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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 (465–469).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [468]
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“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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“This finding on cognitive reactivity to sad mood, a major risk factor for depression, is consistent with findings from a previous study in healthy controls (25).”
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“Probiotic intake has been shown to control emotion processing as measured by lab tests on cognitive reactivity to sad mood (using the validated ‘revised Leiden index of depression sensitivity scale’) and functional magnetic resonance imaging in midbrain, insula and somatosensory cortex on brain connectivity and emotio…”
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“Therefore, studies on microbiota modulation using pro-biotics (Steenbergen et al. 2015), prebiotics (Schmidt et al. 2015), a dietary fiber-rich diet (Cantu-Jungles, Rasmussen, and Hamaker 2019), and SCFAs supplementation in animals (sodium butyrate) have demonstrated control over inflammation,…”
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BackgroundUnderstanding the host-microbe interactions using metabolic modeling
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BackgroundProbiotics in Treatment of Viral Respiratory Infections and Neuroinflammatory Disorders
Shahbazi, R., Yasavoli‐Sharahi, H., Alsadi, N., Ismail, N., & Matar, C. (2020) · Molecules · doi:10.3390/molecules25214891 · Cited by 102
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“Bifidobacterium and Lactobacillus are the main genera of bacteria that convey beneficial effects, for example, on anxiety-and depression-like behaviours (Akkasheh et al., 2016; Steenbergen et al., 2015).”
Repeated sleep disruption in mice leads to persistent shifts in the fecal microbiome and metabolome
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“A randomized, placebocontrolled trial has shown that cognitive reactivity to sad mood was considerably reduced after using multispecies probiotics for a period of 4 weeks [71].”
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“…groups: PL (93), PRlowdose (92), PRhighdose (93) Lactobacillus pentosus strain b240 (1); low-dose: 2 × 109 CFU, high dose: 2 × 1010 CFU; 1/day; tablets Behavioral: POMS↔, SF-36 ↓ Steenbergen et al. (2015) [73] NLD Sad Mood 4 40 (NR); f: 80%; age: PL→19.7 (1.7), PR→20.2 (2.4); healthy; groups: PL…”
InfluentialHow do probiotics and prebiotics function at distant sites?
Reid, G., Abrahamsson, T., Bailey, M. T., Bindels, L. B., Bubnov, R. V., Ganguli, K. A., Martoni, C., O’Neill, C. A., Savignac, H. M., Stanton, C., et al. (2017) · Beneficial Microbes · doi:10.3920/bm2016.0222 · Cited by 84
The Development of High-Quality Multispecies Probiotic Formulations: From Bench to Market
Grumet, L., Tromp, Y., & Stiegelbauer, V. (2020) · Nutrients · doi:10.3390/nu12082453 · Cited by 90
“Evidence is further substantiated by the same formulation showing positive effects on cognitive reactivity to sad mood in healthy subjects [73] and mild to moderately depressed patients [74] as well as demonstrating a significant increase in working memory performance during stress [75].”
ResultEfficacy of probiotics on anxiety-A meta-analysis of randomized controlled trials
Liu, B., He, Y., Wang, M., Liu, J., Ju, Y., Zhang, Y., Liu, T., Li, L., & Li, Q. (2018) · Depression and Anxiety · doi:10.1002/da.22811 · Cited by 81
The brain-gut-microbiota interplay in depression: A key to design innovative therapeutic approaches
Varesi, A., Campagnoli, L. I. M., Chirumbolo, S., Candiano, B., Carrara, A., Ricevuti, G., Esposito, C., & Pascale, A. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2023.106799 · Cited by 88
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“…probiotic supplement, Bifidobacterium bifidum W23, Bifidobacterium lactis W52, Lactobacillus acidophilus W37, Lactobacillus brevis W63, Lactobacillus casei W56, Lactobacillus salivarius W24, Lactococcus lactis (W19 and W58) 2.5 × 10 9 CFU/g Reduced susceptibility to lowered mood states [171].”
