Effect of Probiotics on Psychiatric Symptoms and Central Nervous System Functions in Human Health and Disease: A Systematic Review and Meta-Analysis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Literature Information Sources and Search Strategy
2.2. Eligibility Criteria
2.3. Study Selection, Data Collection and Organization
- Group 1—Probiotics and Depression
- Group 2—Probiotics and Anxiety
- Group 3—Probiotics and Stress
- Group 4—Probiotics and Cognitive Function
- Group 5—Probiotics and Mental Health and Mood
- Group 6—Probiotics and other CNS states
2.4. Data Items and Statistics
2.5. Risk of Bias
3. Results
3.1. Study Selection and Categorization
3.2. Summary of Study Characteristics
3.3. Summary of Study Outcomes
3.3.1. Mood States and Stress
3.3.2. Anxiety, Depression and Psychiatric Distress
3.3.3. Central Nervous System (CNS) Findings in EEG and Brain Imaging
3.4. Risk of Bias
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- The Lancet Global, H. Mental health matters. Lancet Glob. Health 2020, 8, e1352. [Google Scholar] [CrossRef]
- Clarke, D.M.; Currie, K.C. Depression, anxiety and their relationship with chronic diseases: A review of the epidemiology, risk and treatment evidence. Med. J. Aust. 2009, 190, S54–S60. [Google Scholar] [CrossRef] [PubMed]
- Cryan, J.F.; O’Riordan, K.J.; Sandhu, K.; Peterson, V.; Dinan, T.G. The gut microbiome in neurological disorders. Lancet Neurol. 2020, 19, 179–194. [Google Scholar] [CrossRef]
- Thursby, E.; Juge, N. Introduction to the human gut microbiota. Biochem. J. 2017, 474, 1823–1836. [Google Scholar] [CrossRef] [PubMed]
- Caso, J.R.; MacDowell, K.S.; González-Pinto, A.; García, S.; de Diego-Adeliño, J.; Carceller-Sindreu, M.; Sarramea, F.; Caballero-Villarraso, J.; Gracia-García, P.; De la Cámara, C.; et al. Gut microbiota, innate immune pathways, and inflammatory control mechanisms in patients with major depressive disorder. Transl. Psychiatry 2021, 11, 645. [Google Scholar] [CrossRef] [PubMed]
- Rajoka, M.S.R.; Mehwish, H.M.; Kitazawa, H.; Barba, F.J.; Berthelot, L.; Umair, M.; Zhu, Q.; He, Z.; Zhao, L. Techno-functional properties and immunomodulatory potential of exopolysaccharide from Lactiplantibacillus plantarum MM89 isolated from human breast milk. Food Chem. 2021, 377, 131954. [Google Scholar] [CrossRef] [PubMed]
- Carding, S.; Verbeke, K.; Vipond, D.T.; Corfe, B.M.; Owen, L.J. Dysbiosis of the gut microbiota in disease. Microb. Ecol. Health Dis. 2015, 26, 26191. [Google Scholar] [CrossRef] [PubMed]
- Sekirov, I.; Russell, S.L.; Antunes, L.C.M.; Finlay, B.B. Gut Microbiota in Health and Disease. Physiol. Rev. 2010, 90, 859–904. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, H.; Lee, I.S.; Braun, C.; Enck, P. Effect of Probiotics on Central Nervous System Functions in Animals and Humans: A Systematic Review. J. Neurogastroenterol. Motil. 2016, 22, 589–605. [Google Scholar] [CrossRef] [PubMed]
- Dinan, T.G.; Cryan, J.F. Brain-Gut-Microbiota Axis and Mental Health. Psychosom. Med. 2017, 79, 920–926. [Google Scholar] [CrossRef] [PubMed]
- Socała, K.; Doboszewska, U.; Szopa, A.; Serefko, A.; Włodarczyk, M.; Zielińska, A.; Poleszak, E.; Fichna, J.; Wlaź, P. The role of microbiota-gut-brain axis in neuropsychiatric and neurological disorders. Pharmacol. Res. 2021, 172, 105840. [Google Scholar] [CrossRef]
- Mack, I.; Schwille-Kiuntke, J.; Mazurak, N.; Niesler, B.; Zimmermann, K.; Mönnikes, H.; Enck, P. A Nonviable Probiotic in Irritable Bowel Syndrome: A Randomized, Double-Blind, Placebo-Controlled, Multicenter Study. Clin. Gastroenterol. Hepatol. 2021. [Google Scholar] [CrossRef]
- Akter, S.; Park, J.H.; Jung, H.K. Potential Health-Promoting Benefits of Paraprobiotics, Inactivated Probiotic Cells. J. Microbiol. Biotechnol. 2020, 30, 477–481. [Google Scholar] [CrossRef]
- Sakandar, H.A.; Zhang, H. Trends in Probiotic(s)-Fermented milks and their in vivo functionality: A review. Trends Food Sci. Technol. 2021, 110, 55–65. [Google Scholar] [CrossRef]
- Reis, D.J.; Ilardi, S.S.; Punt, S.E.W. The anxiolytic effect of probiotics: A systematic review and meta-analysis of the clinical and preclinical literature. PLoS ONE 2018, 13, e0199041. [Google Scholar] [CrossRef] [Green Version]
- Chudzik, A.; Orzyłowska, A.; Rola, R.; Stanisz, G.J. Probiotics, Prebiotics and Postbiotics on Mitigation of Depression Symptoms: Modulation of the Brain-Gut-Microbiome Axis. Biomolecules 2021, 11, 1000. [Google Scholar] [CrossRef]
- Riaz Rajoka, M.S.; Thirumdas, R.; Mehwish, H.M.; Umair, M.; Khurshid, M.; Hayat, H.F.; Phimolsiripol, Y.; Pallarés, N.; Martí-Quijal, F.J.; Barba, F.J. Role of Food Antioxidants in Modulating Gut Microbial Communities: Novel Understandings in Intestinal Oxidative Stress Damage and Their Impact on Host Health. Antioxidants 2021, 10, 1563. [Google Scholar] [CrossRef]
- Bagga, D.; Aigner, C.S.; Reichert, J.L.; Cecchetto, C.; Fischmeister, F.P.S.; Holzer, P.; Moissl-Eichinger, C.; Schöpf, V. Influence of 4-week multi-strain probiotic administration on resting-state functional connectivity in healthy volunteers. Eur. J. Nutr. 2019, 58, 1821–1827. [Google Scholar] [CrossRef] [Green Version]
- Bagga, D.; Reichert, J.L.; Koschutnig, K.; Aigner, C.S.; Holzer, P.; Koskinen, K.; Moissl-Eichinger, C.; Schöpf, V. Probiotics drive gut microbiome triggering emotional brain signatures. Gut Microbes 2018, 9, 486–496. [Google Scholar] [CrossRef]
- Papalini, S.; Michels, F.; Kohn, N.; Wegman, J.; van Hemert, S.; Roelofs, K.; Arias-Vasquez, A.; Aarts, E. Stress matters: Randomized controlled trial on the effect of probiotics on neurocognition. Neurobiol. Stress 2019, 10, 100141. [Google Scholar] [CrossRef]
- Tillisch, K.; Labus, J.; Kilpatrick, L.; Jiang, Z.; Stains, J.; Ebrat, B.; Guyonnet, D.; Legrain-Raspaud, S.; Trotin, B.; Naliboff, B.; et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 2013, 144, 1394–1401.E4. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, H.; Braun, C.; Murphy, E.F.; Enck, P. Bifidobacterium longum 1714™ Strain Modulates Brain Activity of Healthy Volunteers During Social Stress. Am. J. Gastroenterol. 2019, 114, 1152–1162. [Google Scholar] [CrossRef] [PubMed]
- 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. Probiotic Bifidobacterium longum NCC3001 Reduces Depression Scores and Alters Brain Activity: A Pilot Study in Patients With Irritable Bowel Syndrome. Gastroenterology 2017, 153, 448–459.E8. [Google Scholar] [CrossRef] [PubMed]
- Liberati, A.; Altman, D.G.; Tetzlaff, J.; Mulrow, C.; Gøtzsche, P.C.; Ioannidis, J.P.; Clarke, M.; Devereaux, P.J.; Kleijnen, J.; Moher, D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: Explanation and elaboration. BMJ 2009, 339, b2700. [Google Scholar] [CrossRef] [Green Version]
- Schardt, C.; Adams, M.B.; Owens, T.; Keitz, S.; Fontelo, P. Utilization of the PICO framework to improve searching PubMed for clinical questions. BMC Med. Inform. Decis. Mak. 2007, 7, 16. [Google Scholar] [CrossRef] [Green Version]
- Le Morvan de Sequeira, C.; Kaeber, M.; Cekin, S.E.; Enck, P.; Mack, I. The Effect of Probiotics on Quality of Life, Depression and Anxiety in Patients with Irritable Bowel Syndrome: A Systematic Review and Meta-Analysis. J. Clin. Med. 2021, 10, 3497. [Google Scholar] [CrossRef]
- DerSimonian, R.; Laird, N. Meta-analysis in clinical trials. Control. Clin. Trials 1986, 7, 177–188. [Google Scholar] [CrossRef]
- Normand, S.L. Meta-analysis: Formulating, evaluating, combining, and reporting. Stat. Med. 1999, 18, 321–359. [Google Scholar] [CrossRef]
- Review Manager (RevMan), Version 5.4; The Cochrane Collaboration: London, UK, 2020.
