadi, N., Ismail, N., & Matar, C. (2020) · Molecules · doi:10.3390/molecules25214891 · Cited by 101 · see citing works
The microbiota–microglia axis in central nervous system disorders
Mossad, O., & Erny, D. (2020) · Brain Pathology · doi:10.1111/bpa.12908 · Cited by 98 · see citing works
Antibiotic effects on gut microbiota, metabolism, and beyond
Mu, C., & Zhu, W. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-10165-x · Cited by 97 · see citing works
Autism Spectrum Disorders and the Gastrointestinal Tract: Insights into Mechanisms and Clinical Relevance
Hung, L. Y., & Margolis, K. G. (2024) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-023-00857-1 · Cited by 96 · see citing works
Microbiota-gut-brain axis and toll-like receptors in Alzheimer’s disease
Lin, C., Zhao, S., Zhu, Y., Fan, Z., Wang, J., Zhang, B., & Chen, Y. (2019) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2019.09.008 · Cited by 91 · see citing works
Antibiotic body burden of elderly Chinese population and health risk assessment: A human biomonitoring-based study
Zhu, Y., Liu, K., Zhang, J., Liu, X., Yang, L., Wei, R., Wang, S., Zhang, D., Xie, S., & Tao, F. (2019) · Environmental Pollution · doi:10.1016/j.envpol.2019.113311 · Cited by 89 · see citing works
A review of the antimicrobial side of antidepressants and its putative implications on the gut microbiome
McGovern, A. S., Hamlin, A. S., & Winter, G. (2019) · Australian & New Zealand Journal of Psychiatry · doi:10.1177/0004867419877954 · Cited by 89 · see citing works
Microbiota and Microglia Interactions in ASD
Davoli-Ferreira, M., Thomson, C. A., & McCoy, K. D. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.676255 · Cited by 90 · see citing works
When pharmaceutical drugs become environmental pollutants: Potential neural effects and underlying mechanisms
Vaudin, P., Augé‐Gouillou, C., Just, N., Mhaouty‐Kodja, S., Mortaud, S., & Pillon, D. (2021) · Environmental Research · doi:10.1016/j.envres.2021.112495 · Cited by 95 · see citing works
Reciprocal Interactions Between Gut Microbiota and Host Social Behavior
Münger, E., Montiel-Castro, A. J., Langhans, W., & Pacheco‐López, G. (2018) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2018.00021 · Cited by 84 · see citing works
The gut microbiome and Alzheimer’s disease: Complex and bidirectional interactions
Tarawneh, R. M., & Penhos, E. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104814 · Cited by 88 · see citing works
Dietary emulsifiers consumption alters anxiety-like and social-related behaviors in mice in a sex-dependent manner
Holder, M. K., Peters, N. V., Whylings, J., Fields, C. T., Gewirtz, A. T., Chassaing, B., & Vries, G. J. D. (2019) · Scientific Reports · doi:10.1038/s41598-018-36890-3 · Cited by 85 · see citing works
Mouse strain affects behavioral and neuroendocrine stress responses following administration of probiotic Lactobacillus rhamnosus JB-1 or traditional antidepressant fluoxetine
McVey Neufeld, K.-A., Kay, S., & Bienenstock, J. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00294 · Cited by 79 · see citing works
Feasibility, Acceptability, and Safety of Faecal Microbiota Transplantation in the Treatment of Major Depressive Disorder: A Pilot Randomized Controlled Trial
Green, J. E., Berk, M., Mohebbi, M., Loughman, A., McGuinness, A. J., Castle, D. J., Chatterton, M. L., Perez, J., Strandwitz, P., Athan, E., et al. (2023) · The Canadian Journal of Psychiatry · doi:10.1177/07067437221150508 · Cited by 87 · see citing works
The Gut Microbiome as a Regulator of the Neuroimmune Landscape
Yu, L. W., Agirman, G., & Hsiao, E. Y. (2022) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101320-014237 · Cited by 75 · see citing works
Parental Infections Before, During, and After Pregnancy as Risk Factors for Mental Disorders in Childhood and Adolescence: A Nationwide Danish Study
Lydholm, C. N., Köhler‐Forsberg, O., Nordentoft, M., Yolken, R. H., Mortensen, P. B., Petersen, L. V., & Benros, M. E. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.09.013 · Cited by 80 · see citing works
Microbiome, Parkinson’s Disease and Molecular Mimicry
Miraglia, F., & Colla, E. (2019) · Cells · doi:10.3390/cells8030222 · Cited by 81 · see citing works
Development of Microbiota in Infants and its Role in Maturation of Gut Mucosa and Immune System
Ximénez, C., & Torres, J. (2017) · Archives of Medical Research · doi:10.1016/j.arcmed.2017.11.007 · Cited by 81 · see citing works
Visible-light-driven CQDs@MIL-125(Ti) nanocomposite photocatalyst with enhanced photocatalytic activity for the degradation of tetracycline
Li, Z., Che, G., Jiang, W. H., Liu, L., & Wang, H. (2019) · RSC Advances · doi:10.1039/c9ra05600a · Cited by 77 · see citing works
Microbiome Gut-Brain-Axis: Impact on Brain Development and Mental Health
Ramadan, Y. N., Alqifari, S. F., Alshehri, K., Alhowiti, A., Mirghani, H. O., Alrasheed, T., Aljohani, F., Alghamdi, A. M., & Hetta, ‏. F. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-04846-0 · Cited by 90 · see citing works
Neurodevelopmental outcomes following neonatal late-onset sepsis and blood culture-negative conditions
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Authors: Leclercq, S., Mian, F. M., Stanisz, A. M., Bindels, L. B., Cambier, E., Ben-Amram, H., Koren, O., Forsythe, P., & Bienenstock, J.
Affiliations: St. Joseph’s Healthcare Hamilton (CA)
UCLouvain (BE)
Bar-Ilan University (IL)
Corresponding author: Leclercq, Sophie
Bienenstock, John
ORCID: Leclercq, Sophie
Bindels, Laure B.
Koren, Omry
Forsythe, Paul
Bienenstock, John
Venue: Nature Communications
Publisher: Springer Science and Business Media LLC
Published: 2017-04-04
Volume: 8
Issue: 1
Pages: 15062-15062
ISSN: 2041-1723 (ISSN-L)
DOI: 10.1038/ncomms15062
PMC: PMC5382287
OpenAlex: W2604983128
Cited by: 434
References: 79
Citations by year: 2026: 28 · 2025: 42 · 2024: 45 · 2023: 52 · 2022: 46 · 2021: 53 · 2020: 58 · 2019: 53 · 2018: 43 · 2017: 13
FWCI: 18.65
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Nature Communications (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
DIAL (Catholic University of Leuven) (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: International Development Research Centre
Fonds De La Recherche Scientifique - FNRS
Israel Science Foundation
Azrieli Foundation
Alimentary Health
Canadian Institutes of Health Research
Office of Naval Research (N000141410787, N00014)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Keywords: early-life antibiotic exposure, gut microbiota, brain cytokines, frontal cortex, blood-brain barrier, anxiety-like behavior, social behavior, aggression, neuropsychiatric disorders, postnatal development
MeSH terms: Gastrointestinal Microbiome, Animals, Anti-Bacterial Agents, Anxiety, Female, Frontal Lobe, Lactobacillus, Male, Mice, Inbred C57BL, Penicillin V, Pregnancy, Prenatal Exposure Delayed Effects, Social Behavior, Cytokines, Probiotics

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Low-Dose Penicillin in Early Life Induces Long-Term Changes in Murine Gut Microbiota, Brain Cytokines and Behavior

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