The intestinal microbiome, probiotics and prebiotics in neurogastroenterology

Saulnier, Delphine M.; Ringel, Yehuda; Heyman, Melvin B.; Foster, Jane A.; Bercik, Premysl; Shulman, Robert J.; Versalovic, James; Verdu, Elena F.; Dinan, Ted G.; Hecht, Gail; Guarner, Francisco

doi:10.4161/gmic.22973

Cited by 248Gut microbiota and healthGastrointestinal motility and disordersProbiotics and Fermented Foods

The intestinal microbiome, probiotics and prebiotics in neurogastroenterology

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Saulnier, Delphine M., Ringel, Yehuda, Heyman, Melvin B., Foster, Jane A., Bercik, Premysl, Shulman, Robert J., Versalovic, James, Verdu, Elena F. +3 more·2013·Gut Microbes

DOI 10.4161/gmic.22973PMC PMC3555881

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Abstract

The brain-gut axis allows bidirectional communication between the central nervous system (CNS) and the enteric nervous system (ENS), linking emotional and cognitive centers of the brain with peripheral intestinal functions. Recent experimental work suggests that the gut microbiota have an impact on the brain-gut axis. A group of experts convened by the International Scientific Association for Probiotics and Prebiotics (ISAPP) discussed the role of gut bacteria on brain functions and the implications for probiotic and prebiotic science. The experts reviewed and discussed current available data on the role of gut microbiota on epithelial cell function, gastrointestinal motility, visceral sensitivity, perception and behavior. Data, mostly gathered from animal studies, suggest interactions of gut microbiota not only with the enteric nervous system but also with the central nervous system via neural, neuroendocrine, neuroimmune and humoral links. Microbial colonization impacts mammalian brain development in early life and subsequent adult behavior. These findings provide novel insights for improved understanding of the potential role of gut microbial communities on psychological disorders, most particularly in the field of psychological comorbidities associated with functional bowel disorders like irritable bowel syndrome (IBS) and should present new opportunity for interventions with pro- and prebiotics.

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Gastrointestinal microbiota may contribute to the affective symptoms associated with GI disorders by impacting the CNS via immune, hormonal, and neural mechanisms.
“Gastrointestinal microbiota may also contribute to the affective symptoms associated with GI disorders by impacting the CNS via immune, hormonal, and neural mechanisms (17, 69, 155).”
From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [155]
In the periphery, intestinal microbiota can affect the ENS directly via release of bacterial substances or metabolites, or indirectly by inducing the release of host-derived immune mediators that in turn impact the ENS.
“In the periphery, intestinal microbiota can affect the ENS directly via release of bacterial substances or metabolites, or indirectly by inducing the release of host-derived immune mediators that in turn impact the ENS (10, 155).”
From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [155]

