Microbiota shaping - the effects of probiotics, prebiotics, and fecal microbiota transplant on cognitive functions: A systematic review

Simone Baldi, Tiziana Mundula, Giulia Nannini, Amedeo Amedei, Simone Baldi, Tiziana Mundula, Giulia Nannini, Amedeo Amedei

Abstract

Background: Dementia is a chronic progressive neurological disease affecting millions of people worldwide, and represents a relevant economic burden for healthcare systems. Although its pathogenesis is still unknown, recent findings have reported that a dysregulated gut-brain axis communication, a fundamental relationship mediated by several host and microbial molecules, is associated with cognitive disorders. In addition, gut microbiota manipulation reduces neuroinflammation, improving cognitive function by restoring the functional gut-brain axis.

Aim: To better define the effects of probiotics, prebiotics, synbiotics, and fecal microbiota transplant (FMT) on cognitive function.

Methods: We performed a literature search of human randomized clinical trials to examine the effects of the administration of probiotics, prebiotics, synbiotics, or FMT on cognition outcomes in healthy or sick people of every age, sex, and nationality. We systematically searched Embase, Medline/PubMed, Cochrane Library, central and clinicaltrials.gov databases with a combination of comprehensive terms related to cognition and gut microbiota manipulation. Then we carefully reviewed and synthesized the data by type of study design and setting, characteristics of the studied population, kind of intervention (strain type or mixture type, dosage, and frequency of administration), control treatment, inclusion and exclusion criteria, follow-up duration, and cognitive or memory outcomes.

Results: After examining the titles and abstracts, the initial literature screening identified 995 articles, but we added 23 papers in our systematic review. The analyses of these selected studies highlighted that both probiotic supplementation and FMT improved cognitive function regardless of the type and posology of administration and the adopted cognitive tests and questionnaires. We found that most of the studies conducted in healthy people showed a significant positive effect of the intervention on at least one of the performed cognitive tests. Regarding unhealthy subjects, while FMT and especially probiotic administration had multiple beneficial effects on different cognitive functions, supplementation with prebiotics did not provide any cognitive improvement.

Conclusion: Probiotic supplementation and FMT may represent a promising strategy to restore gut eubiosis and enhance the cognitive functions of healthy people and patients with neurological disorders.

Keywords: Cognitive disorders; Dementia; Fecal microbiota transplant; Gut microbiota; Prebiotics; Probiotics.

Conflict of interest statement

Conflict-of-interest statement: The authors declare no competing interests.

©The Author(s) 2021. Published by Baishideng Publishing Group Inc. All rights reserved.

Figures

Figure 1
Figure 1
PRISMA flow diagram.
Figure 2
Figure 2
Gut-brain axis in eubiosis and dysbiosis condition. A: Eubiosis; B: Dysbiosis condition. AHR: Aryl hydrocarbon receptor; FMT: Fecal microbiota transplant; SCFA: Short-chain fatty acid; SIRT1: Sirtuin 1.