BackgroundInfluentialRudzki, L., & Szulc, A. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00205 · Cited by 80
Eskandarzadeh, S., Effatpanah, M., Khosravi‐Darani, K., Askari, R., Hosseini, A. F., Reisian, M., & Jazayeri, S. (2019) · Nutritional Neuroscience · doi:10.1080/1028415x.2019.1598669 · Cited by 83
Gut-brain axis: A matter of concern in neuropsychiatric disorders…!
Naveed, M., Zhou, Q.-G., Chu, X., Taleb, A., Meng, F. J., Ahmed, B., Zhang, Y., Fukunaga, K., & Han, F. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110051 · Cited by 82
A biological framework for emotional dysregulation in alcohol misuse: from gut to brain
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“Indeed, recent studies showed that special multi-species probiotics were able to improve negative cognitive reactions to stressful situations [45] and that the administration of probiotics in healthy people led to a reduction in depressive and anxiety symptoms [46].”
BackgroundJohnstone, N., Milesi, C., Burn, O., van den Bogert, B., Nauta, A., Hart, K. H., Sowden, P. T., Burnet, P. W. J., & Kadosh, K. C. (2021) · Scientific Reports · doi:10.1038/s41598-021-87865-w · Cited by 88
The gut microbiome in disorders of gut–brain interaction
Kraïmi, N., Ross, T., Pujo, J., & Palma, G. D. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2360233 · Cited by 93
Microbiome and Mental Health, Specifically as It Relates to Adolescents
Simkin, D. R. (2019) · Current Psychiatry Reports · doi:10.1007/s11920-019-1075-3 · Cited by 82
Systems-level metabolism of the altered Schaedler flora, a complete gut microbiota
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“, 2015), emotional health (Steenbergen et al., 2015) and other relevant systems (Cho and Blaser, 2012) to the microbiome.”
Gut–Brain Axis in Regulation of Blood Pressure
Yang, T., & Zubcevic, J. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00845 · Cited by 74
“…GI-derived GABA may be able to diffuse into circulation and cross the BBB (Takanaga et al., 2001; Steenbergen et al., 2015a); and (ii) GI-derived GABA can be sensed by GABA receptors within the ENS, which directly communicates with vagal afferents (Auteri et al., 2015; Steenbergen et al., 2015b).”
BackgroundMicrobiome in brain function and mental health
Kennedy, P. J., Murphy, A., Cryan, J. F., Ross, R. P., Dinan, T. G., & Stanton, C. (2016) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2016.05.001 · Cited by 81
Ramalho, J. B., Soares, M. B., Spiazzi, C. C., Bicca, D. F., Soares, V. M., Pereira, J. G., da Silva, W. P., Sehn, C. P., & Cibin, F. W. S. (2019) · Nutrients · doi:10.3390/nu11040901 · Cited by 72
Emotional well-being and gut microbiome profiles by enterotype
Lee, S., Yoon, S.-H., Jung, Y., Kim, N., Min, U.-G., Chun, J., & Choi, I. (2020) · Scientific Reports · doi:10.1038/s41598-020-77673-z · Cited by 75
Kuijer, E. J., & Steenbergen, L. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105296 · Cited by 76
“3 antibiotics-induced) have been established in rodents with evidence of positive translation to humans (Sarkar et al., 2016; Steenbergen et al., 2015; H. Wang et al., 2016).”