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The Role of Genetics in IBS
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Irritable Bowel Syndrome
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Baseline microbiota activity and initial bifidobacteria counts influence responses to prebiotic dosing in healthy subjects
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The Probiotic Lactobacillus acidophilus Stimulates Chloride/Hydroxyl Exchange Activity in Human Intestinal Epithelial Cells
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Gut health promoting activity of new putative probiotic/protective Lactobacillus spp. strains: A functional study in the small intestinal cell model
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Lactobacillus acidophilus stimulates the expression of SLC26A3 via a transcriptional mechanism
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Effects of the probiotic yeast Saccharomyces boulardii on the neurochemistry of myenteric neurones in pig jejunum
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gamma-Aminobutyric acid uptake by a bacterial system with neurotransmitter binding characteristics.
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Chain reactions: Early-life stress alters the metabolic profile of plasma polyunsaturated fatty acids in adulthood
Clarke, G. A., O’Mahony, S. M., Hennessy, A. A., Ross, R. P., Stanton, C., Cryan, J. F., & Dinan, T. G. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.07.008 · Cited by 33 · see citing works
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Luminal Cholera Toxin Alters Motility in Isolated Guinea-Pig Jejunum via a Pathway Independent of 5-HT3 Receptors
Fung, C., Ellis, M., & Bornstein, J. C. (2010) · Frontiers in Neuroscience · doi:10.3389/fnins.2010.00162 · Cited by 25 · see citing works
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Probiotic Lactobacillus reuteri Alleviates the Response to Gastric Distension in Rats,
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The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems.
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Clinical and metabolic response to probiotic administration in patients with major depressive disorder: A randomized, double-blind, placebo-controlled trial
Akkasheh, G., Kashani-Poor, Z., Tajabadi-Ebrahimi, M., Jafari, P., Akbari, H., Taghizadeh, M., Memarzadeh, M. R., Asemi, Z., & Esmaillzadeh, A. (2016) · Nutrition · doi:10.1016/j.nut.2015.09.003 · Cited by 767 · see citing works
Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress
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Microbiota modulation counteracts Alzheimer’s disease progression influencing neuronal proteolysis and gut hormones plasma levels
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The progress of gut microbiome research related to brain disorders
Zhu, S., Jiang, Y., Xu, K., Cui, M., Ye, W., Zhao, G., Jin, L., & Chen, X. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-1705-z · Cited by 419 · see citing works
Gut Microbiota, Muscle Mass and Function in Aging: A Focus on Physical Frailty and Sarcopenia
Ticinesi, A., Nouvenne, A., Cerundolo, N., Catania, P., Prati, B., Tana, C., & Meschi, T. (2019) · Nutrients · doi:10.3390/nu11071633 · Cited by 418 · see citing works
Gut-brain Axis and migraine headache: a comprehensive review
On behalf of the School of Advanced Studies of the European Headache Federation (EHF-SAS), Arzani, M., Jahromi, S. R., Ghorbani, Z., Vahabizad, F., Martelletti, P., Ghaemi, A., Sacco, S., & Togha, M. (2020) · The Journal of Headache and Pain · doi:10.1186/s10194-020-1078-9 · Cited by 366 · see citing works
The effects of plant-based diets on the body and the brain: a systematic review
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Effect of probiotics on central nervous system functions in animals and humans: a systematic review
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Irritable bowel syndrome: A microbiome-gut-brain axis disorder?
Kennedy, P. J. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i39.14105 · Cited by 335 · see citing works