References

    1. Land KC, Lamb VL. Demography of Aging. In: Heggenhougen K, Stella Q. International Encyclopedia of Public Health. San Diego: Academic Press, 2008: 89-95.
    1. Brayne C, Miller B. Dementia and aging populations-A global priority for contextualized research and health policy. PLoS Med. 2017;14:e1002275.
    1. Tomaskova H, Kuhnova J, Cimler R, Dolezal O, Kuca K. Prediction of population with Alzheimer's disease in the European Union using a system dynamics model. Neuropsychiatr Dis Treat. 2016;12:1589–1598.
    1. Prince MJ, Wu F, Guo Y, Gutierrez Robledo LM, O'Donnell M, Sullivan R, Yusuf S. The burden of disease in older people and implications for health policy and practice. Lancet. 2015;385:549–562.
    1. Sacuiu SF. Dementias. Handb Clin Neurol. 2016;138:123–151.
    1. Snyder HM, Corriveau RA, Craft S, Faber JE, Greenberg SM, Knopman D, Lamb BT, Montine TJ, Nedergaard M, Schaffer CB, Schneider JA, Wellington C, Wilcock DM, Zipfel GJ, Zlokovic B, Bain LJ, Bosetti F, Galis ZS, Koroshetz W, Carrillo MC. Vascular contributions to cognitive impairment and dementia including Alzheimer's disease. Alzheimers Dement. 2015;11:710–717.
    1. Raz L, Knoefel J, Bhaskar K. The neuropathology and cerebrovascular mechanisms of dementia. J Cereb Blood Flow Metab. 2016;36:172–186.
    1. Yiannopoulou KG, Papageorgiou SG. Current and future treatments for Alzheimer's disease. Ther Adv Neurol Disord. 2013;6:19–33.
    1. Boem F, Amedei A. Healthy axis: Towards an integrated view of the gut-brain health. World J Gastroenterol. 2019;25:3838–3841.
    1. Cussotto S, Sandhu KV, Dinan TG, Cryan JF. The Neuroendocrinology of the Microbiota-Gut-Brain Axis: A Behavioural Perspective. Front Neuroendocrinol. 2018;51:80–101.
    1. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012;13:701–712.
    1. Mangiola F, Ianiro G, Franceschi F, Fagiuoli S, Gasbarrini G, Gasbarrini A. Gut microbiota in autism and mood disorders. World J Gastroenterol. 2016;22:361–368.
    1. Noble EE, Hsu TM, Kanoski SE. Gut to Brain Dysbiosis: Mechanisms Linking Western Diet Consumption, the Microbiome, and Cognitive Impairment. Front Behav Neurosci. 2017;11:9.
    1. Ticinesi A, Tana C, Nouvenne A, Prati B, Lauretani F, Meschi T. Gut microbiota, cognitive frailty and dementia in older individuals: a systematic review. Clin Interv Aging. 2018;13:1497–1511.
    1. Bonfili L, Cecarini V, Berardi S, Scarpona S, Suchodolski JS, Nasuti C, Fiorini D, Boarelli MC, Rossi G, Eleuteri AM. Microbiota modulation counteracts Alzheimer's disease progression influencing neuronal proteolysis and gut hormones plasma levels. Sci Rep. 2017;7:2426.
    1. Risk Reduction of Cognitive Decline and Dementia: WHO Guidelines. Geneva: World Health Organization; 2019 .
    1. Chen D, Yang X, Yang J, Lai G, Yong T, Tang X, Shuai O, Zhou G, Xie Y, Wu Q. Prebiotic Effect of Fructooligosaccharides from Morinda officinalis on Alzheimer's Disease in Rodent Models by Targeting the Microbiota-Gut-Brain Axis. Front Aging Neurosci. 2017;9:403.
    1. Larsen N, Vogensen FK, Gøbel RJ, Michaelsen KF, Forssten SD, Lahtinen SJ, Jakobsen M. Effect of Lactobacillus salivarius Ls-33 on fecal microbiota in obese adolescents. Clin Nutr. 2013;32:935–940.
    1. Cammarota G, Ianiro G, Tilg H, Rajilić-Stojanović M, Kump P, Satokari R, Sokol H, Arkkila P, Pintus C, Hart A, Segal J, Aloi M, Masucci L, Molinaro A, Scaldaferri F, Gasbarrini G, Lopez-Sanroman A, Link A, de Groot P, de Vos WM, Högenauer C, Malfertheiner P, Mattila E, Milosavljević T, Nieuwdorp M, Sanguinetti M, Simren M, Gasbarrini A European FMT Working Group. European consensus conference on faecal microbiota transplantation in clinical practice. Gut. 2017;66:569–580.