Self-citationRole of probiotics and prebiotics in mitigation of different diseases
Manzoor, S., Wani, S. M., Mir, S. A., & Rizwan, D. (2022) · Nutrition · doi:10.1016/j.nut.2022.111602 · Cited by 79
Ganci, M., Suleyman, E., Butt, H., & Ball, M. (2019) · Brain and Behavior · doi:10.1002/brb3.1408 · Cited by 75
Bifidobacterium: a probiotic for the prevention and treatment of depression
Li, J., Wang, J., Wang, M., Zheng, L., Cen, Q., Wang, F., Li, Z., Pang, R., & Zhang, A. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1174800 · Cited by 75
“Bifidobacterium bifidum W23 Bifidobacterium lactis W52 Lactobacillus acidophilus W37 Lactobacillus brevis W63 Lactobacillus casei W56 Lactobacillus salivarius W24 Lactococcus lactis (W19 and W58) (Steenbergen et al., 2015) Healthy adults 5 × 109 CFU 4 weeks Reduced overall cognitive reactivity to depression and in par…”
BackgroundInfluentialDairy probiotics: Beyond the role of promoting gut and immune health
Ζουμποπούλου, Γ., Pot, B., Tsakalidou, E., & Papadimitriou, K. (2016) · International Dairy Journal · doi:10.1016/j.idairyj.2016.09.010 · Cited by 74
Role of Probiotics and Diet in the Management of Neurological Diseases and Mood States: A Review
Thangaleela, S., Sivamaruthi, B. S., Kesika, P., & Chaiyasut, C. (2022) · Microorganisms · doi:10.3390/microorganisms10112268 · Cited by 73
Probiotic-fortified fruit juices: Health benefits, challenges, and future perspective
Naseem, Z., Mir, S. A., Wani, S. M., Rouf, M. A., Bashir, I., & Zehra, A. (2023) · Nutrition · doi:10.1016/j.nut.2023.112154 · Cited by 76
Animal inflammation-based models of depression and their application to drug discovery
Ma, L., Demin, K. A., Kolesnikova, T. O., Kharsko, S. L., Zhu, X., Yuan, X., Song, C., Мешалкина, Д. А., Leonard, B. E., Tian, L., et al. (2017) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2017.1362385 · Cited by 71
Neuromicrobiology: How Microbes Influence the Brain
de la Fuente‐Núñez, C., Meneguetti, B. T., Franco, O. L., & Lu, T. K. (2017) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.7b00373 · Cited by 75
Niccolai, E., Boem, F., Russo, E., & Amedei, A. (2019) · Nutrients · doi:10.3390/nu11010156 · Cited by 70
Lactic acid bacteria as probiotics in sustainable development of aquaculture
ЧИЖАЕВА, А. В., Amangeldi, A., Oleinikova, Y., АЛЫБАЕВА, А. Ж., & САДАНОВ, А. К. (2022) · Aquatic Living Resources · doi:10.1051/alr/2022011 · Cited by 67
“Probiotics are definedas livingnon-pathogenicmicroorganisms thatbenefit the host when administered in adequate quantities (Steenbergen et al., 2015; Marco et al., 2021).”
BackgroundThe Impact of Microbiota-Gut-Brain Axis on Diabetic Cognition Impairment
Xu, Y., Zhou, H., & Zhu, Q. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00106 · Cited by 67
“Reports revealed that LPS can stimulate the activation of inflammatory cells (Steenbergen et al., 2015).”
BackgroundSalami, M. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.613120 · Cited by 67
“Indeed, in most, if not all, of human researches, dietary measures are not considered while synergic effect of probiotics with other effective constituents (such as unknown fermented food or substances with symbiotic roles) cannot be ignored (Steenbergen et al., 2015).”
BackgroundLeyrolle, Q., Cserjési, R., Mulders, M. D. G. H., Zamariola, G., Hiel, S., Gianfrancesco, M. A., Portheault, D., Amadieu, C., Bindels, L. B., Leclercq, S., et al. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.01.014 · Cited by 68
“Treatment of healthy volunteers or IBS patients with bacteria of these 92 two genera alone or in combination led to beneficial effects on mood (Allen et al., 2016; Pinto93 Sanchez et al., 2017; Steenbergen et al., 2015).”
BackgroundMedicinal Plants and Their Impact on the Gut Microbiome in Mental Health: A Systematic Review
Pferschy‐Wenzig, E., Pausan, M.-R., Ardjomand-Woelkart, K., Röck, S., Ammar, R. M., Kelber, O., Moissl‐Eichinger, C., & Bauer, R. (2022) · Nutrients · doi:10.3390/nu14102111 · Cited by 73
“Moreover, a randomized, placebo-controlled trial of a multispecies probiotic in 40 participants found significant changes in mood, such as reduced sad mood and aggressive thoughts [51].”
BackgroundThe Role of Probiotics and Their Metabolites in the Treatment of Depression
Jach, M. E., Serefko, A., Szopa, A., Sajnaga, E., Golczyk, H., Santos, L. S., Borowicz, K. K., & Sieniawska, E. (2023) · Molecules · doi:10.3390/molecules28073213 · Cited by 75
Metadata
- 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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