The Impact of Microbiota on Brain and Behavior: Mechanisms & Therapeutic Potential
Borre, Y. E., Moloney, R. D., Clarke, G., Dinan, T. G., & Cryan, J. F. (2014) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-0897-4_17 · Cited by 329 · see citing works
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Autism spectrum disorders and intestinal microbiota
De Angelis, M., Francavilla, R., Piccolo, M., De Giacomo, A., & Gobbetti, M. (2015) · Gut Microbes · doi:10.1080/19490976.2015.1035855 · Cited by 311 · see citing works
Modulation of Gut Microbiota–Brain Axis by Probiotics, Prebiotics, and Diet
Liu, X., Cao, S., & Zhang, X. (2015) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5b02404 · Cited by 304 · see citing works
Microbiota regulation of the mammalian gut-brain axis
Burokas, A., Moloney, R. D., Dinan, T. G., & Cryan, J. F. (2015) · Advances in applied microbiology · doi:10.1016/bs.aambs.2015.02.001 · Cited by 300 · see citing works
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Interplay between the gut-brain axis, obesity and cognitive function
Agustí, A., García-Pardo, M. P., López-Almela, I., Campillo, I., Maes, M., Romaní-Pérez, M., & Sanz, Y. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00155 · Cited by 294 · see citing works
Modulatory Effects of Gut Microbiota on the Central Nervous System: How Gut Could Play a Role in Neuropsychiatric Health and Diseases
Yarandi, S., Peterson, D. A., Treisman, G. J., Moran, T. H., & Pasricha, P. J. (2016) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm15146 · Cited by 294 · see citing works
Sex hormones in the modulation of irritable bowel syndrome
Mulak, A. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i10.2433 · Cited by 277 · see citing works
Alzheimer's disease and the microbiome
Bhattacharjee, S., & Lukiw, W. J. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00153 · Cited by 248 · see citing works
Irritable bowel syndrome, the microbiota and the gut-brain axis
Raskov, H., Burcharth, J., Pommergaard, H.-C., & Rosenberg, J. (2016) · Gut Microbes · doi:10.1080/19490976.2016.1218585 · Cited by 243 · see citing works
Microbe-host interactions: influence of the gut microbiota on the enteric nervous system
Hyland, N. P., & Cryan, J. F. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.06.027 · Cited by 207 · see citing works
Exploring gut microbes in human health and disease: Pushing the envelope
Sun, J., & Chang, E. B. (2014) · Genes & Diseases · doi:10.1016/j.gendis.2014.08.001 · Cited by 194 · see citing works
Emerging Trends in “Smart Probiotics”: Functional Consideration for the Development of Novel Health and Industrial Applications
El Hage, R., Hernandez-Sanabria, E., & Van de Wiele, T. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01889 · Cited by 185 · see citing works
Stress and the gut microbiota-brain axis
Molina‐Torres, G., Rodríguez-Arrastia, M. J., Román, P., Sánchez‐Labraca, N., & Cardona, D. (2019) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000478 · Cited by 181 · see citing works
Co-evolution in context: The importance of studying gut microbiomes in wild animals
Amato, K. R. (2013) · Microbiome Science and Medicine · doi:10.2478/micsm-2013-0002 · Cited by 162 · see citing works
Antibiotic-induced dysbiosis alters host-bacterial interactions and leads to colonic sensory and motor changes in mice
Aguilera, M., Cerdà-Cuéllar, M., & Martínez, V (2015) · Gut Microbes · doi:10.4161/19490976.2014.990790 · Cited by 162 · see citing works
Gut microbiota, the immune system, and diet influence the neonatal gut–brain axis
Sherman, M. P., Zaghouani, H., & Niklas, V. (2014) · Pediatric Research · doi:10.1038/pr.2014.161 · Cited by 161 · see citing works
Gut Microbiome Alterations Precede Cerebral Amyloidosis and Microglial Pathology in a Mouse Model of Alzheimer’s Disease
Chen, Y., Fang, L., Chen, S., Zhou, H., Fan, Y., Li, L., Li, J., Xu, J., Chen, Y., Ma, Y., et al. (2020) · BioMed Research International · doi:10.1155/2020/8456596 · Cited by 150 · see citing works
Organ-On-A-Chip in vitro Models of the Brain and the Blood-Brain Barrier and Their Value to Study the Microbiota-Gut-Brain Axis in Neurodegeneration