- Eskandarzadeh, S.; Effatpanah, M.; Khosravi-Darani, K.; Askari, R.; Hosseini, A.F.; Reisian, M.; Jazayeri, S. Efficacy of a multispecies probiotic as adjunctive therapy in generalized anxiety disorder: A double blind, randomized, placebo-controlled trial. Nutr. Neurosci. 2021, 24, 102–108. [Google Scholar] [CrossRef]
- Sterne, J.A.C.; Savović, J.; Page, M.J.; Elbers, R.G.; Blencowe, N.S.; Boutron, I.; Cates, C.J.; Cheng, H.Y.; Corbett, M.S.; Eldridge, S.M.; et al. RoB 2: A revised tool for assessing risk of bias in randomised trials. BMJ 2019, 366, l4898. [Google Scholar] [CrossRef] [Green Version]
- Akkasheh, G.; Kashani-Poor, Z.; Tajabadi-Ebrahimi, M.; Jafari, P.; Akbari, H.; Taghizadeh, M.; Memarzadeh, M.R.; Asemi, Z.; Esmaillzadeh, A. Clinical and metabolic response to probiotic administration in patients with major depressive disorder: A randomized, double-blind, placebo-controlled trial. Nutrition 2016, 32, 315–320. [Google Scholar] [CrossRef]
- Adikari, A.; Appukutty, M.; Kuan, G. Effects of Daily Probiotics Supplementation on Anxiety Induced Physiological Parameters among Competitive Football Players. Nutrients 2020, 12, 1920. [Google Scholar] [CrossRef]
- Allen, A.P.; Hutch, W.; Borre, Y.E.; Kennedy, P.J.; Temko, A.; Boylan, G.; Murphy, E.; Cryan, J.F.; Dinan, T.G.; Clarke, G. Bifidobacterium longum 1714 as a translational psychobiotic: Modulation of stress, electrophysiology and neurocognition in healthy volunteers. Transl. Psychiatry 2016, 6, e939. [Google Scholar] [CrossRef] [Green Version]
- Benton, D.; Williams, C.; Brown, A. Impact of consuming a milk drink containing a probiotic on mood and cognition. Eur. J. Clin. Nutr. 2007, 61, 355–361. [Google Scholar] [CrossRef] [Green Version]
- Chung, Y.-C.; Jin, H.-M.; Cui, Y.; Kim, D.S.; Jung, J.M.; Park, J.-I.; Jung, E.-S.; Choi, E.-K.; Chae, S.-W. Fermented milk of Lactobacillus helveticus IDCC3801 improves cognitive functioning during cognitive fatigue tests in healthy older adults. J. Funct. Foods 2014, 10, 465–474. [Google Scholar] [CrossRef]
- De Lorenzo, A.; Costacurta, M.; Merra, G.; Gualtieri, P.; Cioccoloni, G.; Marchetti, M.; Varvaras, D.; Docimo, R.; Di Renzo, L. Can psychobiotics intake modulate psychological profile and body composition of women affected by normal weight obese syndrome and obesity? A double blind randomized clinical trial. J. Transl. Med. 2017, 15, 135. [Google Scholar] [CrossRef] [Green Version]
- Dickerson, F.B.; Stallings, C.; Origoni, A.; Katsafanas, E.; Savage, C.L.; Schweinfurth, L.A.; Goga, J.; Khushalani, S.; Yolken, R.H. Effect of probiotic supplementation on schizophrenia symptoms and association with gastrointestinal functioning: A randomized, placebo-controlled trial. Prim. Care Companion CNS Disord. 2014, 16, 26294. [Google Scholar] [CrossRef] [Green Version]
- Dickerson, F.; Adamos, M.; Katsafanas, E.; Khushalani, S.; Origoni, A.; Savage, C.; Schweinfurth, L.; Stallings, C.; Sweeney, K.; Goga, J.; et al. Adjunctive probiotic microorganisms to prevent rehospitalization in patients with acute mania: A randomized controlled trial. Bipolar Disord. 2018, 20, 614–621. [Google Scholar] [CrossRef]
- Diop, L.; Guillou, S.; Durand, H. Probiotic food supplement reduces stress-induced gastrointestinal symptoms in volunteers: A double-blind, placebo-controlled, randomized trial. Nutr. Res. 2008, 28, 1–5. [Google Scholar] [CrossRef]
- Ghaderi, A.; Banafshe, H.R.; Mirhosseini, N.; Moradi, M.; Karimi, M.A.; Mehrzad, F.; Bahmani, F.; Asemi, Z. Clinical and metabolic response to vitamin D plus probiotic in schizophrenia patients. BMC Psychiatry 2019, 19, 77. [Google Scholar] [CrossRef] [Green Version]
- Gualtieri, P.; Marchetti, M.; Cioccoloni, G.; De Lorenzo, A.; Romano, L.; Cammarano, A.; Colica, C.; Condò, R.; Di Renzo, L. Psychobiotics Regulate the Anxiety Symptoms in Carriers of Allele A of IL-1β Gene: A Randomized, Placebo-Controlled Clinical Trial. Mediat. Inflamm. 2020, 2020, 2346126. [Google Scholar] [CrossRef] [Green Version]
- Ho, Y.T.; Tsai, Y.C.; Kuo, T.B.J.; Yang, C.C.H. Effects of Lactobacillus plantarum PS128 on Depressive Symptoms and Sleep Quality in Self-Reported Insomniacs: A Randomized, Double-Blind, Placebo-Controlled Pilot Trial. Nutrients 2021, 13, 2820. [Google Scholar] [CrossRef]
- Hwang, Y.H.; Park, S.; Paik, J.W.; Chae, S.W.; Kim, D.H.; Jeong, D.G.; Ha, E.; Kim, M.; Hong, G.; Park, S.H.; et al. Efficacy and Safety of Lactobacillus Plantarum C29-Fermented Soybean (DW2009) in Individuals with Mild Cognitive Impairment: A 12-Week, Multi-Center, Randomized, Double-Blind, Placebo-Controlled Clinical Trial. Nutrients 2019, 11, 305. [Google Scholar] [CrossRef] [Green Version]
- Inoue, T.; Kobayashi, Y.; Mori, N.; Sakagawa, M.; Xiao, J.Z.; Moritani, T.; Sakane, N.; Nagai, N. Effect of combined bifidobacteria supplementation and resistance training on cognitive function, body composition and bowel habits of healthy elderly subjects. Benef. Microbes 2018, 9, 843–853. [Google Scholar] [CrossRef]
- Karbownik, M.S.; Kręczyńska, J.; Kwarta, P.; Cybula, M.; Wiktorowska-Owczarek, A.; Kowalczyk, E.; Pietras, T.; Szemraj, J. Effect of Supplementation with Saccharomyces Boulardii on Academic Examination Performance and Related Stress in Healthy Medical Students: A Randomized, Double-Blind, Placebo-Controlled Trial. Nutrients 2020, 12, 1469. [Google Scholar] [CrossRef]
- Kato-Kataoka, A.; Nishida, K.; Takada, M.; Kawai, M.; Kikuchi-Hayakawa, H.; Suda, K.; Ishikawa, H.; Gondo, Y.; Shimizu, K.; Matsuki, T.; et al. Fermented Milk Containing Lactobacillus casei Strain Shirota Preserves the Diversity of the Gut Microbiota and Relieves Abdominal Dysfunction in Healthy Medical Students Exposed to Academic Stress. Appl. Environ. Microbiol. 2016, 82, 3649–3658. [Google Scholar] [CrossRef] [Green Version]
