A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood
Open accessAbstract
BACKGROUND: Recent insights into the role of the human microbiota in cognitive and affective functioning have led to the hypothesis that probiotic supplementation may act as an adjuvant strategy to ameliorate or prevent depression. OBJECTIVE: Heightened cognitive reactivity to normal, transient changes in sad mood is an established marker of vulnerability to depression and is considered an important target for interventions. The present study aimed to test if a multispecies probiotic containing Bifidobacterium bifidum W23, Bifidobacterium lactis W52, Lactobacillus acidophilus W37, Lactobacillus brevis W63, Lactobacillus casei W56, Lactobacillus salivarius W24, and Lactococcus lactis (W19 and W58) may reduce cognitive reactivity in non-depressed individuals. DESIGN: In a triple-blind, placebo-controlled, randomized, pre- and post-intervention assessment design, 20 healthy participants without current mood disorder received a 4-week probiotic food-supplement intervention with the multispecies probiotics, while 20 control participants received an inert placebo for the same period. In the pre- and post-intervention assessment, cognitive reactivity to sad mood was assessed using the revised Leiden index of depression sensitivity scale. RESULTS: Compared to participants who received the placebo intervention, participants who received the 4-week multispecies probiotics intervention showed a significantly reduced overall cognitive reactivity to sad mood, which was largely accounted for by reduced rumination and aggressive thoughts. CONCLUSION: These results provide the first evidence that the intake of probiotics may help reduce negative thoughts associated with sad mood. Probiotics supplementation warrants further research as a potential preventive strategy for depression.
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Several studies in healthy participants have demonstrated reduced stress-induced cortisol levels and pro-inflammatory cytokines, along with improved cognitive test performance, perceptions of stress, anxiety, and mood.
“Several studies in healthy participants have demonstrated reduced stress-induced cortisol levels and pro-inflammatory cytokines, along with improved cognitive test performance, perceptions of stress, anxiety, and mood (465–469).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [468]
Various Lactobacillus strains, or Lactobacillus-containing supplements, have been shown to reduce depressive-like behaviour in rodents and improve measures of depression in humans.
“Various Lactobacillus strains, or Lactobacillus-containing supplements, have been shown to reduce depressive-like behaviour in rodents [1, 13, 23, 44, 45] and improve measures of depression in humans [3, 5, 39, 76].”
From Distinct actions of the fermented beverage kefir on host behaviour, immunity and microbiome gut-brain modules in the mouse (2020) · cites this paper as [76]
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“These genera have been found to be effective in ameliorating anxious and depressive symptoms (Benton et al., 2006; Rao et al., 2009; Yamamura et al., 2009; Desbonnet et al., 2010; Bravo et al., 2011; Messaoudi et al., 2011).”
BackgroundThought suppression and cognitive vulnerability to depression
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“…reactivity to transient changes in sad mood was measured by means of the revised Leiden Index of Depression Sensitivity (LEIDS-r; van der Does and Williams, 2003), which has been shown to be predictive of depression in multiple longitudinal studies (van der Does, 2005; Kruijt et al., 2013).”
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“Interestingly, cognitive reactivity to sad mood has been associated with serotonin concentrations, with higher scores correlating with lower serotonin levels (Booij and Van der Does, 2007; Wells et al., 2010; see also Firk and Markus, 2009).”
BackgroundEffect of the rehydration medium on the recovery of freeze-dried lactic acid bacteria
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“The batch used for the present experiments contained >2.5 109 CFU/g, whereas the placebo contained 1 104 CFU/g. Rehydration of freeze-dried lactic acid bacteria in milk, water and physiological salt solution has been shown to result in equal survival rates (de Valdez et al., 1985).”
MethodInfluentialAn Investigation of the Relationship Between Cognitive Reactivity and Rumination
Moulds, M. L., Kandris, E., Williams, A. D., Lang, T., Yap, C. S. L., & Hoffmeister, K. (2007) · Behavior Therapy · doi:10.1016/j.beth.2007.05.001 · Cited by 69 · see citing works
Gut Pathogens: enteric health at the interface of changing microbiology
Ahmed, N., Sechi, L. A., Mégraud, F., & Hasnain, S. E. (2009) · Gut Pathogens · doi:10.1186/1757-4749-1-1 · Cited by 69 · see citing works
Serotonin transporter gene, childhood emotional abuse and cognitive vulnerability to depression
Antypa, N., & van der Does, W. A. J. (2010) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00593.x · Cited by 66 · cited 2× · see citing works
“Internal consistency (Cronbach’s alpha; a) is 0.89 for the LEIDS total score, and ranges between 0.62 (Acceptance/Coping) and 0.84 for the subscales (Hopelessness/Suicidality; Antypa and van der Does, 2010; Williams et al., 2008).”