Raimondi, I., Izzo, L., Tunesi, M., Comar, M., Albani, D., & Giordano, C. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00435 · Cited by 147 · see citing works
Microbiome: Should we diversify from diversity?
Johnson, K. V. ‐., & Burnet, P. W. J. (2016) · Gut Microbes · doi:10.1080/19490976.2016.1241933 · Cited by 142 · see citing works
Psychobiotics: A new approach for treating mental illness?
Misra, S., & Mohanty, D. (2019) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2017.1399860 · Cited by 142 · see citing works
Gut microbiota manipulation through probiotics oral administration restores glucose homeostasis in a mouse model of Alzheimer's disease
Bonfili, L., Cecarini, V., Gogoi, O., Berardi, S., Scarpona, S., Angeletti, M., Rossi, G., & Eleuteri, A. M. (2019) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2019.11.004 · Cited by 134 · see citing works
Autism: Metabolism, Mitochondria, and the Microbiome
Macfabe, D. (2013) · Global Advances in Health and Medicine · doi:10.7453/gahmj.2013.089 · Cited by 131 · see citing works
Lignans and Gut Microbiota: An Interplay Revealing Potential Health Implications
Senizza, A., Rocchetti, G., Mosele, J. I., Patrone, V., Callegari, M. L., Morelli, L., & Lucini, L. (2020) · Molecules · doi:10.3390/molecules25235709 · Cited by 132 · see citing works
The Gut-Brain Axis in Neurodegenerative Diseases and Relevance of the Canine Model: A Review
Ambrosini, Y. M., Borcherding, D. C., Kanthasamy, A., Kim, H. J., Willette, A., Jergens, A., Allenspach, K., & Mochel, J. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00130 · Cited by 116 · see citing works
Dietary Prebiotics and Bioactive Milk Fractions Improve NREM Sleep, Enhance REM Sleep Rebound and Attenuate the Stress-Induced Decrease in Diurnal Temperature and Gut Microbial Alpha Diversity
Thompson, R. S., Roller, R., Mika, A., Greenwood, B. N., Knight, R. D., Chichlowski, M., Berg, B. M., & Fleshner, M. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00240 · Cited by 117 · see citing works
Metabolic tinkering by the gut microbiome
Selkrig, J., Wong, P., Zhang, X., & Pettersson, S. (2014) · Gut Microbes · doi:10.4161/gmic.28681 · Cited by 116 · see citing works
Microbiota modulation as preventative and therapeutic approach in Alzheimer’s disease
Bonfili, L., Cecarini, V., Gogoi, O., Gong, C., Cuccioloni, M., Angeletti, M., Rossi, G., & Eleuteri, A. M. (2020) · FEBS Journal · doi:10.1111/febs.15571 · Cited by 118 · see citing works
Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome
Ringel, Y., & Maharshak, N. (2013) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00207.2012 · Cited by 115 · see citing works
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Eating Disorders and Gastrointestinal Diseases
Santonicola, A., Gagliardi, M., Guarino, M. P. L., Siniscalchi, M., Ciacci, C., & Iovino, P. (2019) · Nutrients · doi:10.3390/nu11123038 · Cited by 107 · see citing works
Effect of continuous ingestion of a beverage prepared with Lactobacillus gasseri CP2305 inactivated by heat treatment on the regulation of intestinal function
Sawada, D., Sugawara, T., Ishida, Y., Aihara, K., Aoki, Y., Takehara, I., Takano, K., & Fujiwara, S. (2015) · Food Research International · doi:10.1016/j.foodres.2015.11.032 · Cited by 104 · see citing works
Gut–brain axis biochemical signalling from the gastrointestinal tract to the central nervous system: gut dysbiosis and altered brain function
Arneth, B. M. (2018) · Postgraduate Medical Journal · doi:10.1136/postgradmedj-2017-135424 · Cited by 104 · see citing works
Effect of prebiotics, probiotics, synbiotics on depression: results from a meta-analysis
Zhang, Q., Chen, B., Zhang, J., Dong, J., Ma, J., Zhang, Y., Jin, K., & Lü, J. (2023) · BMC Psychiatry · doi:10.1186/s12888-023-04963-x · Cited by 114 · see citing works
Impact of gut microbiota on neurological diseases: Diet composition and novel treatments
Larroya-García, A., Navas-Carrillo, D., & Orenes‐Piñero, E. (2018) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1484340 · Cited by 105 · see citing works
Role of Gut Microbiota in Neurological Disorders and Its Therapeutic Significance