- Kazemi, A.; Noorbala, A.A.; Azam, K.; Eskandari, M.H.; Djafarian, K. Effect of probiotic and prebiotic vs placebo on psychological outcomes in patients with major depressive disorder: A randomized clinical trial. Clin. Nutr. 2019, 38, 522–528. [Google Scholar] [CrossRef]
- 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. Lost in translation? The potential psychobiotic Lactobacillus rhamnosus (JB-1) fails to modulate stress or cognitive performance in healthy male subjects. Brain Behav. Immun. 2017, 61, 50–59. [Google Scholar] [CrossRef]
- Kobayashi, Y.; Kuhara, T.; Oki, M.; Xiao, J.Z. Effects of Bifidobacterium breve A1 on the cognitive function of older adults with memory complaints: A randomised, double-blind, placebo-controlled trial. Benef. Microbes 2019, 10, 511–520. [Google Scholar] [CrossRef] [PubMed]
- Lew, L.C.; Hor, Y.Y.; Yusoff, N.A.A.; Choi, S.B.; Yusoff, M.S.B.; Roslan, N.S.; Ahmad, A.; Mohammad, J.A.M.; Abdullah, M.; Zakaria, N.; et al. Probiotic Lactobacillus plantarum P8 alleviated stress and anxiety while enhancing memory and cognition in stressed adults: A randomised, double-blind, placebo-controlled study. Clin. Nutr. 2019, 38, 2053–2064. [Google Scholar] [CrossRef] [PubMed]
- Messaoudi, M.; Lalonde, R.; Violle, N.; Javelot, H.; Desor, D.; Nejdi, A.; Bisson, J.F.; Rougeot, C.; Pichelin, M.; Cazaubiel, M.; et al. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br. J. Nutr. 2011, 105, 755–764. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mohammadi, A.A.; Jazayeri, S.; Khosravi-Darani, K.; Solati, Z.; Mohammadpour, N.; Asemi, Z.; Adab, Z.; Djalali, M.; Tehrani-Doost, M.; Hosseini, M.; et al. The effects of probiotics on mental health and hypothalamic-pituitary-adrenal axis: A randomized, double-blind, placebo-controlled trial in petrochemical workers. Nutr. Neurosci. 2016, 19, 387–395. [Google Scholar] [CrossRef] [PubMed]
- Murata, M.; Kondo, J.; Iwabuchi, N.; Takahashi, S.; Yamauchi, K.; Abe, F.; Miura, K. Effects of paraprobiotic Lactobacillus paracasei MCC1849 supplementation on symptoms of the common cold and mood states in healthy adults. Benef. Microbes 2018, 9, 855–864. [Google Scholar] [CrossRef] [PubMed]
- Nishida, K.; Sawada, D.; Kawai, T.; Kuwano, Y.; Fujiwara, S.; Rokutan, K. Para-psychobiotic Lactobacillus gasseri CP2305 ameliorates stress-related symptoms and sleep quality. J. Appl. Microbiol. 2017, 123, 1561–1570. [Google Scholar] [CrossRef] [Green Version]
- Nishida, K.; Sawada, D.; Kuwano, Y.; Tanaka, H.; Rokutan, K. Health Benefits of Lactobacillus gasseri CP2305 Tablets in Young Adults Exposed to Chronic Stress: A Randomized, Double-Blind, Placebo-Controlled Study. Nutrients 2019, 11, 1859. [Google Scholar] [CrossRef] [Green Version]
- Nishihira, J.; Kagami-Katsuyama, H.; Tanaka, A.; Nishimura, M.; Kobayashi, T.; Kawasaki, Y. Elevation of natural killer cell activity and alleviation of mental stress by the consumption of yogurt containing Lactobacillus gasseri SBT2055 and Bifidobacterium longum SBT2928 in a double-blind, placebo-controlled clinical trial. J. Funct. Foods 2014, 11, 261–268. [Google Scholar] [CrossRef]
- Ohsawa, K.; Nakamura, F.; Uchida, N.; Mizuno, S.; Yokogoshi, H. Lactobacillus helveticus-fermented milk containing lactononadecapeptide (NIPPLTQTPVVVPPFLQPE) improves cognitive function in healthy middle-aged adults: A randomised, double-blind, placebo-controlled trial. Int. J. Food Sci. Nutr. 2018, 69, 369–376. [Google Scholar] [CrossRef]
- Östlund-Lagerström, L.; Kihlgren, A.; Repsilber, D.; Björkstén, B.; Brummer, R.J.; Schoultz, I. Probiotic administration among free-living older adults: A double blinded, randomized, placebo-controlled clinical trial. Nutr. J. 2016, 15, 80. [Google Scholar] [CrossRef] [Green Version]
- Patterson, E.; Griffin, S.M.; Ibarra, A.; Ellsiepen, E.; Hellhammer, J. Lacticaseibacillus paracasei Lpc-37® improves psychological and physiological markers of stress and anxiety in healthy adults: A randomized, double-blind, placebo-controlled and parallel clinical trial (the Sisu study). Neurobiol. Stress 2020, 13, 100277. [Google Scholar] [CrossRef]
- Rao, A.V.; Bested, A.C.; Beaulne, T.M.; Katzman, M.A.; Iorio, C.; Berardi, J.M.; Logan, A.C. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathog. 2009, 1, 6. [Google Scholar] [CrossRef] [Green Version]
- Raygan, F.; Ostadmohammadi, V.; Bahmani, F.; Asemi, Z. The effects of vitamin D and probiotic co-supplementation on mental health parameters and metabolic status in type 2 diabetic patients with coronary heart disease: A randomized, double-blind, placebo-controlled trial. Prog. Neuropsychopharmacol. Biol. Psychiatry 2018, 84, 50–55. [Google Scholar] [CrossRef]
- Raygan, F.; Ostadmohammadi, V.; Asemi, Z. The effects of probiotic and selenium co-supplementation on mental health parameters and metabolic profiles in type 2 diabetic patients with coronary heart disease: A randomized, double-blind, placebo-controlled trial. Clin. Nutr. 2019, 38, 1594–1598. [Google Scholar] [CrossRef]
- Reininghaus, E.Z.; Platzer, M.; Kohlhammer-Dohr, A.; Hamm, C.; Mörkl, S.; Bengesser, S.A.; Fellendorf, F.T.; Lahousen-Luxenberger, T.; Leitner-Afschar, B.; Schöggl, H.; et al. PROVIT: Supplementary Probiotic Treatment and Vitamin B7 in Depression-A Randomized Controlled Trial. Nutrients 2020, 12, 3422. [Google Scholar] [CrossRef]
- Roman, P.; Estévez, A.F.; Miras, A.; Sánchez-Labraca, N.; Cañadas, F.; Vivas, A.B.; Cardona, D. A Pilot Randomized Controlled Trial to Explore Cognitive and Emotional Effects of Probiotics in Fibromyalgia. Sci. Rep. 2018, 8, 10965. [Google Scholar] [CrossRef]
- Romijn, A.R.; Rucklidge, J.J.; Kuijer, R.G.; Frampton, C. A double-blind, randomized, placebo-controlled trial of Lactobacillus helveticus and Bifidobacterium longum for the symptoms of depression. Aust. N. Z. J. Psychiatry 2017, 51, 810–821. [Google Scholar] [CrossRef] [Green Version]
- Rudzki, L.; Ostrowska, L.; Pawlak, D.; Małus, A.; Pawlak, K.; Waszkiewicz, N.; Szulc, A. Probiotic Lactobacillus Plantarum 299v decreases kynurenine concentration and improves cognitive functions in patients with major depression: A double-blind, randomized, placebo controlled study. Psychoneuroendocrinology 2019, 100, 213–222. [Google Scholar] [CrossRef]
- Sanchez, M.; Darimont, C.; Panahi, S.; Drapeau, V.; Marette, A.; Taylor, V.H.; Doré, J.; Tremblay, A. Effects of a Diet-Based Weight-Reducing Program with Probiotic Supplementation on Satiety Efficiency, Eating Behaviour Traits, and Psychosocial Behaviours in Obese Individuals. Nutrients 2017, 9, 284. [Google Scholar] [CrossRef]
- Sashihara, T.; Nagata, M.; Mori, T.; Ikegami, S.; Gotoh, M.; Okubo, K.; Uchida, M.; Itoh, H. Effects of Lactobacillus gasseri OLL2809 and α-lactalbumin on university-student athletes: A randomized, double-blind, placebo-controlled clinical trial. Appl. Physiol. Nutr. Metab. 2013, 38, 1228–1235. [Google Scholar] [CrossRef]
- Sawada, D.; Kawai, T.; Nishida, K.; Kuwano, Y.; Fujiwara, S.; Rokutan, K. Daily intake of Lactobacillus gasseri CP2305 improves mental, physical, and sleep quality among Japanese medical students enrolled in a cadaver dissection course. J. Funct. Foods 2017, 31, 188–197. [Google Scholar] [CrossRef]
- Severance, E.G.; Gressitt, K.L.; Stallings, C.R.; Katsafanas, E.; Schweinfurth, L.A.; Savage, C.L.G.; Adamos, M.B.; Sweeney, K.M.; Origoni, A.E.; Khushalani, S.; et al. Probiotic normalization of Candida albicans in schizophrenia: A randomized, placebo-controlled, longitudinal pilot study. Brain Behav. Immun. 2017, 62, 41–45. [Google Scholar] [CrossRef] [Green Version]
- Shinkai, S.; Toba, M.; Saito, T.; Sato, I.; Tsubouchi, M.; Taira, K.; Kakumoto, K.; Inamatsu, T.; Yoshida, H.; Fujiwara, Y.; et al. Immunoprotective effects of oral intake of heat-killed Lactobacillus pentosus strain b240 in elderly adults: A randomised, double-blind, placebo-controlled trial. Br. J. Nutr. 2013, 109, 1856–1865. [Google Scholar] [CrossRef] [Green Version]
- Steenbergen, L.; Sellaro, R.; van Hemert, S.; Bosch, J.A.; Colzato, L.S. A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain Behav. Immun. 2015, 48, 258–264. [Google Scholar] [CrossRef] [Green Version]
- Takada, M.; Nishida, K.; Kataoka-Kato, A.; Gondo, Y.; Ishikawa, H.; Suda, K.; Kawai, M.; Hoshi, R.; Watanabe, O.; Igarashi, T.; et al. Probiotic Lactobacillus casei strain Shirota relieves stress-associated symptoms by modulating the gut-brain interaction in human and animal models. Neurogastroenterol. Motil. 2016, 28, 1027–1036. [Google Scholar] [CrossRef] [Green Version]
- Takada, M.; Nishida, K.; Gondo, Y.; Kikuchi-Hayakawa, H.; Ishikawa, H.; Suda, K.; Kawai, M.; Hoshi, R.; Kuwano, Y.; Miyazaki, K.; et al. Beneficial effects of Lactobacillus casei strain Shirota on academic stress-induced sleep disturbance in healthy adults: A double-blind, randomised, placebo-controlled trial. Benef. Microbes 2017, 8, 153–162. [Google Scholar] [CrossRef]
- Tran, N.; Zhebrak, M.; Yacoub, C.; Pelletier, J.; Hawley, D. The gut-brain relationship: Investigating the effect of multispecies probiotics on anxiety in a randomized placebo-controlled trial of healthy young adults. J. Affect. Disord. 2019, 252, 271–277. [Google Scholar] [CrossRef]
- Xiao, J.; Katsumata, N.; Bernier, F.; Ohno, K.; Yamauchi, Y.; Odamaki, T.; Yoshikawa, K.; Ito, K.; Kaneko, T. Probiotic Bifidobacterium breve in Improving Cognitive Functions of Older Adults with Suspected Mild Cognitive Impairment: A Randomized, Double-Blind, Placebo-Controlled Trial. J. Alzheimers Dis. 2020, 77, 139–147. [Google Scholar] [CrossRef]
- Yamamura, S.; Morishima, H.; Kumano-go, T.; Suganuma, N.; Matsumoto, H.; Adachi, H.; Sigedo, Y.; Mikami, A.; Kai, T.; Masuyama, A.; et al. The effect of Lactobacillus helveticus fermented milk on sleep and health perception in elderly subjects. Eur. J. Clin. Nutr. 2009, 63, 100–105. [Google Scholar] [CrossRef]
- Zhang, X.; Chen, S.; Zhang, M.; Ren, F.; Ren, Y.; Li, Y.; Liu, N.; Zhang, Y.; Zhang, Q.; Wang, R. Effects of Fermented Milk Containing Lacticaseibacillus paracasei Strain Shirota on Constipation in Patients with Depression: A Randomized, Double-Blind, Placebo-Controlled Trial. Nutrients 2021, 13, 2238. [Google Scholar] [CrossRef]
- Preidis, G.A.; Weizman, A.V.; Kashyap, P.C.; Morgan, R.L. AGA Technical Review on the Role of Probiotics in the Management of Gastrointestinal Disorders. Gastroenterology 2020, 159, 708–738.E4. [Google Scholar] [CrossRef]
- Mazurak, N.; Broelz, E.; Storr, M.; Enck, P. Probiotic Therapy of the Irritable Bowel Syndrome: Why Is the Evidence Still Poor and What Can Be Done About It? J. Neurogastroenterol. Motil. 2015, 21, 471–485. [Google Scholar] [CrossRef] [Green Version]
- O’Toole, P.W.; Marchesi, J.R.; Hill, C. Next-generation probiotics: The spectrum from probiotics to live biotherapeutics. Nat. Microbiol. 2017, 2, 17057. [Google Scholar] [CrossRef] [PubMed]
Author (Year) | Country | Subject | Intake Length (Week) | SampleSize (A); Sex (f%); AgeMean (SD); HealthCondition; Groups (N) | Probiotic Species (N); Dose; Times Intake per Day; Application | Outcomes |
---|---|---|---|---|---|---|
Akkasheh et al. (2016) [32] | IRN | Depression | 8 | 40 (40); f: 85%; age: PL→36.2 (8.2), PR→38.3 (12.1); MDD; groups: PL (20), PR (20) | Tak Gen Zist Pharmaceutical Company (3); each 2 × 109 CFU/g; 1/day; capsule | Behavioral: BDI ↓ |
Adikari et al. (2020) [33] | MYS | Anxiety | 8 | 20 (19); f: 0%; age: PL→19 ± 0.66, PR→19 ± 0.81; healthy; groups: PL (9), PR (10) | Lactobacillus casei Shirota (1); 3 × 1010 CFU; 1/day; liquid | Neuropsychological: DVT reaction time ↓, accuracy percentage ↔ Neurophysiological: EEG ↔ (week 8), ↑ theta brain wave + delta brain wave for probiotic group (week 4); EDR ↔ |
Allen et al. (2016) [34] | IRL | Stress | 8 | 27 (22); f: 0%; age: 25.5 (1.2); healthy; RCT Crossover : 4 weeks placebo, 4 weeks probiotics, no washout | Bifidobacterium longum 1714 (1); 1 × 109 CFU; 1/day; powder | Behavioral: Cohen PSS: ↓; STAI: ↔ Neuropsychological: PAL (total errors): ↔ Neurophysiological: EEG Mobility ↑, Cz theta power ↓ |
Bagga et al. (2018) [19] | AUT | Emotional brain signatures | 4 | 45 (NR); f: 48.9%; age: PL→27.25 (5.78), PR→28.27 (4.2), NI→26.87 (4.97); healthy; groups: PL (15), PR (15), NI (15) | Ecologic 825 by Winclove Probiotics (9); 7.5 × 109 CFU/g; 1/day; powder | Behavioral: Post-hoc comparisons: PANAS ↑↑; SCL-90 ↔; ADS ↔; LEIDS: Subscales hopelessness ↓↓ and risk aversion ↓; PRP with less decision change for unpleasant stimuli ↑↑ RAU (response accuracy for unpleasant stimuli) Neurophysiological: fMRI BOLD contrast correlated with PANAS positive score ↑; Emotional decision-making task (neutral > baseline) contrast: significant differences (p value NR) in brain activity in left anterior cingulum compared to NI |
Bagga et al. (2019) [18] | AUT | Functional connectivity in brain | 4 | 45 (NR); f: 51.1%; age: 26.24 (4.76); healthy; groups: PL (15), PR (15), CN (15) | Ecologic 825 by Winclove Probiotics (9); 7.5 × 106 CFU/g; 1/day; powder | Neurophysiological: significant changes in the functional connectivity (FC) comparing PRP with CON and PLP comparing to CON: ↑ Salience network in Cingulate gyrus + Precuneus cortex), ↓ Middle and superior frontal gyrus network in Frontal pole + Frontal medial cortex; comparing to PLP: ↓ Visual network in Postcentral gyrus + Precuneus and Default mode network in Frontal pole, Superior frontal gyrus + Paracingulate gyrus probiotic intervention did not influence the structural connectivity |
Benton et al. (2007) [35] | UK | Mood and Cognition | 3 | 132 (126); f: 59.52%; age: 61.8 ± 7.3; healthy; groups: NR | Lactobacillus casei Shirota (1); 6.5 × 109 CFU; 1/day; liquid | Behavioral: POMS: ↔ Neuropsychological: Memory: Wechsler Memory scale, Retrieval from long-term memory, Test of verbal fluency: ↔; NART: converted to Z scores: ↔ |
Chung et al. (2014) [36] | KOR | Cognitive Fatigue | 12 | 39 (36); f: 44.4%; age: 65.00 ± 4.14; >24 in MMSE-K; groups: PL (10), LHFM 500 mg (10), LHFM 1000 mg (7), LHFM 2000 mg (9) | Lactobacillus helveticus IDCC3801 (1); dose NR; 4/day; tablet | Behavioral: PSS ↔, GDS-SF ↔ Neuropsychological: DST, SRL, VLT, Serial 3 s and 7 s: ↔, RVIP: 1000 mg ↑ correct responses (post-hoc), ST: error responses 500 mg ↓ |
De Lorenzo et al. (2017) [37] | ITA | Psychological Profile | 3 | 48 (48); f: 100%; age: NWL30.18 ± 2.04, NWO: 40.00 ± 12.54, PreobOB: 33.57 ± 10.57; healthy; groups: PL (24), PR (24); RCT Crossover: 3 weeks intervention, 3 weeks wash-out, 3 weeks other intervention | Biocult Strong, HOMEOSYN (9); each 1.5 × 1010 CFU/3 g; 1/day; powder | Behavioral: SCL90R: ↔; BUT ↓ (S) |
Dickerson et al. (2014) [38] | USA | Schizophrenia | 14 | 65 (65); f: 35.4%; age: PL→48.1 (9.4), PR→44.4 (11.0); diagnosed schizophrenia with antipsychotic medication; groups: PL (32), PR (33) | Bifiform Balance (2); each 109 CFU; 1/day; tablet | Behavioral: PANSS ↔ |
Dickerson et al. (2018) [39] | USA | Acute Mania | 24 | 66 (66); f: 63.6%; age: PL→33.3 (±13.3), PR→37.9 (±11.7); maniac episode; groups: PL (33), PR (33) | Chr. Hansen (2); >108 CFU; 1/day; tablet | Behavioral: YMRS, MADRS, BPRS ↔ |
Diop et al. (2008) [40] | FRA | Stress | 3 | 75 (75); f: 72%; age: 38 ± 11; healthy; groups: PL (37), PR (38) | Probio stick (2); 3 × 109 CFU; 1/day; powder | Behavioral: Questionnaire assessing stress-induced symptoms (62 items) VAS 10 cm: ↓ abdominal pain, ↓ nausea/vomiting |
Eskandarzadeh et al. (2021) [30] | IRN | Generalized Anxiety Disorder | 8 | 48 (39); f: 81.25%; age: PL→33.67 ± 6.56, PR→34.17 ± 6.14; GAD-7 score > 7; groups: PL (24), PR (24); Intake with sertraline in both groups | Takgene Zist Company (4); 1.8 × 1010 CFU; 1/day; capsule | Behavioral: HAM-A ↓↓, State-Anxiety score ↓, Trait-Anxiety score ↔, BAI ↔, WHO-QOL-BREF ↔ |
Ghaderi et al. (2019) [41] | IRN | Schizophrenia | 12 | 60 (60); f: 6.7%; age: PL→43.2 ± 6.0, PR→44.8 ± 8.3; diagnosed schizophrenia; groups: PL (30), PR (30); probiotic group within take of 50,000 IU of Vitamin D3 every 2 weeks | Lacto Care (4); each 2 × 109 CFU; 1/day; capsule | Behavioral: PANSS ↓↓ in general and total subscore Neuropsychological: BPRS ↔ |
Gualtieri et al. (2020) [42] | ITA | Anxiety | 12 | 142 (97); f: 61.9%; age: 41.29 (±14.9); healthy; groups: PL (71), PR (71) | Biocult Strong, HOMEOSYN (9); each 1.5 × 1010 CFU/3 g; 1/day; powder | Behavioral: HAM-A↓↓ (especially ↓ in IL-1β rs16944 carriers than in non-carrier), BUT ↔, SCL-90 ↔ |
Ho et al. (2021) [43] | TWN | Depression | 4 (30 days) | 40 (40); f: 67.5%; age: PL→25.47 ± 4.64, PR→26.43 ± 5.95; PSQI > 5, ISI > 13; and met the DSM-5 criteria for chronic primary insomnia; group: PL (19), PR (21) | Lactobacillus plantarum PS128 (1); 3 × 1010 CFU; 2/day; capsule | Behavioral: BDI-II ↓, BAI ↔, PSQI ↔, ISI ↔, ESS ↔, VAS fatigued before sleep ↓↓ Neurophysiological: sleep EEG ↔ (During N1: theta power % ↓ at day 15) |
Hwang et al. (2019) [44] | KOR | Mild Cognitive Impairment | 12 | 100 (100); f: 66%; age: PL→69.2 (7.00), PR→68.0 (5.12); healthy with MCI; groups: PL (50), PR (50) | DW2009 Lactobacillus plantarum C29 (1); 1.25 × 1010 CFU/g; 1/day; 2 capsules (800 mg) | Neuropsychological: VLT, ACPT, DST: ↑ combined cognitive function (subscore: Attention/Prefrontal function ↑ in composite score) |
Inoue et al. (2018) [45] | JAP | Cognitive Function | 12 | 39 (38); f: 64.1%; age: 70.3 (±3.1); healthy; groups: PL (19), PR (20); intake with physical training | Morinaga Milk Industry Co., Ltd. (4); each 1.25 × 1010 CFU; 1/day; powder | Behavioral: PHQ-9 ↔, GAD-7 ↔ Neuropsychological: MoCA-J ↔ |
Karbownik et al. (2020) [46] | POL | Stress | 4 | 92 (92); f: 60%; age: 22.6 ± 1.3; healthy; groups: PL (29), PR-Lactobacillus (32), PR-Saccharomyces (31) | LacidoEnter (1): 5 × 109; Dicoflor 60 (1): 6 × 109; 1/day; capsule | Behavioral: STAI ↔ Neuropsychological: Performance in Academic Examination ↔ |
Kato-Kataoka et al. (2016) [47] | JAP | Stress | 8 | 49 (47); f: 44.9%; age: PL→22.8 (±0.3), PR→22.8 (±0.4); healthy; groups: PL (25), PR (24) | L.casei strain Shirota YIT 9029 (1); 1.0 × 1011 CFU; 1/day; liquid | Behavioral: feelings of stress by 100 mm VAS ↓, STAI ↔, NEO-FFI ↔ |
Kazemi et al. (2019) [48] | IRN | Depression | 8 | 110 (110); f: 70.9%; age: 36.47 (8.03); mild to moderate major depression; groups: PL (36), PR (38), PRE (36) | Lallemand Health Solution (2); >10 × 109 CFU; 1/day; powder | Behavioral: BDI ↓ |
Kelly et al. (2017) [49] | IRL | Stress and Cognitive Performance | 8 | 29 (NR); f: 0%; age: 24.59 (0.75); healthy; groups: PL-PR (15), PR-PL (14); RCT Crossover: switch of treatment after 4 weeks, no washout | Lactobacillus rhamnosus (JB-1) (1); 1 × 109 CFU; 1/day; capsule | Behavioral: BDI, BAI, PSS, STAI, SCL-90, PSQI, CCL: ↔ Neuropsychological: Test from CANTAB battery ↔; SECPT ↔ Neurophysiological: EEG ↔ |
Kobayashi et al. (2019) [50] | JAP | Memory | 12 | 121 (117); f: 50.4%; age: PL→61.6 (6.37), PR→61.5 (6.83); subjective memory complaints and MMSE score 22–27; groups: PL (60), PR (61) | Bifidobacterium breve A1 (1); >1 × 1010 CFU; 1/day; capsule | Neuropsychological: RBANS ↔, MMSE ↔ |
Lew et al. (2019) [51] | MYS | Stress, Anxiety, Memory, Cognition | 12 | 132 (103); f: 76.7%; age: PL→32.1 ± 11.4, PR→31.3 ± 10.8; healthy with score of moderate stress level on PSS-10; groups: PL (51), PR (52) | Lactobacillus plantarum P8 (1); 2 × 1010 CFU; 1/day; powder | Behavioral: PSS-10: ↔; DASS-42 total: ↓ week 4 + 12; DASS-42 stress: ↓ week 4, 8, 12; DASS-42 anxiety: ↓ week 4, 12; DASS-42 depression ↔ Neuropsychological: CBB speed for social emotional cognition (in women) ↓↓; international shopping list memory test ↑ |
Messaoudi et al. (2011) [52] | FRA | Anxiety, depression, stress and coping | 4 (30 days) | 55 (55); f: 74.5%; age: PL→43.2 (8.5), PR→42.4 (7.5); score of <12 in the HADS-anxiety subscale and the HADS-depression subscale; groups: PL (29), PR (26) | Institut Rosell-Lallemand (2); 3 × 109 CFU; 1/day; powder | Behavioral: HSCL-90-GSI↓, HADS↓, HADS-A ↔, HADS-D ↔, PSS ↔, CCL ↔ |
Mohammadi et al. (2016) [53] | IRN | mental health | 6 | 75 (70); f: 48.6%; age: PL→33.1 ± 6.1, PRyogurt→33.2 ± 6.4, PRcapsule→31.5 ± 5.8; healthy; groups: PL (20), PRyogurt (25), PRcapsule (25) | yogurt: Pegah Company (2), capsules: ZistTakhmir Co. (7); CFU: different, see Table S1; 1/day | Behavioral: GHQ ↔, DASS ↔ |
Murata et al. (2018) [54] | JAP | Mood States | 12 | 241 (202); f: 100%; age: PL→20.2 ± 0.1, PR (10LP)→20.9 ± 0.5, PR (30LP)→21.1 ± 0.6; healthy; groups: PL (70), PR10LP (69), PR30LP (63) | LAC-Shield (1); 10PL: 1 × 1010 CFU, 30PL: 3 × 1010 CFU; 1/day; powder | Behavioral: POMS2 10LP group: ↓ T-scores for Friendliness week 6 + 12, ↓ T-scores for Vigour-Activity week 6 |
Nishida et al. (2017) [55] | JAP | Stress, Sleep Quality | 5 | 32 (32); f: 34.4%; age: PL→21.31 ± 0.9, PR→34.4%; healthy; groups: PL (16), PR (16) | heat-inactivated Lactobacillus gasseri CP2305 (1); 1 × 1010 CFU; 1/day; liquid | Behavioural: GHQ-28 total score ↔, ↑ somatic symptom score, significant interaction of treatment and sex; Zung-SDS ↔; HADS ↔; STAI ↔; PSQI ↔ |
Nishida et al. (2019) [56] | JAP | Stress | 24 | 60 (NR); f: 31.7%; age: PL→25.3 ± 0.6, PR→24.9 ± 0.5; healthy; groups: PL (31), PR (29) | Lactobacillus gasseri CP2305 (1); 1 × 1010 bacterial cells; 2 tablets 1/day | Behavioral: STAI-state ↔, STAI-trait ↓; GHQ28 total ↔, depression ↓; HADS ↔; PSQI ↓ Neurophysiological: EEG: REM and non-REM sleep times ↔, total delta power ↔, ↑ ration of EEG delta power in the first sleep cycle, ↓ sleep latency of the first N3 stage and wake time after sleep onset |
Nishihira et al. (2014) [57] | JAP | Stress | 12 | 238 (224); f: 69.2%; age: PL→54.25 ± 10.93, PR→53.61 ± 11.31; healthy; groups: PL (109), PR (115) | MegMilk Snow Brand Co. Ltd. (2); SBT2055 > 5 × 108 CFU, SBT2928 > 1 × 109 CFU; 1/day; yogurt | Behavioral: GHQ-28 ↔ |
Ohsawa et al. (2018) [58] | JAP | Cognitive Function | 8 | 61 (60); f: 56.7%; age: PL→57.8 ± 5.9, PR→58.5 ± 6.5; healthy, baseline RBANS total score 29–52; groups: PL (29), PR (31) | Lactobacillus helveticus CM4 (1); dose: NR; 1/day; liquid | Behavioral: POMS ↔ Neuropsychological: RBANS total ↔, five index scores: ↑ attention score, subtest index score: ↑ Coding |