BackgroundInfluentialNeural and Hormonal Regulation of Gastrointestinal Function: An Overview
Grossman, M. I. (1979) · Annual Review of Physiology · doi:10.1146/annurev.ph.41.030179.000331 · Cited by 66 · cited 1× · see citing works
“The intestine and the brain are intimately connected via the brain-gut axis, which involves bidirectional communication via neural, endocrine and immune pathways (Grossman, 1979; Grenham et al., 2011; Mayer, 2011; Mayer et al., 2014).”
BackgroundCognitive and serotonergic vulnerability to depression: Convergent findings.
Booij, L., & van der Does, W. A. J. (2007) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.116.1.86 · Cited by 55 · cited 2× · see citing works
“…found to predict depression incidence in multiple longitudinal studies and to correlate with depression risk factors, such as depression history (Moulds et al., 2008), genetic markers of depression (Antypa and van der Does, 2010), and reaction to tryptophan depletion (Booij and van der Does, 2007).”
BackgroundPsychometric Properties of the Leiden Index of Depression Sensitivity (LEIDS)
Solis, E., Antypa, N., Conijn, J. M., Kelderman, H., & van der Does, W. (2017) · Psychological Assessment · doi:10.1037/pas0000326 · Cited by 54 · see citing works
Kruijt, A.-W., Antypa, N., Booij, L., de Jong, P. J., Glashouwer, K., Penninx, B. W. J. H., & Van der Does, W. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070245 · Cited by 49 · see citing works
Stress modulation of visuomotor binding
Colzato, L. S., Kool, W., & Hommel, B. (2008) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2008.01.006 · Cited by 44 · cited 1× · see citing works
“The M.I.N.I. is a short structured interview, taking about 15 min, which screens for several psychiatric disorders (Sheehan et al., 1998; Colzato et al., 2008, 2010).”
BackgroundSelf-citationClinical Studies Evaluating Effects of Probiotics on Parameters of Intestinal Barrier Function
van Hemert, S., Verwer, J. H., & Schütz, B. (2013) · Advances in Microbiology · doi:10.4236/aim.2013.32032 · Cited by 34 · cited 2× · see citing works
“Thus, our results show that the intake of multispecies probiotics for a 4-week period significantly reduced overall cognitive reactivity to depression and in particular aggressive and ruminative thoughts.”
BackgroundWells, T. T., Beevers, C. G., & McGeary, J. E. (2010) · Journal of Affective Disorders · doi:10.1016/j.jad.2010.03.019 · Cited by 31 · see citing works
Intestinal permeability measurements: general aspects and possible pitfalls.
Teixeira, T. F. S., Moreira, A. P. B., Souza, N. C., Frías, R., & Pelúzio, M. D. C. G. (2014) · PubMed · doi:10.3305/nh.2014.29.2.7076 · Cited by 21 · see citing works
De Beck Depression Inventory (BDI).
Bouman, T. K. (1994) · University of Groningen research database (University of Groningen / Centre for Information Technology) · Cited by 21 · see citing works
van Hemert, S., & Ormel, G. (2014) · Food and Nutrition Sciences · doi:10.4236/fns.2014.518187 · Cited by 20 · cited 1× · see citing works
“Each bacterial strain of the multispecies probiotics used in this study has been found to improve epithelial barrier function both when tested separately and in combination (Van Hemert and Ormel, 2014).”
BackgroundThe role of vagal function in the prevention of and risk for cardiovascular disease and mortality
Thayer, J. F., & Lane, R. D. (2006) · European Journal of Cardiovascular Prevention & Rehabilitation · doi:10.1097/00149831-200605001-00124 · Cited by 4 · see citing works
Flagged first, then by citations
3 of the 80 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
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
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“…of small studies in healthy individuals suggest pre- and probiotic consumption can positively affect aspects of mood and anxiety (Messaoudi et al., 2011; Steenbergen et al., 2015), modulate HPA function (Messaoudi et al., 2011; Schmidt et al., 2015) and alter brain activity (Tillisch et al., 2013).”