Tiwari, P., Dwivedi, R., Bansal, M., Tripathi, M., & Dada, R. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12041650 · Cited by 106 · see citing works
The Gastrointestinal Tract Microbiome and Potential Link to Alzheimerâ€™s Disease
Hill, J. M., Bhattacharjee, S., Pogue, A. I., & Lukiw, W. J. (2014) · Frontiers in Neurology · doi:10.3389/fneur.2014.00043 · Cited by 98 · see citing works
The connection between microbiome and schizophrenia
Golofast, B., & Vales, K. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.12.011 · Cited by 92 · see citing works
Postnatal colonization with human "infant-type" Bifidobacterium species alters behavior of adult gnotobiotic mice
Luk, B., Veeraragavan, S., Engevik, M., Balderas, M., Major, A., Runge, J., Luna, R. A., & Versalovic, J. (2018) · PLOS ONE · doi:10.1371/journal.pone.0196510 · Cited by 90 · see citing works
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Early life diets with prebiotics and bioactive milk fractions attenuate the impact of stress on learned helplessness behaviours and alter gene expression within neural circuits important for stress resistance
Mika, A., Day, H. E. W., Martinez, A. S., Rumian, N. L., Greenwood, B. N., Chichlowski, M., Berg, B. M., & Fleshner, M. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13444 · Cited by 88 · see citing works
‘As above, so below’ examining the interplay between emotion and the immune system
Brod, S., Rattazzi, L., Piras, G., & D’Acquisto, F. (2014) · Immunology · doi:10.1111/imm.12341 · Cited by 86 · see citing works
Short-Chain Fatty Acids in the Microbiota–Gut–Brain Axis: Role in Neurodegenerative Disorders and Viral Infections
Majumdar, A., Venkatesh, I. P. S., & Basu, A. (2023) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.2c00803 · Cited by 85 · see citing works
Introduction to the special focus issue on the impact of diet on gut microbiota composition and function and future opportunities for nutritional modulation of the gut microbiome to improve human health
Donovan, S. M. (2017) · Gut Microbes · doi:10.1080/19490976.2017.1299309 · Cited by 85 · see citing works
Enteric nervous system assembly: Functional integration within the developing gut
Hao, M. M., Foong, J. P. P., Bornstein, J. C., Li, Z. L., Berghe, P. V., & Boesmans, W. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.05.030 · Cited by 84 · see citing works
Effect of commensals and probiotics on visceral sensitivity and pain in irritable bowel syndrome
Theodorou, V., Ait-Belgnaoui, A., Agostini, S., & Eutamene, H. (2014) · Gut Microbes · doi:10.4161/gmic.29796 · Cited by 83 · see citing works
Prebiotics and Bioactive Milk Fractions Affect Gut Development, Microbiota, and Neurotransmitter Expression in Piglets
Berding, K., Wang, M., Monaco, M. H., Alexander, L. S., Mudd, A. T., Chichlowski, M., Waworuntu, R. V., Berg, B. M., Miller, M. J., Dilger, R. N., et al. (2016) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001200 · Cited by 81 · see citing works
Human resident gut microbe Bacteroides thetaiotaomicron regulates colonic neuronal innervation and neurogenic function
Aktar, R., Parkar, N., Stentz, R., Baumard, L., Parker, A., Goldson, A. J., Brion, A., Carding, S. R., Blackshaw, L. A., & Peiris, M. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1766936 · Cited by 80 · see citing works
Aronia melanocarpa polysaccharide ameliorates inflammation and aging in mice by modulating the AMPK/SIRT1/NF-κB signaling pathway and gut microbiota
Zhao, Y., Liu, X., Zheng, Y., Liu, W., & Ding, C. (2021) · Scientific Reports · doi:10.1038/s41598-021-00071-6 · Cited by 78 · see citing works
Bacillus Subtilis Delays Neurodegeneration and Behavioral Impairment in the Alzheimer’s Disease Model Caenorhabditis Elegans
Cogliati, S., Clementi, V., Francisco, M., Crespo, C., Argañaraz, F., & Grau, R. R. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-190837 · Cited by 77 · see citing works
Probiotic bacteria and bile acid profile are modulated by prebiotic diet and associate with facilitated diurnal clock/sleep realignment after chronic disruption of rhythms
Thompson, R. S., Gaffney, M., Hopkins, S., Kelley, T., González, A., Bowers, S. J., Vitaterna, M. H., Turek, F. W., Foxx, C. L., Lowry, C. A., et al. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.07.006 · Cited by 80 · see citing works