Östlund-Lagerström et al. (2016) [59] | SWE | Wellbeing | 12 | 290 (249); f: PR→57%, PL→65.6%; age: PR→72.6 (5.8), PL→72 (5.6); mentally and physically fit; groups: PL (124), PR (125) | Lactobacillus reuteri DSM 17938 (1); 1 × 108 CFU; 2/day; powder | Behavioral: HADS ↔,PSS ↔ |
Papalini et al. (2019) [20] | NLD | Neurocognition | 4 (28 days) | 61 (58); f: 100%; age: PL→22 (SEM: 0.5), PR→21 (SEM: 0.4); healthy; groups: PL (29), PR (29) | Ecologic Barrier (9); 5 × 109 CFU; 1/day; powder | Behavioral: BDI ↔, LEIDS-r ↔, BIS-BAS ↔ Neuropsychological: SECPT↔; Digit Span Test ↔, Emotional face-matching paradigm ↔, Emotional face-word stroop paradigm ↔, Classic colour-word stroop paradigm↔ Neurophysiological: fMRI ↔ |
Patterson et al. (2020) [60] | DEU | Stress, Anxiety | 5 | 120 (117); f: 49.6%; age: PL→23.25 (4.20), PR→23.73 (4.27); healthy; groups: PL (59), PR (58) | Lacticaseibacillus paracasei Lpc-37 (1); 1.75 × 1010 CFU; 1/day; capsule | Behavioral: STAI ↔, VAS Stress ↔, VAS Insecurity ↔ (↓male), VAS Anxiety ↔ (↓male), VAS Exhaustion ↔, PSS ↔ (↑ female), BAI ↔, DASS-24 ↔, Online Diary ↔ (Perceived Productivity + Perceived Health Status ↑ and Sleep Related Recovery ↑↑ in high chronic stress subgroup) |
Rao et al. (2009) [61] | CAN | Chronic Fatigue Syndrome | 8 | 39 (35); f: 77.1%; age: 18–65; healthy, diagnostic criteria for CFS; groups: PL (16), PR (19) | Lactobacillus casei strain Shirota (1); 8 × 109 CFU; 3/day; powder | Behavioral: BDI ↔, BAI ↓ |
Raygan et al. (2018) [62] | IRN | Mental health | 12 | 60 (60); f: 50%; age: PL→67.3 ± 11.0, PR→71.5 ± 10.9; diagnosed with type 2 diabetic and coronary heart disease (2–3 vessel); groups: PL (30), PR (30); Intervention Group with 50,000 IU vitamin D every 2 weeks | LactoCare (4); 8 × 109 CFU; 1/day; application: NR | Behavioral: BDI ↓↓, BAI ↓↓, GHQ-28 ↓↓ |
Raygan et al. (2019) [63] | IRN | Mental health | 12 | 60 (54); f: 61.1%; age: PL→62.4 ± 13.1, PR→64.8 ± 8.3; diagnosed with type 2 diabetic and coronary heart disease (2–3 vessel); groups: PL (27), PR (27); Intervention Group with 200 µg/day selenium | LactoCare (4); 8 × 109 CFU; 1/day; application: NR | Behavioral: BDI ↓↓, BAI ↓, PSQI ↔ |
Reininghaus et al.(2020) [64] | AUT | Depression | 4 (28 days) | 82 (61); f: 77.0%; age: PL→40.11 (11.45), PR→43.00 (14.31); depressive episode by MINI; groups: PL (33), PR (28); bothgroups: 125 mg (D-Biotin) Vitamin D7 | OMNi-BiOTiC Stress Repair (9); 7.5 × 109 CFU; 1/day; powder | Behavioral: HAMD, BDI-II, SCL-90R, MSS, GLQI: ↔ |
Roman et al. (2018) [65] | ESP | Fibromyalgia | 8 | 40 (31); f: 92.5%; age: PL→50.27 ± 7.86, PR→55.00 ± 8.37; diagnosed with FMS; groups: PL (20), PR (20) | ERGYPHILUS Plus (4); 6 × 106 CFU; 4/day; capsule | Behavioral: STAI ↔, BDI ↔ Neuropsychological: MMSE ↔, two-choice task ↓, IGT ↔ |
Romijn et al. (2017) [66] | NZL | Depression | 8 | 79 (79); f: 78.5%; age: PL→35.1 (14.5), PR→35.8 (14); healthy; ≥11 on QIDS-SR16 or ≥14 on DASS-42; groups: PL (39), PR (40) | Lallemand Health Solution (2); ≥ 3 × 109 CFU; 1/day; powder | Behavioral: MADRS, iCGI, QIDS-SR16, GAF, DASS-42: ↔ |
Rudzki et al. (2019) [67] | POL | Depression | 8 | 79 (60); f: 71.7%; age: PL→38.9 (12), PR→39.13 (9.96); major depression during SSRI monotherapy or drug free; groups: PL (39), PR (40); with SSRI treatment | Sanprobi IBS (1); 10 × 109 CFU; 2/day; capsule | Behavioral: HAM-D 17 ↔, SCL-90 ↔, PSS-10 ↔ Neuropsychological: APT ↑↑, Stroop Test A + B ↔, RFFT ↔, TMT A + B ↔, CVLT ↑ |
Sanchez et al. (2017) [68] | CAN | Depression, Anxiety and Stress | 24 | 126 (125); f: 61.6%; age: PL→37 ± 10, PR→35 ± 10; BMI between 29 and 41kg/m; groups: PL (63), PR (62) | Lactobacillus rhamnosus CGMCC1.3724 (1); 3.24 × 108 CFU/day; 2/day; capsules | Behavioral: BDI ↓, STAI ↔, PSS ↔ |
Sashihara et al. (2013) [69] | JAP | Mental Condition | 4 | 44 (44); f: 0%; age: PL→20.2 ± 1.1, PR+αLA→19.9 ± 0.9, PR→19.8 ± 0.9; engaged in high-intensity training ≥5 days/week; groups: PL (14), PR (15), PR+αLA (15) | Lactobacillus gasseri OLL2809 (1); 1 × 1010 CFU; 2 tablets 3/day | Behavioral: POMS and VAS for fatigue ↔ |
Sawada et al. (2017) [70] | JAP | Mental and Sleep Quality | 4 | 24 (NR); f: 0%; age: NR; healthy; RCTCrossover; group1: placebo (4 weeks), washout (3 weeks), probiotic (4 weeks), group2: probiotic (4 weeks), washout (3 weeks), placebo (4 weeks) | Lactobacillus gasseri CP2305 (1); 1 × 1010 CFU; 1/day; powder | Behavioral: GHQ28 ↔, Zung-SDS ↔, HADS depression + anxiety ↓, STAI state ↓, PSQI global + disturbance score ↓ |
Severance et al. (2017) [71] | USA | Schizophrenia | 14 | 65 (56); f: 33.9%; age: PL→48.11 ± 9.6, PR→44.66 ± 11.4; diagnosis of schizophrenia or schizoaffective disorder; groups: PL (26), PR (30) | Bifiform Balance (2); each 109 CFU; 1/day; application: NR | Behavioral: PANSS ↔ |
Shinkai et al. (2013) [72] | JAP | Mood and Quality of Life | 20 | 300 (278); f: 50.4%; age: PL→70.9 ± 2.7, PRlowdose→71.0 ± 4, PRhighdose→70.8 ± 3.4; healthy; 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 (20), PR (20) | Ecologic Barrier (8); 2.5 × 109 CFU/g; 1/day; powder | Behavioral: LEIDS-r total ↓↓↓: aggression ↓↓; rumination ↓↓↓; BDI II ↔; BAI ↔ |
Takada et al. (2016) [74] | JAP | Stress | 8 | 149 (140); f: 45.7%; age: PL→22.8 ± 0.2, PR→23.0 ± 0.2; healthy; groups: PL (70), PR (70) | Lactobacillus casei YIT 9029 (1); 1 × 109 CFU/mL; liquid (100 mL); 1/day | Behavioral: STAI ↔ |
Takada et al. (2017) [75] | JAP | Stress and Sleep | 11 | 98 (94); f: 41.5%; age: PL→22.6 ± 0.2, PR→22.8 ± 0.2; healthy; groups: PL (48), PR (50) | L. casei strain Shirota YIT 9029 (1); 1 × 109 CFU/mL; 100 mL liquid; 1/day | Behavioral: GHQ ↔; NEO-FFI ↔; STAI ↔; PSQI ↔; total OSA ↔; subdivided factors (subsequently compared): sleepiness on rising ↑, sleep length↑↑ Neurophysiological: Sleep EEG: WASO ↑; N3 sleep ↓↓ |