BackgroundMartin, C. R., Osadchiy, V., Kalani, A., & Mayer, E. A. (2018) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2018.04.003 · Cited by 1,284 · see citing works
Stress & the gut-brain axis: Regulation by the microbiome
Foster, J. A., Rinaman, L., & Cryan, J. F. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.03.001 · Cited by 1,150 · see citing works
The microbiome-gut-brain axis in health and disease
Dinan, T. G., & Cryan, J. F. (2017) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2016.09.007 · Cited by 1,111 · see citing works
Kelly, J. R., Kennedy, P. J., Cryan, J. F., Dinan, T. G., Clarke, G., & Hyland, N. P. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00392 · Cited by 1,110 · see citing works
Control of brain development, function, and behavior by the microbiome
Sampson, T. R., & Mazmanian, S. K. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.04.011 · Cited by 1,093 · see citing works
Psychobiotics and the manipulation of bacteria–gut–brain signals
Sarkar, A., Lehto, S. M., Harty, S., Dinan, T. G., Cryan, J. F., & Burnet, P. W. J. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.09.002 · Cited by 1,068 · see citing works
“In studies that show effects of mixtures of probiotics [35,42,152], it is unclear whether the outcome emerges from additive or synergistic interactions between bacterial families, or whether only some of the probiotics in the mixture are truly exerting effects.”
The microbiota-gut-brain axis: from motility to mood
Margolis, K. G., Cryan, J. F., & Mayer, E. A. (2021) · Gastroenterology · doi:10.1053/j.gastro.2020.10.066 · Cited by 999 · see citing works
Kynurenine pathway metabolism and the microbiota-gut-brain axis
Kennedy, P. J., Cryan, J. F., Dinan, T. G., & Clarke, G. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.07.002 · Cited by 724 · see citing works
“Emerging data in healthy humans support preclinical findings suggesting the gut microbiota influence mood and anxiety (Benton et al., 2007; Messaoudi et al., 2011; Steenbergen et al., 2015).”
BackgroundGut Microbiota’s Effect on Mental Health: The Gut-Brain Axis
Clapp, M., Aurora, N., Herrera, L., Bhatia, M., Wilen, E., & Wakefield, S. (2017) · Clinics and Practice · doi:10.4081/cp.2017.987 · Cited by 608 · see citing works
“toms and improved HPA-axis functionality as well as Citalopram and Diazepam.(53,54)”
BackgroundLiu, R. T., Walsh, R. F. L., & Sheehan, A. E. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.03.023 · Cited by 564 · see citing works
“There were 22 trials with 23 unique effects for probiotics and anxiety (Colica et al., 2017; Cremon et al., 2017; Kato-Kataoka et al., 2016; Kelly et al., 2017; Kitaoka et al., 2009; Lyra et al., 2016; Marcos et al., 2004; Messaoudi et al., 2011; Östlund-Lagerström et al., 2016; Pinto-Sanchez et al., 2017; Reale et al…”
BackgroundAnxiety, depression, and the microbiome: A role for gut peptides
Lach, G., Schellekens, H., Dinan, T. G., & Cryan, J. F. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0585-0 · Cited by 573 · see citing works
“salivarius, and Lactococcus lactis [51].”
The microbiome and host behavior
Vuong, H. E., Yano, J. M., Fung, T. C., & Hsiao, E. Y. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031347 · Cited by 537 · see citing works
“Across various paradigms, pre- or probiotic treatment positively affected emotion-related scores and reduced feelings of aggression and rumination (Pärtty et al. 2013, Schmidt et al. 2015, Steenbergen et al. 2015).”
BackgroundAllen, A. P., Hutch, W., Borre, Y. E., Kennedy, P. J., Temko, A., Boylan, G., Murphy, E., Cryan, J. F., Dinan, T. G., & Clarke, G. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.191 · Cited by 513 · see citing works
The microbiome: a key regulator of stress and neuroinflammation
Rea, K., Dinan, T. G., & Cryan, J. F. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.03.001 · Cited by 508 · see citing works
“…processing of emotional material in a functional magnetic resonance imaging brain scan study (Tillisch et al., 2013), as well as reducing negative thoughts associated with sad mood (Steenbergen et al., 2015) reinforcing the role for gastrointestinal microbiota in stress and emotional responses.”
Huang, R., Wang, K., & Hu, J. (2016) · Nutrients · doi:10.3390/nu8080483 · Cited by 505 · see citing works
“11); and that conducted by Steenbergen [30] showed MD = ́0.”
BackgroundMethodInfluentialFeeding the microbiota–gut–brain axis: Diet, microbiome, and neuropsychiatry
Sandhu, K. V., Sherwin, E., Schellekens, H., Stanton, C., Dinan, T. G., & Cryan, J. F. (2017) · Translational Research · doi:10.1016/j.trsl.2016.10.002 · Cited by 491 · see citing works
The role of inflammation and the gut microbiome in depression and anxiety
Peirce, J. M., & Alviña, K. (2019) · Journal of Neuroscience Research · doi:10.1002/jnr.24476 · Cited by 466 · see citing works
The effects of probiotics on depressive symptoms in humans: a systematic review
Wallace, C. J. K., & Milev, R. (2017) · Annals of General Psychiatry · doi:10.1186/s12991-017-0138-2 · Cited by 471 · see citing works
“Forty healthy young adults consumed either a probiotic supplement or placebo for 4 weeks and found that consumption of the multispecies probiotic formula significantly reduced overall cognitive reactivity to depression, in particular aggressive and ruminative thoughts [45].”
BackgroundThe role of the microbiome for human health: From basic science to clinical applications
Mohajeri, M. H., Brummer, R. J. M., Rastall, R. A., Weersma, R. K., Harmsen, H. J. M., Faas, M., & Eggersdorfer, M. (2018) · European Journal of Nutrition · doi:10.1007/s00394-018-1703-4 · Cited by 440 · see citing works
“by healthy participants produced a significant reduction in overall cognitive reactivity (negative thoughts) to sad mood [111].”
BackgroundGut microbiome-wide association study of depressive symptoms
Radjabzadeh, D., Bosch, J. A., Uitterlinden, A. G., Zwinderman, A. H., Ikram, M. A., van Meurs, J. B. J., Luik, A. I., Nieuwdorp, M., Lok, A., van Duijn, C. M., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-34502-3 · Cited by 446 · see citing works
Self-citationMicrobiota-Gut-Brain Axis: New Therapeutic Opportunities
Long-Smith, C., O'Riordan, K. J., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2020) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010919-023628 · Cited by 419 · see citing works
Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
Rusch, J. A., Layden, B. T., & Dugas, L. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1130689 · Cited by 415 · see citing works
Relationship between the gut microbiome and brain function
Mohajeri, M. H., La Fata, G., Steinert, R. E., & Weber, P. (2018) · Nutrition Reviews · doi:10.1093/nutrit/nuy009 · Cited by 376 · see citing works
“Several studies in humans (Table 2) support the data from animal studies and show that the gut microbiota may play a role in modulating depression and anxiety.(73,97,105) Some researchers have reported that the composition of the microbiome was different in patients with major depressive disorder than in their healthy…”
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
“Current Opinion in Biotechnology 2018, 49:140–147 and this is supported in probiotics studies which have indicated that probiotic Lactobacillus might improve symptoms of human depression [63,64].”
BackgroundThomas, S., Izard, J., Walsh, E. K., Batich, K. A., Chongsathidkiet, P., Clarke, G. A., Sela, D. A., Muller, A. J., Mullin, J. M., Albert, K., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-2929 · Cited by 369 · see citing works
Microbiomes as sources of emergent host phenotypes
Lynch, J. B., & Hsiao, E. Y. (2019) · Science · doi:10.1126/science.aay0240 · Cited by 339 · see citing works
A meta-analysis of the use of probiotics to alleviate depressive symptoms
Ng, Q. X., Peters, C., Ho, C. Y. X., Lim, D. Y., & Yeo, W.-S. (2018) · Journal of Affective Disorders · doi:10.1016/j.jad.2017.11.063 · Cited by 357 · see citing works
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 · see citing works
The Gut-Brain Axis: Influence of Microbiota on Mood and Mental Health.
Appleton, J. (2018) · Europe PMC (PubMed Central) · Cited by 337 · see citing works
The advancement of probiotics research and its application in fish farming industries
Banerjee, G., & Ray, A. K. (2017) · Research in Veterinary Science · doi:10.1016/j.rvsc.2017.01.016 · Cited by 337 · see citing works
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 · see citing works
“A recent study using multi-strain probiotics found improvement in the LEIDS-r score, which is predictive of depression.(53) Two studies by Messaoudi et al(39,61) found probiotic formulations of B.”
ResultNeurotransmitters as food supplements: the effects of GABA on brain and behavior
Boonstra, E., de Kleijn, R., Colzato, L. S., Alkemade, A., Forstmann, B. U., & Nieuwenhuis, S. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01520 · Cited by 330 · see citing works
Self-citationBrain-Gut-Microbiota Axis and Mental Health
Dinan, T. G., & Cryan, J. F. (2017) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000519 · Cited by 325 · see citing works
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 · see citing works
“Since the 2015 review, Steenbergen et al. (2015) reported that a multispecies probiotic formulation reduced cognitive reactivity to sad mood significantly more than placebo in a healthy sample; however, there was no effect of probiotics on Beck Depression Inventory (BDI) scores in this study.”
BackgroundDepression's Unholy Trinity: Dysregulated Stress, Immunity, and the Microbiome
Cruz-Pereira, J. S., Rea, K., Nolan, Y. M., O'Leary, O. F., Dinan, T. G., & Cryan, J. F. (2020) · Annual Review of Psychology · doi:10.1146/annurev-psych-122216-011613 · Cited by 320 · see citing works
“…and processing of emotional information in a functional magnetic resonance imaging study (Tillisch et al. 2013) and in the attenuation of negative thoughts associated with a negative mood (Steenbergen et al. 2015), supporting the importance of gut microbiota in stress and emotional responses.”
BackgroundThe gut microbiome composition associates with bipolar disorder and illness severity
Evans, S. J., Bassis, C. M., Hein, R., Assari, S., Flowers, S. A., Kelly, M., Young, V. B., Ellingrod, V. E., & McInnis, M. G. (2016) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2016.12.007 · Cited by 308 · see citing works
The food-gut axis: lactic acid bacteria and their link to food, the gut microbiome and human health
De Filippis, F., Pasolli, E., & Ercolini, D. (2020) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaa015 · Cited by 303 · see citing works
Sherwin, E., Sandhu, K. V., Dinan, T. G., & Cryan, J. F. (2016) · CNS Drugs · doi:10.1007/s40263-016-0370-3 · Cited by 297 · see citing works
“A recent study by Steenbergen and colleagues [139] further demonstrated the beneficial effects of a Lactobacillus and Bifidobacterium mixed probiotic on mood in healthy individuals.”
ResultInterplay 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
Slyepchenko, A., Maes, M., Jacka, F. N., Köhler, C. A., Barichello, T., McIntyre, R. S., Berk, M., Grande, I., Foster, J. A., Vieta, E., et al. (2017) · Psychotherapy and Psychosomatics · doi:10.1159/000448957 · Cited by 278 · see citing works
International Society of Sports Nutrition Position Stand: Probiotics
Jäger, R., Mohr, A. E., Carpenter, K. C., Kerksick, C. M., Purpura, M., Moussa, A., Townsend, J. R., Lamprecht, M., West, N. P., Black, K., et al. (2019) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-019-0329-0 · Cited by 277 · 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
Fatigue in IBD: epidemiology, pathophysiology and management
Borren, N. Z., van der Woude, C. J., & Ananthakrishnan, A. N. (2018) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-018-0091-9 · Cited by 275 · see citing works
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 · see citing works
Gut-Brain Psychology: Rethinking Psychology From the Microbiota–Gut–Brain Axis
Liang, S., Wu, X., & Jin, F. (2018) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2018.00033 · Cited by 269 · see citing works
Chahwan, B., Kwan, S., Isik, A., van Hemert, S., Burke, C., & Roberts, L. (2019) · Journal of Affective Disorders · doi:10.1016/j.jad.2019.04.097 · Cited by 256 · see citing works
“which is a vulnerability marker of depression (Kruijt et al., 2013; Steenbergen et al., 2015; Van der Does, 2005).”
BackgroundResultInfluentialIrritable 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
Schaub, A.-C., Schneider, E., Vázquez-Castellanos, J. F., Schweinfurth, N., Kettelhack, C., Doll, J. P. K., Yamanbaeva, G., Mählmann, L., Brand, S., Beglinger, C., et al. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-01977-z · Cited by 273 · see citing works
“The study intervention took four weeks (31 days) as previous studies could find effects after the same period [36, 37].”
ResultMitrea, L., Nemeș, S. A., Szabo, K., Teleky, B., & Vodnar, D. C. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.813204 · Cited by 242 · see citing works
“(122) administered a multispecies probiotic food-supplement consisting of Bifidobacterium bifidum W23, Bifidobacterium lactis W52, L.”
BackgroundMethodThe 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 231 · see citing works
“In these studies, affective changes have been noted in selfreports[60,62,66].”
BackgroundInfluentialProbiotics drive gut microbiome triggering emotional brain signatures
Bagga, D., Reichert, J. L., Koschutnig, K., Aigner, C. S., Holzer, P. D., Koskinen, K., Moissl‐Eichinger, C., & Schöpf, V. (2018) · Gut Microbes · doi:10.1080/19490976.2018.1460015 · Cited by 230 · see citing works
“Our findings are in line with previous studies showing that manipulation of gut microbiota influences mood and cognition as assessed by psychological questionnaires.(7,8) Neural correlates of emotional decision-making and memory processes: Given that emotion and cognition are inseparable and probiotic administration c…”
ResultUpdate of probiotics in human world: A nonstop source of benefactions till the end of time
Zommiti, M., Feuilloley, M. G. J., & Connil, N. (2020) · Microorganisms · doi:10.3390/microorganisms8121907 · Cited by 225 · see citing works
Hao, Z., Wang, W., Guo, R., & Liu, H. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.02.025 · Cited by 242 · see citing works
Regulation of energy balance by a gut–brain axis and involvement of the gut microbiota
Bauer, P. V., Hamr, S. C., & Duca, F. A. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2083-z · Cited by 221 · see citing works
“with colitis, possibly through a vagally mediated mechanism that regulates BDNF [206] and probiotic supplementation in humans has been shown to improve cognitive reactivity to sad mood through the reduction of rumination and aggressive thoughts [207].”
BackgroundCurrent perspectives on gut microbiome dysbiosis and depression
Capuco, A., Urits, I., Hasoon, J., Chun, R., Gerald, B., Wang, J. K., Kassem, H., Ngo, A. L., Abd-Elsayed, A., Simopoulos, T., et al. (2020) · Advances in Therapy · doi:10.1007/s12325-020-01272-7 · Cited by 216 · see citing works
Neuroactive compounds in foods: Occurrence, mechanism and potential health effects
Yılmaz, C., & Gökmen, V. (2019) · Food Research International · doi:10.1016/j.foodres.2019.108744 · Cited by 216 · see citing works
Mind-altering with the gut: Modulation of the gut-brain axis with probiotics
Kim, N., Yun, M., Oh, Y. J., & Choi, H.-J. (2018) · Journal of Microbiology · doi:10.1007/s12275-018-8032-4 · Cited by 210 · see citing works
A gut (microbiome) feeling about the brain
Sherwin, E., Rea, K., Dinan, T. G., & Cryan, J. F. (2016) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000244 · Cited by 206 · see citing works
“A recent study by Steenbergen and colleagues [52] demonstrated that a 4-week supplementation with a probiotic composed of several”
BackgroundAntidepressive Mechanisms of Probiotics and Their Therapeutic Potential
Yong, S. J., Tong, T., Chew, J., & Lim, W. L. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01361 · Cited by 217 · see citing works
Early-life adversity and brain development: Is the microbiome a missing piece of the puzzle?
O’Mahony, S. M., Clarke, G., Dinan, T. G., & Cryan, J. F. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.068 · Cited by 203 · see citing works
Probiotic treatment reduces depressive-like behaviour in rats independently of diet
Abildgaard, A., Elfving, B., Hokland, M., Wegener, G., & Lund, S. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.02.014 · Cited by 196 · see citing works
Brain-gut-microbiota axis: challenges for translation in psychiatry
Kelly, J. R., Clarke, G. A., Cryan, J. F., & Dinan, T. G. (2016) · Annals of Epidemiology · doi:10.1016/j.annepidem.2016.02.008 · Cited by 200 · see citing works
Sundman, M., Chen, N., Subbian, V., & Chou, Y. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.05.009 · Cited by 200 · see citing works
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Communicating systems in the body: how microbiota and microglia cooperate
Erny, D., de Angelis, A. L. H., & Prinz, M. (2016) · Immunology · doi:10.1111/imm.12645 · Cited by 190 · see citing works
Harnessing Gut Microbes for Mental Health: Getting From Here to There
Bruce‐Keller, A. J., Salbaum, J. M., & Berthoud, H. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.08.014 · Cited by 188 · see citing works
Gut Microbiota and Brain Function: An Evolving Field in Neuroscience: Table 1.
Foster, J. A., Lyte, M., Meyer, E., & Cryan, J. F. (2015) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyv114 · Cited by 188 · see citing works
“Other combinations of probiotics have been shown to reduce a sad mood triggered by a psychological stimulus (Steenbergen et al., 2015) and to reduce depression anxiety and stress scales whilst modulating the hypothalamic pituitary adrenal (HPA) axis in petrochemical workers (Mohammadi et al., 2015).”
Effects of Probiotics on Cognitive Reactivity, Mood, and Sleep Quality
Marotta, A., Sarno, E., Del Casale, A., Pane, M., Mogna, L., Amoruso, A., Felis, G. E., & Fiorio, M. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00164 · Cited by 186 · see citing works
“In line with previous studies (12, 36, 37), we found a reduction in depressive mood state in the group that received the probiotics.”
BackgroundMethodResultInfluentialSteroids, stress and the gut microbiome-brain axis
Tetel, M. J., de Vries, G. J., Melcangi, R. C., Panzica, G., & O'Mahony, S. M. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12548 · Cited by 187 · see citing works
“Steenbergen and colleagues (100) showed that a multispecies probiotic reduced negative thoughts associated with sad mood, which the authors suggest supports the concept of probiotics intervention as a preventive approach for depression (100).”
The Gut-Brain Axis, the Human Gut Microbiota and Their Integration in the Development of Obesity
Bliss, E., & Whiteside, E. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00900 · Cited by 188 · see citing works
“Additionally, probiotic treatment, in particular, treatment selective for an increase in Bifidobacterium and Lactobacilli, reduces anxiety in mice with inflammatory bowel disease, enhances cognitive reactivity to depressed mood in humans and reduces depression scores in patients with irritable bowel syndrome, as well…”
BackgroundToro-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
“Even though the authors did not measure any biological markers to elucidate a possible action mechanism behind the psychobiotic effect, they did state that intestinal microbiota increase plasma tryptophan levels, facilitating serotonin turnover in the brain, which has been associated with cognitive reactivity to sad m…”
BackgroundEl 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
“, 2014, 2017) through production of neuroactive substances (Steenbergen et al., 2015; Kristensen et al., 2016).”
BackgroundAshique, S., Mohanto, S., Ahmed, M. G., Mishra, N., Garg, A., Chellappan, D. K., Omara, T., Iqbal, S., & Kahwa, I. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e34092 · Cited by 201 · see citing works
“Results show that BDNF articulation was upgraded in cortical designs lined up with further developed longer potentiation [119].”
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A review of dietary and microbial connections to depression, anxiety, and stress
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“This suggests that the probiotics or gut microbes may be a useful therapeutic option in stress-related disorders such as depression and anxiety (13, 20).”
BackgroundDo bacteria shape our development? Crosstalk between intestinal microbiota and HPA axis
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“…decreased psychological stress, anxiety, and cortisol stress reactivity (Allen et al., 2016), reduced negative thoughts associated with sad mood (Steenbergen et al., 2015), and altered brain activity and information processing of emotional material in a brain imaging study (Tillisch et al.,…”
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 186 · see citing works
“significantly reduced self-reported cognitive reactivity to sad mood in depressed individuals, thus alleviating stress-induced symptoms (Steenbergen et al., 2015).”
The link between inflammation, bugs, the intestine and the brain in alcohol dependence
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The Role of Gut Dysbiosis in the Pathophysiology of Neuropsychiatric Disorders
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The contribution of the gut microbiome to neurodevelopment and neuropsychiatric disorders
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“Similarly, when healthy male and female participants (n = 20) were administered with, either a placebo product or a mixture of several probiotics strains of Bifidobacteria and Lactobacilli over a period of 4 weeks, they exhibited substantially reduced reactivity to sad mood compared to control group [129].”
BackgroundKadosh, K. C., Muhardi, L., Parikh, P., Basso, M., Mohamed, H. J. J., Prawitasari, T., Samuel, F. O., Ma, G., & Geurts, J. M. W. (2021) · Nutrients · doi:10.3390/nu13010199 · Cited by 186 · see citing works
Gutted! Unraveling the Role of the Microbiome in Major Depressive Disorder
Bastiaanssen, T. F. S., Cussotto, S., Claesson, M. J., Clarke, G., Dinan, T. G., & Cryan, J. F. (2020) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000243 · Cited by 159 · see citing works
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“lactis W19 and W58 for 30 days reported reduced reactivity to sad mood, which was associated with reduced rumination and aggressive cognition, in the probiotic treated group compared to placebo group.(124) Fully understanding the mechanisms of microbiota-gut-brain axis communication will catalyze the development of mi…”
ResultMechanistic Insights into the Link between Gut Dysbiosis and Major Depression: An Extensive Review
Sonali, S., Ray, B., Hediyal, T. A., Rathipriya, A. G., Sunanda, T., Mahalakshmi, A. M., Rungratanawanich, W., Essa, M. M., Qoronfleh, M. W., Chidambaram, S. B., et al. (2022) · Cells · doi:10.3390/cells11081362 · Cited by 159 · see citing works
“In another study, a cocktail of probiotics, including Bifidobacterium lactis W52, Lactobacillus acidophilus W37, Bifidobacterium bifidum W23, Lactobacillus brevis W63, Lactobacillus salivarius W24, Lactobacillus casei W56, and Lactococcus lactis (W19 and W58), has shown promising results in reducing negative thoughts…”
BackgroundImpact of Environmental Pollutants on Gut Microbiome and Mental Health via the Gut–Brain Axis
Singh, S., Sharma, P., Pal, N., Kumawat, M., Shubham, S., Sarma, D. K., Tiwari, R. R., Kumar, M., & Nagpal, R. (2022) · Microorganisms · doi:10.3390/microorganisms10071457 · Cited by 157 · see citing works
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“, 2007), multi-species probiotics (Steenbergen et al., 2015), or a combination of Lactobacillus helveticus R0052 and Bifidobacterium longum R0175 (Messaoudi et al.”
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“[155] demonstrated that, after 4 weeks of probiotic supplementation, a statistically significant improvement of aggression and rumination compared to placebo was found.”
BackgroundThe Relationship Between the Gut Microbiome-Immune System-Brain Axis and Major Depressive Disorder
Foster, J. A., Baker, G. B., & Dursun, S. M. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.721126 · Cited by 153 · see citing works
A potential role for the gut microbiome in substance use disorders
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“Butyrate, in particular, is known to be a potent HDAC inhibitor, and other SCFAs such as propionate have also demonstrated HDAC inhibition (Stilling et al. 2014; Koh et al. 2016).”
Role of the intestinal microbiome, intestinal barrier and psychobiotics in depression
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Targeting gut microbiome: a novel and potential therapy for autism
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“While the present study did not examine the biological mechanisms responsible for the beneficial effects on mood, a number of hypotheses have been made, including an increase in plasma tryptophan concentrations leading to a facilitation of serotonin turnover in the brain, and an improvement in the epithelial barrier f…”
BackgroundYang, Z., Li, J., Gui, X., Shi, X., Bao, Z., Han, H., & Li, M. D. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0729-1 · Cited by 138 · see citing works
“(W19 and W58), it was found that 4-week probiotic intervention significantly reduced overall cognitive reactivity to sad mood in comparison with the participants receiving placebo [100].”
Result
- Authors
- Steenbergen, L., Sellaro, R., van Hemert, S., Bosch, J. A., & Colzato, L. S.
- Affiliations
- Leiden University (NL)
- University of Amsterdam (NL)
- Corresponding author
- Steenbergen, Laura
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2015-08
- Volume
- 48
- Pages
- 258-264
- ISSN
- 0889-1591 (ISSN-L)
- OpenAlex
- W1978433534
- Cited by
- 671
- References
- 80
- Citations by year
- 2026: 26 · 2025: 44 · 2024: 58 · 2023: 52 · 2022: 73 · 2021: 72 · 2020: 88 · 2019: 68 · 2018: 65 · 2017: 59 · 2016: 51 · 2015: 15
- FWCI
- 84.76
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Brain Behavior and Immunity (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Leiden Repository (Leiden University) (submittedVersion)
- UvA-DARE (University of Amsterdam) (submittedVersion, cc-by-nc-nd)
- Padua Research Archive (University of Padova) (submittedVersion, cc-by-nc-nd)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (452-12-001)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- multispecies probiotics, depression vulnerability, rumination, aggressive thoughts, Bifidobacterium bifidum, Bifidobacterium animalis subsp. lactis, Lactobacillus, Lactococcus lactis, gut microbiota, depression prevention, probiotic supplementation
- MeSH terms
- Adolescent, Affect, Bifidobacterium, Cognition, Depressive Disorder, Double-Blind Method, Female, Humans, Lactobacillus, Lactobacillus acidophilus, Male, Social Behavior, Dietary Supplements, Probiotics, Young Adult
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