    1. Sun J, Xu J, Ling Y, Wang F, Gong T, Yang C, Ye S, Ye K, Wei D, Song Z, Chen D, Liu J. Fecal microbiota transplantation alleviated Alzheimer's disease-like pathogenesis in APP/PS1 transgenic mice. Transl Psychiatry. 2019;9:189.
    1. Goloshchapov OV, Olekhnovich EI, Sidorenko SV, Moiseev IS, Kucher MA, Fedorov DE, Pavlenko AV, Manolov AI, Gostev VV, Veselovsky VA, Klimina KM, Kostryukova ES, Bakin EA, Shvetcov AN, Gumbatova ED, Klementeva RV, Shcherbakov AA, Gorchakova MV, Egozcue JJ, Pawlowsky-Glahn V, Suvorova MA, Chukhlovin AB, Govorun VM, Ilina EN, Afanasyev BV. Long-term impact of fecal transplantation in healthy volunteers. BMC Microbiol. 2019;19:312.
    1. Neisser U. Cognitive psychology. Englewood Cliffs: Prentice-Hall ll, Inc., 1967.
    1. Agahi A, Hamidi GA, Daneshvar R, Hamdieh M, Soheili M, Alinaghipour A, Esmaeili Taba SM, Salami M. Does Severity of Alzheimer's Disease Contribute to Its Responsiveness to Modifying Gut Microbiota? Front Neurol. 2018;9:662.
    1. Akbari E, Asemi Z, Daneshvar Kakhaki R, Bahmani F, Kouchaki E, Tamtaji OR, Hamidi GA, Salami M. Effect of Probiotic Supplementation on Cognitive Function and Metabolic Status in Alzheimer's Disease: A Randomized, Double-Blind and Controlled Trial. Front Aging Neurosci. 2016;8:256.
    1. Bagga D, Reichert JL, Koschutnig K, Aigner CS, Holzer P, Koskinen K, Moissl-Eichinger C, Schöpf V. Probiotics drive gut microbiome triggering emotional brain signatures. Gut Microbes. 2018;9:486–496.
    1. Bajaj JS, Heuman DM, Hylemon PB, Sanyal AJ, Puri P, Sterling RK, Luketic V, Stravitz RT, Siddiqui MS, Fuchs M, Thacker LR, Wade JB, Daita K, Sistrun S, White MB, Noble NA, Thorpe C, Kakiyama G, Pandak WM, Sikaroodi M, Gillevet PM. Randomised clinical trial: Lactobacillus GG modulates gut microbiome, metabolome and endotoxemia in patients with cirrhosis. Aliment Pharmacol Ther. 2014;39:1113–1125.
    1. Bajaj JS, Kassam Z, Fagan A, Gavis EA, Liu E, Cox IJ, Kheradman R, Heuman D, Wang J, Gurry T, Williams R, Sikaroodi M, Fuchs M, Alm E, John B, Thacker LR, Riva A, Smith M, Taylor-Robinson SD, Gillevet PM. Fecal microbiota transplant from a rational stool donor improves hepatic encephalopathy: A randomized clinical trial. Hepatology. 2017;66:1727–1738.
    1. Bajaj JS, Salzman NH, Acharya C, Sterling RK, White MB, Gavis EA, Fagan A, Hayward M, Holtz ML, Matherly S, Lee H, Osman M, Siddiqui MS, Fuchs M, Puri P, Sikaroodi M, Gillevet PM. Fecal Microbial Transplant Capsules Are Safe in Hepatic Encephalopathy: A Phase 1, Randomized, Placebo-Controlled Trial. Hepatology. 2019;70:1690–1703.
    1. 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.
    1. Buigues C, Fernández-Garrido J, Pruimboom L, Hoogland AJ, Navarro-Martínez R, Martínez-Martínez M, Verdejo Y, Mascarós MC, Peris C, Cauli O. Effect of a Prebiotic Formulation on Frailty Syndrome: A Randomized, Double-Blind Clinical Trial. Int J Mol Sci. 2016;17
    1. Capitão LP, Baião R, Baek HK, Kappelmann N, Sharman R, Harvey CJ, Montgomery P, Burnet PW. Prebiotic supplementation does not affect reading and cognitive performance in children: A randomised placebo-controlled study. J Psychopharmacol. 2020;34:148–152.
    1. Ceccarelli G, Brenchley JM, Cavallari EN, Scheri GC, Fratino M, Pinacchio C, Schietroma I, Fard SN, Scagnolari C, Mezzaroma I, Vullo V, d'Ettorre G. Impact of High-Dose Multi-Strain Probiotic Supplementation on Neurocognitive Performance and Central Nervous System Immune Activation of HIV-1 Infected Individuals. Nutrients. 2017;9