Tillisch et al. (2013) [21] | USA | Brain Activity | 4 | 36 (NR); f: 100%; age: 30 ± 10.4; healthy; groups: PL (11), PR (12), NI (13) | Danone Research facilities (4);dose: different, see Table S1; 2/day; liquid | Behavioral: Diary mood symptoms ↔; HAD ↔ Neurophysiological: Neuroimaging Acquisition and Analysis fMRI ↓↓↓ BOLD activity in the primary viscerosensory and somatosensory cortices |
Tran et al. (2019) [76] | USA | Anxiety | 4 (28 days) | 90 (68); f: 75.6%; age: 20.59 (2.65); healthy; ConditionA (17): highCFU[50billion] + high species count [18], ConditionB (19): highCFU[50billion] + low species count [10], ConditionC (16): control/placebo group, ConditionD (19): lowCFU[15billion]+high species count[18], ConditionE (19): lowCFU[10billion]+low species count [10] | commercially available as over-the-counter products (e.g., Amazon) (from 10 till 20); 1 × 1010–5 × 1010 CFU; 1/day; pills | Behavioural: BAI, ACQ-R, PANAS, NMR, PSWQ ↔ |
Wang et al. (2019) [22] | DEU | Stress | 4 | 43 (40); f: 65%; age: PL→33.00 ± 2.83, PR→31.00 ± 2.28; healthy; groups: PL (20), PR (20) | Bifidobacterium longum 1714 (1); 1 × 109 CFU; 1/day; powder | Behavioural: SF-36↔ Neurophysiological: resting state MEG: ↑ theta band power, ↓ beta-3 band power in different brain region; during social distress: ↑ (S) theta band power,↑ alpha band power in different brain region; in both conditions’ inclusion/exclusion; NTS ↔; SEP ↔; MQ ↔ |
Xiao et al. (2020) [77] | JAP | Memory | 16 | 80 (80); f: 51.3%; age: PL→60.9 (6.9), PR→61.3 (7.7); MMSE score 22 or more; group: PL (40), PR (40) | Bifidobacterium breve A1 (1); 1 × 1010 CFU; 1/day; capsule | Neuropsychological: RBANS ↓↓↓ in RBANS total score, Immediate memory, Visuospatial/Constructional, Delayed memory; JMCIS ↔ |
Yamamura et al. (2009) [78] | JAP | Sleep | 3 | 30 (29); f: 20.7%; age: PL→70.6 ± 5.65, PR→72.14 ± 5.67; healthy, no use of substances that influence sleep; groups: PLfirst (15), PRfirst (14); RCT Crossover→placebo first group: placebo (3 weeks), washout (3 weeks), probiotic (3 weeks), probiotic first group: probiotic (3 weeks), washout (3 weeks), placebo (3 weeks) | Lactobacillus helveticus strain CM4 (1); dose: NR; 1/day; liquid | Behavioural: SHRI ↔, SF-36 ↔ Neurophysiological: Actigraphy ↔ |
Zhang et al. (2021) [79] | CHN | Depression | 9 | 82 (69); f: 63.8%; age: PL→49.7 ± 9.6, PR→45.8 ± 12.3; diagnosed depression (DSM-5); groups: PL (31), PR (38) | Lacticaseibacillus paracasei YIT 9029 (strain Shirota: LcS) (1); 1.0 × 1010 CFU; 1/day; liquid | Behavioural: BDI, HAMD: decreased significantly in both groups, no comparison between groups |
Intention-to-Treat | D1 | D2 | D3 | D4 | D5 | Overall |
---|---|---|---|---|---|---|
Akkasheh 2016 [32] | ||||||
Allen 2016 [59] | ||||||
Bagga 2018 [19] | ||||||
Bagga 2019 [18] | ||||||
Benton 2007 [60] | ||||||
De Lorenzo 2017 [61] | ||||||
Dickerson 2018 [73] | ||||||
Diop 2008 [62] | ||||||
Ghaderi 2019 [34] | ||||||
Ho 2021 [55] | ||||||
Hwang 2019 [35] | ||||||
Karbownik 2020 [64] | ||||||
Kato-Kataoka 2016 [37] | ||||||
Kazemi 2019 [38] | ||||||
Kelly 2017 [65] | ||||||
Nishida 2017 [43] | ||||||
Nishida 2019 [44] | ||||||
Östlund-Lagerström 2016 [67] | ||||||
Patterson 2020 [68] | ||||||
Raygan 2018 [48] | ||||||
Romijn 2017 [79] | ||||||
Sanchez 2017 [78] | ||||||
Sashihara 2013 [49] | ||||||
Sawada 2017 [50] | ||||||
Steenbergen 2015 [72] | ||||||
Xiao 2020 [56] | ||||||
Per-protocol | D1 | D2 | D3 | D4 | D5 | Overall |
Adikari 2020 [54] | ||||||
Chung 2014 [33] | ||||||
Dickerson 2014 [74] | ||||||
Eskandarzadeh 2021 [30] | ||||||
Gualtieri 2020 [63] | ||||||
Inoue 2018 [36] | ||||||
Kobayashi 2019 [39] | ||||||
Lew 2019 [40] | ||||||
Messaoudi 2011 [66] | ||||||
Mohammadi 2016 [41] | ||||||
Murata 2018 [42] | ||||||
Nishihira 2014 [45] | ||||||
Ohsawa 2018 [46] | ||||||
Papalini 2019 [20] | ||||||
Rao 2009 [75] | ||||||
Raygan 2019 [47] | ||||||
Reininghaus2020 [69] | ||||||
Roman 2018 [70] | ||||||
Romijn 2017 [79] | ||||||
Rudzki 2019 [71] | ||||||
Shinkai 2013 [58] | ||||||
Takada 2016 [52] | ||||||
Takada 2017 [51] | ||||||
Tillisch 2013 [21] | ||||||
Tran 2019 [77] | ||||||
Wang 2019 [22] | ||||||
Yamamura 2009 [53] | ||||||
Zhang 2021 [57] | ||||||
Low risk | ||||||
Some concerns | ||||||
High risk | ||||||
D1 | Randomisation process | |||||
D2 | Deviations from the intended interventions | |||||
D3 | Missing outcome data | |||||
D4 | Measurement of the outcome | |||||
D5 | Selection of the reported result |
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Le Morvan de Sequeira, C.; Hengstberger, C.; Enck, P.; Mack, I. Effect of Probiotics on Psychiatric Symptoms and Central Nervous System Functions in Human Health and Disease: A Systematic Review and Meta-Analysis. Nutrients 2022, 14, 621. https://doi.org/10.3390/nu14030621
Le Morvan de Sequeira C, Hengstberger C, Enck P, Mack I. Effect of Probiotics on Psychiatric Symptoms and Central Nervous System Functions in Human Health and Disease: A Systematic Review and Meta-Analysis. Nutrients. 2022; 14(3):621. https://doi.org/10.3390/nu14030621
Chicago/Turabian StyleLe Morvan de Sequeira, Charlotte, Charlotte Hengstberger, Paul Enck, and Isabelle Mack. 2022. "Effect of Probiotics on Psychiatric Symptoms and Central Nervous System Functions in Human Health and Disease: A Systematic Review and Meta-Analysis" Nutrients 14, no. 3: 621. https://doi.org/10.3390/nu14030621