Probiotics for the treatment of depression and anxiety: A systematic review and meta-analysis of randomized controlled trials
El Dib, R., Periyasamy, A. G., de Barros, J. L., França, C. G., Senefonte, F. L., Vesentini, G., Alves, M. G. O., Rodrigues, J. V. D. S., Gomaa, H., Gomes Júnior, J. R., et al. (2021) · Clinical Nutrition ESPEN · doi:10.1016/j.clnesp.2021.07.027 · Cited by 75 · see citing works
Systematic review of gut microbiota and attention-deficit hyperactivity disorder (ADHD)
Sukmajaya, A. C., Lusida, M. I., Soetjipto, S., & Setiawati, Y. (2021) · Annals of General Psychiatry · doi:10.1186/s12991-021-00330-w · Cited by 74 · see citing works
Probiotics for Neurodegenerative Diseases: A Systemic Review
Ojha, S., Patil, N., Jain, M., Kole, C., & Kaushik, P. (2023) · Microorganisms · doi:10.3390/microorganisms11041083 · Cited by 77 · see citing works
Lactobacillus acidophilus NCFM affects colonic mucosal opioid receptor expression in patients with functional abdominal pain ‐ a randomised clinical study
Ringel‐Kulka, T., Goldsmith, J. R., Carroll, I. M., Barros, S. P., Palsson, O. S., Jobin, C., & Ringel, Y. (2014) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.12800 · Cited by 76 · see citing works
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Implications of the human microbiome in inflammatory bowel diseases
Bakhtiar, S. M., LeBlanc, J. G., Salvucci, E., Ali, A., Martín, R., Langella, P., Chatel, J., Miyoshi, A., Bermúdez‐Humarán, L. G., & Azevedo, V. (2013) · FEMS Microbiology Letters · doi:10.1111/1574-6968.12111 · Cited by 72 · see citing works
Clinical and psychological responses to synbiotic supplementation in obese or overweight adults: A randomized clinical trial
Hadi, A., Sepandi, M., Marx, W., Moradi, S., & Parastouei, K. (2019) · Complementary Therapies in Medicine · doi:10.1016/j.ctim.2019.102216 · Cited by 73 · see citing works
Bacterial extracellular vesicles: A position paper by the microbial vesicles task force of the Chinese society for extracellular vesicles
Wen, M., Wang, J., Ou, Z., Nie, G., Chen, Y., Li, M., Wu, Z., Xiong, S., Zhou, H., Yang, Z., et al. (2023) · Interdisciplinary medicine · doi:10.1002/inmd.20230017 · Cited by 70 · see citing works
The Impact of Microbiota-Gut-Brain Axis on Diabetic Cognition Impairment
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Authors: 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., & Guarner, F.
Affiliations: University of North Carolina at Chapel Hill (US)
University of California, San Francisco (US)
McMaster University (CA)
Baylor College of Medicine (US)
University of Illinois Chicago (US)
Vall d'Hebron Hospital Universitari (ES)
Corresponding author: Saulnier, Delphine M.
ORCID: Heyman, Melvin B.
Foster, Jane A.
Shulman, Robert J.
Versalovic, James
Verdu, Elena F.
Hecht, Gail
Guarner, Francisco
Venue: Gut Microbes
Publisher: Informa UK Limited
Published: 2013-01
Volume: 4
Issue: 1
Pages: 17-27
ISSN: 1949-0976 (ISSN-L)
1949-0984
DOI: 10.4161/gmic.22973
PMC: PMC3555881
OpenAlex: W2031431575
Cited by: 248
References: 90
Citations by year: 2026: 11 · 2025: 14 · 2024: 10 · 2023: 19 · 2022: 20 · 2021: 25 · 2020: 20 · 2019: 24 · 2018: 23 · 2017: 18 · 2016: 16 · 2015: 20 · 2014: 20 · 2013: 8
FWCI: 1.40
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Gut Microbes (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institute of Diabetes and Digestive and Kidney Diseases (R01DK097043)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Keywords: gut microbiota, gut-brain axis, probiotics, prebiotics, enteric nervous system, central nervous system, neurogastroenterology, gastrointestinal motility, visceral sensitivity, neuroimmune interactions, neuroendocrine signaling, brain development, mental illness, irritable bowel syndrome, functional bowel disorders, microbial colonization
MeSH terms: Behavior, Central Nervous System, Emotions, Gastrointestinal Agents, Gastrointestinal Diseases, Gastrointestinal Motility, Humans, Enteric Nervous System, Probiotics, Gastrointestinal Tract, Metagenome, Prebiotics

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