    1. Chung YC, Jin HM, Cui Y, Kim DS, Jung JM, Park JI, Jung ES, Choi EK, Chae SW. Fermented milk of Lactobacillus helveticus IDCC3801 improves cognitive functioning during cognitive fatigue tests in healthy older adults. J Funct Foods. 2014;10:465–474.
    1. Inoue T, Kobayashi Y, Mori N, Sakagawa M, Xiao JZ, 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.
    1. Hwang YH, Park S, Paik JW, Chae SW, Kim DH, Jeong DG, Ha E, Kim M, Hong G, Park SH, Jung SJ, Lee SM, Na KH, Kim J, Chung YC. 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
    1. Kelly JR, Allen AP, Temko A, Hutch W, Kennedy PJ, Farid N, Murphy E, Boylan G, Bienenstock J, Cryan JF, Clarke G, Dinan TG. Lost in translation? Brain Behav Immun. 2017;61:50–59.
    1. Kobayashi Y, Kuhara T, Oki M, Xiao JZ. 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.
    1. Lew LC, Hor YY, Yusoff NAA, Choi SB, Yusoff MSB, Roslan NS, Ahmad A, Mohammad JAM, Abdullah MFIL, Zakaria N, Wahid N, Sun Z, Kwok LY, Zhang H, Liong MT. 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.
    1. 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.
    1. 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.
    1. Roman P, Estévez AF, Miras A, Sánchez-Labraca N, Cañadas F, Vivas AB, Cardona D. A Pilot Randomized Controlled Trial to Explore Cognitive and Emotional Effects of Probiotics in Fibromyalgia. Sci Rep. 2018;8:10965.
    1. 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.
    1. Smith AP, Sutherland D, Hewlett P. An Investigation of the Acute Effects of Oligofructose-Enriched Inulin on Subjective Wellbeing, Mood and Cognitive Performance. Nutrients. 2015;7:8887–8896.
    1. Tamtaji OR, Heidari-Soureshjani R, Mirhosseini N, Kouchaki E, Bahmani F, Aghadavod E, Tajabadi-Ebrahimi M, Asemi Z. Probiotic and selenium co-supplementation, and the effects on clinical, metabolic and genetic status in Alzheimer's disease: A randomized, double-blind, controlled trial. Clin Nutr. 2019;38:2569–2575.
    1. Tamtaji OR, Taghizadeh M, Daneshvar Kakhaki R, Kouchaki E, Bahmani F, Borzabadi S, Oryan S, Mafi A, Asemi Z. Clinical and metabolic response to probiotic administration in people with Parkinson's disease: A randomized, double-blind, placebo-controlled trial. Clin Nutr. 2019;38:1031–1035.
    1. Lee MT, Jang Y, Chang WY. How do impairments in cognitive functions affect activities of daily living functions in older adults? PLoS One. 2019;14:e0218112.
    1. Bunn F, Burn AM, Goodman C, Rait G, Norton S, Robinson L, Schoeman J, Brayne C. Comorbidity and dementia: a scoping review of the literature. BMC Med. 2014;12:192.
    1. Qiu C, Kivipelto M, von Strauss E. Epidemiology of Alzheimer's disease: occurrence, determinants, and strategies toward intervention. Dialogues Clin Neurosci. 2009;11:111–128.
    1. Vuotto C, Battistini L, Caltagirone C, Borsellino G. Gut Microbiota and Disorders of the Central Nervous System. Neuroscientist. 2020;26:487–502.
    1. Sarkar A, Lehto SM, Harty S, Dinan TG, Cryan JF, Burnet PWJ. Psychobiotics and the Manipulation of Bacteria-Gut-Brain Signals. Trends Neurosci. 2016;39:763–781.
    1. Cryan JF, O'Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, Codagnone MG, Cussotto S, Fulling C, Golubeva AV, Guzzetta KE, Jaggar M, Long-Smith CM, Lyte JM, Martin JA, Molinero-Perez A, Moloney G, Morelli E, Morillas E, O'Connor R, Cruz-Pereira JS, Peterson VL, Rea K, Ritz NL, Sherwin E, Spichak S, Teichman EM, van de Wouw M, Ventura-Silva AP, Wallace-Fitzsimons SE, Hyland N, Clarke G, Dinan TG. The Microbiota-Gut-Brain Axis. Physiol Rev. 2019;99:1877–2013.
    1. Martin CR, Osadchiy V, Kalani A, Mayer EA. The Brain-Gut-Microbiome Axis. Cell Mol Gastroenterol Hepatol. 2018;6:133–148.
