The DOI matches its Crossref record; 100 of the 100 references it cites were found in a registry or an index.
The anxiolytic effect of probiotics: A systematic review and meta-analysis of the clinical and preclinical literature
Open accessAbstract
BACKGROUND: Probiotics have generated intensive research interest in recent years as a novel mode of treatment for physical and mental illness. Nevertheless, the anxiolytic potential of probiotics remains unclear. The present systematic review and meta-analysis aimed to evaluate the clinical and preclinical (animal model) evidence regarding the effect of probiotic administration on anxiety. METHODS: The PubMed, PsycINFO, and Web of Science databases were reviewed for preclinical and clinical studies that met the defined inclusion and exclusion criteria. The effects of probiotics on anxiety-like behavior and symptoms of anxiety were analyzed by meta-analyses. Separate subgroup analyses were conducted on diseased versus healthy animals, specific preclinical probiotic species, and clinical versus healthy human samples. RESULTS: Data were extracted from 22 preclinical studies (743 animals) and 14 clinical studies (1527 individuals). Overall, probiotics reduced anxiety-like behavior in animals (Hedges' g = -0.47, 95% CI -0.77 --0.16, p = 0.004). Subgroup analyses revealed a significant reduction only among diseased animals. Probiotic species-level analyses identified only Lactobacillus (L.) rhamnosus as an anxiolytic species, but these analyses were broadly under-powered. Probiotics did not significantly reduce symptoms of anxiety in humans (Hedges' g = -0.12, 95% CI -0.29-0.05, p = 0.151), and did not differentially affect clinical and healthy human samples. CONCLUSIONS: While preclinical (animal) studies suggest that probiotics may help reduce anxiety, such findings have not yet translated to clinical research in humans, perhaps due to the dearth of extant research with clinically anxious populations. Further investigation of probiotic treatment for clinically relevant anxiety is warranted, particularly with respect to the probiotic species L. rhamnosus.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“More recently, a systematic review and meta-analysis of clinical and pre-clinical literature on the effects of probiotics on anxiety asserted that probiotics may help reduce anxiety [297].”
From International Society of Sports Nutrition Position Stand: Probiotics (2019) · cites this paper as [297]
In the citing paper
“Furthermore, probiotic supplementations, as Lactobacillus rhamnosus (JB-1), in already colonized mice, reduced anxiety- and depression-like behavior in steady-state conditions (92, 93).”
From The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology (2020) · cites this paper as [92]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,893
Measuring inconsistency in meta-analyses
Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003) · BMJ · doi:10.1136/bmj.327.7414.557 · Cited by 63,139
Bias in meta-analysis detected by a simple, graphical test
Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997) · BMJ · doi:10.1136/bmj.315.7109.629 · Cited by 56,722
The Cochrane Collaboration's tool for assessing risk of bias in randomised trials
Higgins, J. P. T., Altman, D. G., Gotzsche, P. C., Juni, P., Moher, D., Oxman, A. D., Savovic, J., Schulz, K. F., Weeks, L., Sterne, J. A. C., et al. (2011) · BMJ · doi:10.1136/bmj.d5928 · Cited by 33,817
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P. C., Ioannidis, J. P. A., Clarke, M., Devereaux, P. J., Kleijnen, J., & Moher, D. (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000100 · Cited by 28,164
Dermyshi, E., Wang, Y., Yan, C., Hong, W., Qiu, G., Gong, X., & Zhang, T. (2017) · Neonatology · doi:10.1159/000454668 · Cited by 24,586
Sterne, J. A. C., Sutton, A. J., Ioannidis, J. P. A., Terrin, N., Jones, D. R., Lau, J., Carpenter, J., Rucker, G., Harbord, R. M., Schmid, C. H., et al. (2011) · BMJ · doi:10.1136/bmj.d4002 · Cited by 7,709
Power failure: why small sample size undermines the reliability of neuroscience
Button, K. S., Ioannidis, J. P. A., Mokrysz, C., Nosek, B. A., Flint, J., Robinson, E. S. J., & Munafò, M. R. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3475 · Cited by 7,641
Changes of Intestinal Functions in Liver Cirrhosis
Fukui, H., & Wiest, R. (2016) · Inflammatory Intestinal Diseases · doi:10.1159/000444436 · Cited by 6,820
Diversity, stability and resilience of the human gut microbiota
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K., & Knight, R. (2012) · Nature · doi:10.1038/nature11550 · Cited by 5,533
Host-Bacterial Mutualism in the Human Intestine
Bäckhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A., & Gordon, J. I. (2005) · Science · doi:10.1126/science.1104816 · Cited by 5,277
SYRCLE’s risk of bias tool for animal studies
Hooijmans, C. R., Rovers, M. M., de Vries, R. B., Leenaars, M., Ritskes-Hoitinga, M., & Langendam, M. W. (2014) · BMC Medical Research Methodology · doi:10.1186/1471-2288-14-43 · Cited by 4,415
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888
Guyot, P., Ades, A. E., Ouwens, M., & Welton, N. J. (2012) · BMC Medical Research Methodology · doi:10.1186/1471-2288-12-9 · Cited by 2,560
The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems.
(2015) · PubMed Central · Cited by 2,540
Host Remodeling of the Gut Microbiome and Metabolic Changes during Pregnancy
Koren, O., Goodrich, J. K., Cullender, T. C., Spor, A., Laitinen, K., Kling Bäckhed, H., Gonzalez, A., Werner, J. J., Angenent, L. T., Knight, R., et al. (2012) · Cell · doi:10.1016/j.cell.2012.07.008 · Cited by 2,165
The global burden of mental disorders: An update from the WHO World Mental Health (WMH) surveys
Kessler, R. C., Aguilar-Gaxiola, S., Alonso, J., Chatterji, S., Lee, S., Ormel, J., Üstün, T. B., & Wang, P. S. (2009) · Epidemiologia e Psichiatria Sociale · doi:10.1017/s1121189x00001421 · Cited by 1,895
Messaoudi, M., Lalonde, R., Violle, N., Javelot, H., Desor, D., Nejdi, A., Bisson, J.-F., Rougeot, C., Pichelin, M., Cazaubiel, M., et al. (2011) · British Journal of Nutrition · doi:10.1017/s0007114510004319 · Cited by 1,324
Consumption of fermented milk product with probiotic modulates brain activity
Tillisch, K., Labus, J., Kilpatrick, L., Jiang, Z., Stains, J., Ebrat, B., Guyonnet, D., Legrain–Raspaud, S., Trotin, B., Naliboff, B., et al. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.02.043 · Cited by 1,192
Long-term ecological impacts of antibiotic administration on the human intestinal microbiota
Jernberg, C., Löfmark, S., Edlund, C., & Jansson, J. K. (2007) · The ISME Journal · doi:10.1038/ismej.2007.3 · Cited by 1,134
Temporal and spatial variation of the human microbiota during pregnancy
DiGiulio, D. B., Callahan, B. J., McMurdie, P. J., Costello, E. K., Lyell, D. J., Robaczewska, A., Sun, C. L., Goltsman, D. S. A., Wong, R. J., Shaw, G., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1502875112 · Cited by 1,129
Bercik, P., Park, A. J., Sinclair, D., Khoshdel, A., Lu, J., Huang, X., Deng, Y., Blennerhassett, P. A., Fahnestock, M., Moine, D., et al. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2011.01796.x · Cited by 1,018
Lai, H. M. X., Cleary, M., Sitharthan, T., & Hunt, G. E. (2015) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2015.05.031 · Cited by 941
Anxiety and Risk of Incident Coronary Heart Disease
Roest, A. M., Martens, E. J., de Jonge, P., & Denollet, J. (2010) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2010.03.034 · Cited by 865
Pinto-Sanchez, M. I., Hall, G. B., Ghajar, K., Nardelli, A., Bolino, C., Lau, J. T., Martin, F.-P., Cominetti, O., Welsh, C., Rieder, A., et al. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.05.003 · Cited by 821
Small sample adjustments for robust variance estimation with meta-regression.
Tipton, E. (2015) · Psychological Methods · doi:10.1037/met0000011 · Cited by 810
Melsen, W. G., Bootsma, M. C. J., Rovers, M. M., & Bonten, M. J. M. (2014) · Clinical Microbiology and Infection · doi:10.1111/1469-0691.12494 · Cited by 776
The global burden of anxiety disorders in 2010
Baxter, A. J., Vos, T., Scott, K. M., Ferrari, A. J., & Whiteford, H. A. (2014) · Psychological Medicine · doi:10.1017/s0033291713003243 · Cited by 768
Bercik, P., Verdu, E. F., Foster, J. A., Macri, J., Potter, M., Huang, X., Malinowski, P., Jackson, W., Blennerhassett, P., Neufeld, K. A., et al. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.06.063 · Cited by 674
Steenbergen, L., Sellaro, R., van Hemert, S., Bosch, J. A., & Colzato, L. S. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.04.003 · Cited by 671
Liang, S., Wang, T., Hu, X., Luo, J., Li, W., Wu, X., Duan, Y., & Jin, F. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.033 · Cited by 651
Fond, G., Loundou, A., Hamdani, N., Boukouaci, W., Dargel, A., Oliveira, J., Roger, M., Tamouza, R., Leboyer, M., & Boyer, L. (2014) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-014-0502-z · Cited by 647
Ait-Belgnaoui, A., Durand, H., Cartier, C., Chaumaz, G., Eutamene, H., Ferrier, L., Houdeau, E., Fioramonti, J., Bueno, L., & Theodorou, V. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.03.024 · Cited by 612
Response rates for CBT for anxiety disorders: need for standardized criteria
Loerinc, A. G., Meuret, A. E., Twohig, M. P., Rosenfield, D., Bluett, E. J., & Craske, M. G. (2015) · Clinical Psychology Review · doi:10.1016/j.cpr.2015.08.004 · Cited by 592
Depression and anxiety in patients with Inflammatory Bowel Disease: a systematic review
Neuendorf, R., Harding, A., Stello, N., Hanes, D., & Wahbeh, H. (2016) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2016.06.001 · Cited by 561
McNulty, N. P., Yatsunenko, T., Hsiao, A., Faith, J. J., Muegge, B. D., Goodman, A. L., Henrissat, B., Oozeer, R., Cools-Portier, S., Gobert, G., et al. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3002701 · Cited by 559
Efficacy of treatments for anxiety disorders: a meta-analysis
Bandelow, B., Reitt, M., Röver, C., Michaelis, S., Görlich, Y., & Wedekind, D. (2015) · International Clinical Psychopharmacology · doi:10.1097/yic.0000000000000078 · Cited by 555
Impact of consuming a milk drink containing a probiotic on mood and cognition
Benton, D., Williams, C., & Brown, A. (2007) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602546 · Cited by 554
Towards a better understanding of Lactobacillus rhamnosus GG - host interactions
Segers, M. E., & Lebeer, S. (2014) · Microbial Cell Factories · doi:10.1186/1475-2859-13-s1-s7 · Cited by 535
Meta-analysis of data from animal studies: A practical guide
Vesterinen, H. M., Sena, E. S., Egan, K. J., Hirst, T. C., Churolov, L., Currie, G. L., Antonic‐Baker, A., Howells, D. W., & Macleod, M. R. (2013) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2013.09.010 · Cited by 488
Labus, J. S., Bolus, R., Chang, L., Wiklund, I., Naesdal, J., Mayer, E. A., & Naliboff, B. D. (2004) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2004.02007.x · Cited by 475
Systematic review automation technologies
Tsafnat, G., Glasziou, P., Choong, M. K., Dunn, A., Galgani, F., & Coiera, E. (2014) · Systematic Reviews · doi:10.1186/2046-4053-3-74 · Cited by 472
Immunomodulatory mechanisms of lactobacilli
Wells, J. M. (2011) · Microbial Cell Factories · doi:10.1186/1475-2859-10-s1-s17 · Cited by 449
Role of the intestinal microbiome in health and disease: from correlation to causation
de Vos, W. M., & de Vos, E. A. (2012) · Nutrition Reviews · doi:10.1111/j.1753-4887.2012.00505.x · Cited by 440
Ait‐Belgnaoui, A., Colom, A., Braniste, V., Ramalho, L., Marrot, A., Cartier, C., Houdeau, E., Theodorou, V., & Tompkins, T. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12295 · Cited by 434
Slykerman, R. F., Hood, F., Wickens, K., Thompson, J. M. D., Barthow, C., Murphy, R., Kang, J., Rowden, J., Stone, P., Crane, J., et al. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.09.013 · Cited by 422
A systematic review of sleep disturbance in anxiety and related disorders
Cox, R. C., & Olatunji, B. O. (2016) · Journal of Anxiety Disorders · doi:10.1016/j.janxdis.2015.12.001 · Cited by 395
A systematic review of the safety of probiotics
Didari, T., Solki, S., Mozaffari, S., Nikfar, S., & Abdollahi, M. (2014) · Expert Opinion on Drug Safety · doi:10.1517/14740338.2014.872627 · Cited by 367
Risk of bias in reports of in vivo research: a focus for improvement
Macleod, M. R., Lawson McLean, A., Kyriakopoulou, A., Serghiou, S., de Wilde, A., Sherratt, N., Hirst, T., Hemblade, R., Bahor, Z., Nunes-Fonseca, C., et al. (2015) · PLOS Biology · doi:10.1371/journal.pbio.1002273 · Cited by 358
Didari, T. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i10.3072 · Cited by 356
Kelly, J. R., Allen, A. P., Temko, A., Hutch, W., Kennedy, P. J., Farid, N., Murphy, E., Boylan, G., Bienenstock, J., Cryan, J. F., et al. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.11.018 · Cited by 355
Effect of probiotics on central nervous system functions in animals and humans: a systematic review
Wang, H., Lee, I.-S., Braun, C., & Enck, P. (2016) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm16018 · Cited by 334
Romijn, A. R., Rucklidge, J. J., Kuijer, R. G., & Frampton, C. (2017) · Australian & New Zealand Journal of Psychiatry · doi:10.1177/0004867416686694 · Cited by 323
Ganji‐Arjenaki, M., & Rafieian‐Kopaei, M. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.25911 · Cited by 314
Efficacy of drug treatments for generalised anxiety disorder: systematic review and meta-analysis
Baldwin, D. S., Woods, R., Lawson, R., & Taylor, D. M. (2011) · BMJ · doi:10.1136/bmj.d1199 · Cited by 301
The need for randomization in animal trials: an overview of systematic reviews
Hirst, J. A., Howick, J., Aronson, J. K., Roberts, N., Perera, R., Koshiaris, C., & Heneghan, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098856 · Cited by 294
Psychotropic effects of Lactobacillus plantarum PS128 in early life-stressed and naïve adult mice
Liu, Y.-W., Liu, W., Wu, C.-C., Juan, Y.-C., Wu, Y.-C., Tsai, H.-P., Wang, S. Z., & Tsai, Y.-C. (2015) · Brain Research · doi:10.1016/j.brainres.2015.11.018 · Cited by 290
Kato-Kataoka, A., Nishida, K., Takada, M., Kawai, M., Kikuchi-Hayakawa, H., Suda, K., Ishikawa, H., Gondo, Y., Shimizu, K., Matsuki, T., et al. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.04134-15 · Cited by 288
Goehler, L. E., Park, S. M., Opitz, N., Lyte, M., & Gaykema, R. P. A. (2008) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.08.009 · Cited by 287
Pirbaglou, M., Katz, J., de Souza, R. J., Stearns, J. C., Motamed, M., & Ritvo, P. (2016) · Nutrition Research · doi:10.1016/j.nutres.2016.06.009 · Cited by 270
Liu, W.-H., Chuang, H.-L., Huang, Y.-T., Wu, C.-C., Chou, G.-T., Wang, S., & Tsai, Y.-C. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.10.046 · Cited by 269
Emergency medicine animal research: does use of randomization and blinding affect the results?
Bebarta, V., Luyten, D., & Heard, K. (2003) · Academic Emergency Medicine · doi:10.1111/j.1553-2712.2003.tb00056.x · Cited by 244
Takada, M., Nishida, K., Kataoka‐Kato, A., Gondo, Y., Ishikawa, H., Suda, K., Kawai, M., Hoshi, R., Watanabe, O., Igarashi, T., et al. (2016) · Neurogastroenterology & Motility · doi:10.1111/nmo.12804 · Cited by 243
Bharwani, A., Mian, M. F., Surette, M. G., Bienenstock, J., & Forsythe, P. (2017) · BMC Medicine · doi:10.1186/s12916-016-0771-7 · Cited by 236
Empirical Evidence of Bias in the Design of Experimental Stroke Studies
Crossley, N. A., Sena, E. S., Göhler, J., Horn, J., van der Worp, H. B., Bath, P. M., Macleod, M. R., & Dirnagl, U. (2008) · Stroke · doi:10.1161/strokeaha.107.498725 · Cited by 235
Wang, T., Hu, X., Liang, S., Li, W., Wu, X., Wang, L., & Jin, F. (2015) · Beneficial Microbes · doi:10.3920/bm2014.0177 · Cited by 233 · cited 2×
“Study Baseline characteristics Incomplete outcome data Selective reporting Other bias Agusti et al. 2017 Unclear Low Low Low Barrera-Bugueno et al. 2017 Unclear Low Low High Beilharz et al. 2017 Unclear Low Low Low Bercik et al. 2010 Unclear Low Low Unclear Bercik et al. 2011 Unclear Unclear Low Unclear Bharwani et al…”
BackgroundInfluentialAntibiotic Exposure and the Risk for Depression, Anxiety, or Psychosis: A Nested Case-Control Study
Lurie, I., Yang, Y.-X., Haynes, K., Mamtani, R., & Boursi, B. (2015) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.15m09961 · Cited by 231
Lyte, M., Varcoe, J. J., & Bailey, M. T. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00145-0 · Cited by 218
Ibnou-Zekri, N., Blum, S., Schiffrin, E. J., & von der Weid, T. (2002) · Infection and Immunity · doi:10.1128/iai.71.1.428-436.2003 · Cited by 216
The probiotic Bifidobacterium infantis 35624 displays visceral antinociceptive effects in the rat
McKernan, D. P., Fitzgerald, P., Dinan, T. G., & Cryan, J. F. (2010) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01520.x · Cited by 205
Harmer, C. J., & Cowen, P. J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0407 · Cited by 197
Jerndal, P., Ringström, G., Agerforz, P., Karpefors, M., Akkermans, L. M., Bayati, A., & Simrén, M. (2010) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01493.x · Cited by 192
Luo, J., Wang, T., Liang, S., Hu, X., Li, W., & Jin, F. (2014) · Science China Life Sciences · doi:10.1007/s11427-014-4615-4 · Cited by 187
Moya-Pérez, Á., Pérez‐Villalba, A., Benítez‐Páez, A., Campillo, I., & Sanz, Y. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.05.011 · Cited by 181
SIMRÉN, M., ÖHMAN, L., OLSSON, J., SVENSSON, U., OHLSON, K., POSSERUD, I., & STRID, H. (2010) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2009.04183.x · Cited by 169
Takada, M., Nishida, K., Gondo, Y., Kikuchi-Hayakawa, H., Ishikawa, H., Suda, K., Kawai, M., Hoshi, R., Kuwano, Y., Miyazaki, K., et al. (2017) · Beneficial Microbes · doi:10.3920/bm2016.0150 · Cited by 160
Emge, J. R., Huynh, K., Miller, E. N., Kaur, M., Reardon, C., Barrett, K. E., & Gareau, M. G. (2016) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00086.2016 · Cited by 152
Mantegazza, C., Molinari, P., D’Auria, E., Sonnino, M., Morelli, L., & Zuccotti, G. (2017) · Pharmacological Research · doi:10.1016/j.phrs.2017.08.001 · Cited by 149
Probiotics normalize the gut-brain-microbiota axis in immunodeficient mice
Smith, C. J., Emge, J. R., Berzins, K., Lung, L., Khamishon, R., Shah, P., Rodrigues, D. M., Sousa, A. J., Reardon, C., Sherman, P. M., et al. (2014) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00238.2014 · Cited by 143
On communication between gut microbes and the brain
Forsythe, P., Kunze, W. A., & Bienenstock, J. (2012) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e3283572ffa · Cited by 137
I.31, a new combination of probiotics, improves irritable bowel syndrome-related quality of life
Lorenzo‐Zúñiga, V. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i26.8709 · Cited by 120
Marcos, A., W�rnberg, J., Nova, E., Gómez‐Martínez, S., Alvarez, A. M., Alvarez, R., Mateos, J. A., & Cobo, J. M. (2004) · European Journal of Nutrition · doi:10.1007/s00394-004-0517-8 · Cited by 116
Beilharz, J. E., Kaakoush, N. O., Maniam, J., & Morris, M. J. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.38 · Cited by 116
Divyashri, G., Krishna, G., ., M., & Prapulla, S. G. (2015) · Journal of Medical Microbiology · doi:10.1099/jmm.0.000184 · Cited by 110
Lamousé-Smith, E. S. N., Tzeng, A., & Starnbach, M. N. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027662 · Cited by 109
Irritable bowel syndrome symptom severity improves equally with probiotic and placebo
Lyra, A., Hillilä, M., Huttunen, T., Männikkö, S., Taalikka, M., Tennilä, J., Tarpila, A., Lahtinen, S., Ouwehand, A. C., & Veijola, L. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i48.10631 · Cited by 106
Ingestion of mycobacterium vaccae decreases anxiety-related behavior and improves learning in mice
Matthews, D. M., & Jenks, S. M. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2013.02.007 · Cited by 105
Agusti, A., Moya-Pérez, A., Campillo, I., Montserrat-de la Paz, S., Cerrudo, V., Perez-Villalba, A., & Sanz, Y. (2018) · Molecular Neurobiology · doi:10.1007/s12035-017-0768-z · Cited by 85
Cowan, C. S. M., Callaghan, B. L., & Richardson, R. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.94 · Cited by 83
Systematic review of evidence to support the theory of psychobiotics
Romijn, A. R., & Rucklidge, J. J. (2015) · Nutrition Reviews · doi:10.1093/nutrit/nuv025 · Cited by 81
Matijašić, B. B., Obermajer, T., Lipoglavšek, L., Sernel, T., Locatelli, I., Kos, M., Šmid, A., & Rogelj, I. (2016) · Journal of Dairy Science · doi:10.3168/jds.2015-10743 · Cited by 81
Mackos, A. R., Eubank, T. D., Parry, N. M. A., & Bailey, M. T. (2013) · Infection and Immunity · doi:10.1128/iai.00278-13 · Cited by 78
Probiotics reduce psychological stress in patients before laryngeal cancer surgery
Yang, H., Zhao, X., Tang, S., Huang, H., Zhao, X., Ning, Z., Fu, X., & Zhang, C. (2016) · Asia-Pacific Journal of Clinical Oncology · doi:10.1111/ajco.12120 · Cited by 66
Walter, S. A., Jones, M., Talley, N. J., Kjellström, L., Nyhlin, H., Andréasson, A., & Agréus, L. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12155 · Cited by 62
L. fermentum CECT 5716 prevents stress‐induced intestinal barrier dysfunction in newborn rats
Vanhaecke, T., Aubert, P., Grohard, P. ‐., Durand, T., Hulin, P., Paul‐Gilloteaux, P., Fournier, A. P., Docagne, F., Ligneul, A., Fressange-Mazda, C., et al. (2017) · Neurogastroenterology & Motility · doi:10.1111/nmo.13069 · Cited by 45
Anxiogenic effects of a Lactobacillus, inulin and the synbiotic on healthy juvenile rats
Barrera-Bugueño, C., Realini, O., Escobar-Luna, J., Sotomayor-Zárate, R., Gotteland, M., Julio-Pieper, M., & Bravo, J. A. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.06.064 · Cited by 38
Jang, H., Jang, S., Han, M. J., & Kim, D.-H. (2017) · Beneficial Microbes · doi:10.3920/bm2016.0226 · Cited by 38
Flaws in animal studies exploring statins and impact on meta‐analysis
Moja, L., Pecoraro, V. L., Ciccolallo, L., Dall’Olmo, L., Virgili, G., & Garattini, S. K. (2014) · European Journal of Clinical Investigation · doi:10.1111/eci.12264 · Cited by 23
Bruch, J. D. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.05.014 · Cited by 23
Shapiro, J. M., Cho, J. H., Sands, B. E., & LeLeiko, N. S. (2015) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2015.02.028 · Cited by 13
Flagged first, then by citations
Cited by
Sorted by citations
The pros, cons, and many unknowns of probiotics
Suez, J., Zmora, N., Segal, E., & Elinav, E. (2019) · Nature Medicine · doi:10.1038/s41591-019-0439-x · Cited by 1,398
The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology
Rutsch, A., Kantsjö, J. B., & Ronchi, F. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.604179 · Cited by 821
Liu, R. T., Walsh, R. F. L., & Sheehan, A. E. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.03.023 · Cited by 564
Health-Promoting Components in Fermented Foods: An Up-to-Date Systematic Review
Melini, F., Melini, V., Luziatelli, F., Ficca, A. G., & Ruzzi, M. (2019) · Nutrients · doi:10.3390/nu11051189 · Cited by 438
Probiotics and the microbiota-gut-brain axis: Focus on psychiatry
Mörkl, S., Butler, M. I., Holl, A., Cryan, J. F., & Dinan, T. G. (2020) · Current Nutrition Reports · doi:10.1007/s13668-020-00313-5 · Cited by 337
Metadata
- Authors
- Reis, D. J., Ilardi, S. S., & Punt, S. E. W.
- Affiliations
- University of Kansas (US)
- Corresponding author
- Reis, Daniel J.
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2018-06-20
- Volume
- 13
- Issue
- 6
- Pages
- e0199041
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC6010276
- OpenAlex
- W2809387633
- Cited by
- 123
- References
- 100
- Citations by year
- 2026: 8 · 2025: 18 · 2024: 19 · 2023: 18 · 2022: 13 · 2021: 14 · 2020: 16 · 2019: 14 · 2018: 2
- FWCI
- 1.16
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- KU ScholarWorks (University of Kansas) (submittedVersion, cc-by)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Medicine › Complementary and alternative medicine › Medicinal Plant Extracts Effects
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- probiotics, anxiety, anxiolytic effects, anxiety-like behavior, Lactobacillus rhamnosus, clinical anxiety, animal models of anxiety, gut microbiota, translational research
- MeSH terms
- Animals, Anxiety, Anxiety Disorders, Drug Evaluation, Preclinical, Exploratory Behavior, Female, Humans, Male, Research Design, Species Specificity, Anti-Anxiety Agents, Randomized Controlled Trials as Topic, Maze Learning, Probiotics, Mice, Rats, Lacticaseibacillus rhamnosus
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