    1. Liu S, Gao J, Zhu M, Liu K, Zhang HL. Gut Microbiota and Dysbiosis in Alzheimer's Disease: Implications for Pathogenesis and Treatment. Mol Neurobiol. 2020;57:5026–5043.
    1. Cerovic M, Forloni G, Balducci C. Neuroinflammation and the Gut Microbiota: Possible Alternative Therapeutic Targets to Counteract Alzheimer's Disease? Front Aging Neurosci. 2019;11:284.
    1. Rao RK, Samak G. Protection and Restitution of Gut Barrier by Probiotics: Nutritional and Clinical Implications. Curr Nutr Food Sci. 2013;9:99–107.
    1. Cheng S, Ma X, Geng S, Jiang X, Li Y, Hu L, Li J, Wang Y, Han X. Fecal Microbiota Transplantation Beneficially Regulates Intestinal Mucosal Autophagy and Alleviates Gut Barrier Injury. mSystems. 2018;3
    1. Li LL, Wang YT, Zhu LM, Liu ZY, Ye CQ, Qin S. Inulin with different degrees of polymerization protects against diet-induced endotoxemia and inflammation in association with gut microbiota regulation in mice. Sci Rep. 2020;10:978.
    1. Bermudez-Brito M, Plaza-Díaz J, Muñoz-Quezada S, Gómez-Llorente C, Gil A. Probiotic mechanisms of action. Ann Nutr Metab. 2012;61:160–174.
    1. Plaza-Diaz J, Ruiz-Ojeda FJ, Gil-Campos M, Gil A. Mechanisms of Action of Probiotics. Adv Nutr. 2019;10:S49–S66.
    1. Ma Q, Xing C, Long W, Wang HY, Liu Q, Wang RF. Impact of microbiota on central nervous system and neurological diseases: the gut-brain axis. J Neuroinflammation. 2019;16:53.
    1. Wang Y, Kasper LH. The role of microbiome in central nervous system disorders. Brain Behav Immun. 2014;38:1–12.
    1. Bonaz B, Bazin T, Pellissier S. The Vagus Nerve at the Interface of the Microbiota-Gut-Brain Axis. Front Neurosci. 2018;12:49.
    1. Kim N, Yun M, Oh YJ, Choi HJ. Mind-altering with the gut: Modulation of the gut-brain axis with probiotics. J Microbiol. 2018;56:172–182.
    1. Qin Y, Wade PA. Crosstalk between the microbiome and epigenome: messages from bugs. J Biochem. 2018;163:105–112.
    1. Bonfili L, Cecarini V, Cuccioloni M, Angeletti M, Berardi S, Scarpona S, Rossi G, Eleuteri AM. SLAB51 Probiotic Formulation Activates SIRT1 Pathway Promoting Antioxidant and Neuroprotective Effects in an AD Mouse Model. Mol Neurobiol. 2018;55:7987–8000.
    1. Agus A, Planchais J, Sokol H. Gut Microbiota Regulation of Tryptophan Metabolism in Health and Disease. Cell Host Microbe. 2018;23:716–724.
    1. Birner A, Platzer M, Bengesser SA, Dalkner N, Fellendorf FT, Queissner R, Pilz R, Rauch P, Maget A, Hamm C, Herzog-Eberhard S, Mangge H, Fuchs D, Moll N, Zelzer S, Schütze G, Schwarz M, Reininghaus B, Kapfhammer HP, Reininghaus EZ. Increased breakdown of kynurenine towards its neurotoxic branch in bipolar disorder. PLoS One. 2017;12:e0172699.
    1. Bansal Y, Singh R, Parhar I, Kuhad A, Soga T. Quinolinic Acid and Nuclear Factor Erythroid 2-Related Factor 2 in Depression: Role in Neuroprogression. Front Pharmacol. 2019;10:452.
    1. Wong CB, Tanaka A, Kuhara T, Xiao JZ. Potential Effects of Indole-3-Lactic Acid, a Metabolite of Human Bifidobacteria, on NGF-induced Neurite Outgrowth in PC12 Cells. Microorganisms. 2020;8
    1. Cuartero MI, Ballesteros I, de la Parra J, Harkin AL, Abautret-Daly A, Sherwin E, Fernández-Salguero P, Corbí AL, Lizasoain I, Moro MA. L-kynurenine/aryl hydrocarbon receptor pathway mediates brain damage after experimental stroke. Circulation. 2014;130:2040–2051.
    1. Rothhammer V, Quintana FJ. The aryl hydrocarbon receptor: an environmental sensor integrating immune responses in health and disease. Nat Rev Immunol. 2019;19:184–197.
    1. Takamura T, Harama D, Fukumoto S, Nakamura Y, Shimokawa N, Ishimaru K, Ikegami S, Makino S, Kitamura M, Nakao A. Lactobacillus bulgaricus OLL1181 activates the aryl hydrocarbon receptor pathway and inhibits colitis. Immunol Cell Biol. 2011;89:817–822.
    1. Lamas B, Hernandez-Galan L, Galipeau HJ, Constante M, Clarizio A, Jury J, Breyner NM, Caminero A, Rueda G, Hayes CL, McCarville JL, Bermudez Brito M, Planchais J, Rolhion N, Murray JA, Langella P, Loonen LMP, Wells JM, Bercik P, Sokol H, Verdu EF. Aryl hydrocarbon receptor ligand production by the gut microbiota is decreased in celiac disease leading to intestinal inflammation. Sci Transl Med. 2020;12
    1. Liang S, Wang T, Hu X, Luo J, Li W, Wu X, Duan Y, Jin F. Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress. Neuroscience. 2015;310:561–577.
    1. Gu F, Wu Y, Liu Y, Dou M, Jiang Y, Liang H. Lactobacillus casei improves depression-like behavior in chronic unpredictable mild stress-induced rats by the BDNF-TrkB signal pathway and the intestinal microbiota. Food Funct. 2020;11:6148–6157.
    1. Orlando A, Chimienti G, Lezza AMS, Pesce V, Gigante I, D'Attoma B, Russo F. Lactobacillus Rhamnosus GG Affects the BDNF System in Brain Samples of Wistar Rats with Pepsin-Trypsin-Digested Gliadin (PTG)-Induced Enteropathy. Nutrients. 2020;12
    1. McLoughlin RF, Berthon BS, Jensen ME, Baines KJ, Wood LG. Short-chain fatty acids, prebiotics, synbiotics, and systemic inflammation: a systematic review and meta-analysis. Am J Clin Nutr. 2017;106:930–945.
    1. Silva YP, Bernardi A, Frozza RL. The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication. Front Endocrinol (Lausanne) 2020;11:25.
    1. Vendrik KEW, Ooijevaar RE, de Jong PRC, Laman JD, van Oosten BW, van Hilten JJ, Ducarmon QR, Keller JJ, Kuijper EJ, Contarino MF. Fecal Microbiota Transplantation in Neurological Disorders. Front Cell Infect Microbiol. 2020;10:98.
    1. D'Amato A, Di Cesare Mannelli L, Lucarini E, Man AL, Le Gall G, Branca JJV, Ghelardini C, Amedei A, Bertelli E, Regoli M, Pacini A, Luciani G, Gallina P, Altera A, Narbad A, Gulisano M, Hoyles L, Vauzour D, Nicoletti C. Faecal microbiota transplant from aged donor mice affects spatial learning and memory via modulating hippocampal synaptic plasticity- and neurotransmission-related proteins in young recipients. Microbiome. 2020;8:140.
    1. Sanders ME, Akkermans LM, Haller D, Hammerman C, Heimbach J, Hörmannsperger G, Huys G, Levy DD, Lutgendorff F, Mack D, Phothirath P, Solano-Aguilar G, Vaughan E. Safety assessment of probiotics for human use. Gut Microbes. 2010;1:164–185.
    1. Lerner A, Shoenfeld Y, Matthias T. Probiotics: If It Does Not Help It Does Not Do Any Harm. Really? Microorganisms. 2019;7
    1. Zawistowska-Rojek A, Tyski S. Are Probiotic Really Safe for Humans? Pol J Microbiol. 2018;67:251–258.
    1. Sbahi H, Di Palma JA. Faecal microbiota transplantation: applications and limitations in treating gastrointestinal disorders. BMJ Open Gastroenterol. 2016;3:e000087.
    1. Gill HS, Rutherfurd KJ, Cross ML. Dietary probiotic supplementation enhances natural killer cell activity in the elderly: an investigation of age-related immunological changes. J Clin Immunol. 2001;21:264–271.
    1. Snydman DR. The safety of probiotics. Clin Infect Dis. 2008;46 Suppl 2:S104–11; discussion S144.
    1. Wardill HR, Secombe KR, Bryant RV, Hazenberg MD, Costello SP. Adjunctive fecal microbiota transplantation in supportive oncology: Emerging indications and considerations in immunocompromised patients. EBioMedicine. 2019;44:730–740.
    1. Merrick B, Allen L, Masirah M Zain N, Forbes B, Shawcross DL, Goldenberg SD. Regulation, risk and safety of Faecal Microbiota Transplant. Infect Prev Pract. 2020;2:100069.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe