The Potential Utility of Prebiotics to Modulate Alzheimer’s Disease: A Review of the Evidence
Abstract
:1. Introduction
2. Links between Gut Microbiome Composition and AD and Associated Co-Morbidities
3. Overview of Prebiotic Types and Their Roles in Modifying Gut Microbiota
4. Effectiveness of Prebiotics in Modulating Gut Microbiome Composition and Microbial Metabolite Production
5. Current Evidence for Effectiveness of Prebiotics in AD Animal Models and Human Trials
5.1. Animal Models
5.2. Human Trials
6. Concluding Remarks
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Turnbaugh, P.J.; Ley, R.E.; Mahowald, M.A.; Magrini, V.; Mardis, E.R.; Gordon, J.I. An Obesity-Associated Gut Microbiome with Increased Capacity for Energy Harvest. Nature 2006, 444, 1027–1031. [Google Scholar] [CrossRef]
- Forslund, K.; Hildebrand, F.; Nielsen, T.; Falony, G.; Le Chatelier, E.; Sunagawa, S.; Prifti, E.; Vieira-Silva, S.; Gudmundsdottir, V.; Krogh Pedersen, H.; et al. Disentangling Type 2 Diabetes and Metformin Treatment Signatures in the Human Gut Microbiota. Nature 2015, 528, 262–266. [Google Scholar] [CrossRef]
- Vogt, N.M.; Kerby, R.L.; Dill-McFarland, K.A.; Harding, S.J.; Merluzzi, A.P.; Johnson, S.C.; Carlsson, C.M.; Asthana, S.; Zetterberg, H.; Blennow, K.; et al. Gut Microbiome Alterations in Alzheimer’s Disease. Sci. Rep. 2017, 7, 13537. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- Selkoe, D.J. Alzheimer’s Disease: Genes, Proteins, and Therapy. Physiol. Rev. 2001, 81, 741–766. [Google Scholar] [CrossRef]
- Mahley, R.W.; Weisgraber, K.H.; Huang, Y. Apolipoprotein E4: A Causative Factor and Therapeutic Target in Neuropathology, Including Alzheimer’s Disease. Proc. Natl. Acad. Sci. USA 2006, 103, 5644–5651. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Strittmatter, W.J.; Saunders, A.M.; Schmechel, D.; Pericak-Vance, M.; Enghild, J.; Salvesen, G.S.; Roses, A.D. Apolipoprotein E: High-Avidity Binding to Beta-Amyloid and Increased Frequency of Type 4 Allele in Late-Onset Familial Alzheimer Disease. Proc. Natl. Acad. Sci. USA 1993, 90, 1977–1981. [Google Scholar] [CrossRef] [Green Version]
- Baumgart, M.; Snyder, H.M.; Carrillo, M.C.; Fazio, S.; Kim, H.; Johns, H. Summary of the Evidence on Modifiable Risk Factors for Cognitive Decline and Dementia: A Population-Based Perspective. Alzheimer’s Dement. 2015, 11, 718–726. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Glenner, G.G.; Wong, C.W. Alzheimer’s Disease: Initial Report of the Purification and Characterization of a Novel Cerebrovascular Amyloid Protein. Biochem. Biophys. Res. Commun. 1984, 120, 885–890. [Google Scholar] [CrossRef]
- Wischik, C.M.; Novak, M.; Edwards, P.C.; Klug, A.; Tichelaar, W.; Crowther, R.A. Structural Characterization of the Core of the Paired Helical Filament of Alzheimer Disease. Proc. Natl. Acad. Sci. USA 1988, 85, 4884–4888. [Google Scholar] [CrossRef] [Green Version]
- Sochocka, M.; Diniz, B.S.; Leszek, J. Inflammatory Response in the CNS: Friend or Foe? Mol. Neurobiol. 2017, 54, 8071–8089. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tohidpour, A.; Morgun, A.V.; Boitsova, E.B.; Malinovskaya, N.A.; Martynova, G.P.; Khilazheva, E.D.; Kopylevich, N.V.; Gertsog, G.E.; Salmina, A.B. Neuroinflammation and Infection: Molecular Mechanisms Associated with Dysfunction of Neurovascular Unit. Front. Cell. Infect. Microbiol. 2017, 7, 276. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carabotti, M.; Scirocco, A.; Maselli, M.A.; Severi, C. The Gut-Brain Axis: Interactions between Enteric Microbiota, Central and Enteric Nervous Systems. Ann. Gastroenterol. 2015, 28, 203–209. [Google Scholar] [PubMed]
- Bindels, L.B.; Delzenne, N.M.; Cani, P.D.; Walter, J. Towards a More Comprehensive Concept for Prebiotics. Nat. Rev. Gastroenterol. Hepatol. 2015, 12, 303–310. [Google Scholar] [CrossRef]
- Carlson, J.L.; Erickson, J.M.; Lloyd, B.B.; Slavin, J.L. Health Effects and Sources of Prebiotic Dietary Fiber. Curr. Dev. Nutr. 2018, 2, nzy005. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Filippo, C.D.; Cavalieri, D.; Paola, M.D.; Ramazzotti, M.; Poullet, J.B.; Massart, S.; Collini, S.; Pieraccini, G.; Lionetti, P. Impact of Diet in Shaping Gut Microbiota Revealed by a Comparative Study in Children from Europe and Rural Africa. Proc. Natl. Acad. Sci. USA 2010, 107, 14691–14696. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Claesson, M.J.; Jeffery, I.B.; Conde, S.; Power, S.E.; O’Connor, E.M.; Cusack, S.; Harris, H.M.B.; Coakley, M.; Lakshminarayanan, B.; O’Sullivan, O.; et al. Gut Microbiota Composition Correlates with Diet and Health in the Elderly. Nature 2012, 488, 178–184. [Google Scholar] [CrossRef]
- Kashyap, P.C.; Marcobal, A.; Ursell, L.K.; Larauche, M.; Duboc, H.; Earle, K.A.; Sonnenburg, E.D.; Ferreyra, J.A.; Higginbottom, S.K.; Million, M.; et al. Complex Interactions Among Diet, Gastrointestinal Transit, and Gut Microbiota in Humanized Mice. Gastroenterology 2013, 144, 967–977. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parks, B.W.; Nam, E.; Org, E.; Kostem, E.; Norheim, F.; Hui, S.T.; Pan, C.; Civelek, M.; Rau, C.D.; Bennett, B.J.; et al. Genetic Control of Obesity and Gut Microbiota Composition in Response to High-Fat, High-Sucrose Diet in Mice. Cell Metab. 2013, 17, 141–152. [Google Scholar] [CrossRef] [Green Version]
- Daniel, H.; Gholami, A.M.; Berry, D.; Desmarchelier, C.; Hahne, H.; Loh, G.; Mondot, S.; Lepage, P.; Rothballer, M.; Walker, A.; et al. High-Fat Diet Alters Gut Microbiota Physiology in Mice. ISME J. 2014, 8, 295–308. [Google Scholar] [CrossRef] [PubMed]
- Carmody, R.N.; Gerber, G.K.; Luevano, J.M.; Gatti, D.M.; Somes, L.; Svenson, K.L.; Turnbaugh, P.J. Diet Dominates Host Genotype in Shaping the Murine Gut Microbiota. Cell Host Microbe 2015, 17, 72–84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Filippis, F.D.; Pellegrini, N.; Vannini, L.; Jeffery, I.B.; Storia, A.L.; Laghi, L.; Serrazanetti, D.I.; Cagno, R.D.; Ferrocino, I.; Lazzi, C.; et al. High-Level Adherence to a Mediterranean Diet Beneficially Impacts the Gut Microbiota and Associated Metabolome. Gut 2016, 65, 1812–1821. [Google Scholar] [CrossRef] [PubMed]
- Vaughn, A.C.; Cooper, E.M.; DiLorenzo, P.M.; O’Loughlin, L.J.; Konkel, M.E.; Peters, J.H.; Hajnal, A.; Sen, T.; Lee, S.H.; de La Serre, C.B.; et al. Energy-Dense Diet Triggers Changes in Gut Microbiota, Reorganization of Gut-Brain Vagal Communication and Increases Body Fat Accumulation. Acta Neurobiol. Exp. 2017, 77, 18–30. [Google Scholar] [CrossRef] [Green Version]
- Zou, J.; Chassaing, B.; Singh, V.; Pellizzon, M.; Ricci, M.; Fythe, M.D.; Kumar, M.V.; Gewirtz, A.T. Fiber-Mediated Nourishment of Gut Microbiota Protects against Diet-Induced Obesity by Restoring IL-22-Mediated Colonic Health. Cell Host Microbe 2018, 23, 41–53.e4. [Google Scholar] [CrossRef] [Green Version]
- Beilharz, J.E.; Kaakoush, N.O.; Maniam, J.; Morris, M.J. Cafeteria Diet and Probiotic Therapy: Cross Talk among Memory, Neuroplasticity, Serotonin Receptors and Gut Microbiota in the Rat. Mol. Psychiatry 2018, 23, 351–361. [Google Scholar] [CrossRef] [PubMed]
- Hildebrandt, M.A.; Hoffmann, C.; Sherrill-Mix, S.A.; Keilbaugh, S.A.; Hamady, M.; Chen, Y.; Knight, R.; Ahima, R.S.; Bushman, F.; Wu, G.D. High-Fat Diet Determines the Composition of the Murine Gut Microbiome Independently of Obesity. Gastroenterology 2009, 137, 1716–1724.e2. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Walker, A.; Pfitzner, B.; Neschen, S.; Kahle, M.; Harir, M.; Lucio, M.; Moritz, F.; Tziotis, D.; Witting, M.; Rothballer, M.; et al. Distinct Signatures of Host–Microbial Meta-Metabolome and Gut Microbiome in Two C57BL/6 Strains under High-Fat Diet. ISME J. 2014, 8, 2380–2396. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, K.-A.; Gu, W.; Lee, I.-A.; Joh, E.-H.; Kim, D.-H. High Fat Diet-Induced Gut Microbiota Exacerbates Inflammation and Obesity in Mice via the TLR4 Signaling Pathway. PLoS ONE 2012, 7, e47713. [Google Scholar] [CrossRef] [PubMed]
- de La Serre, C.B.; Ellis, C.L.; Lee, J.; Hartman, A.L.; Rutledge, J.C.; Raybould, H.E. Propensity to High-Fat Diet-Induced Obesity in Rats Is Associated with Changes in the Gut Microbiota and Gut Inflammation. Am. J. Physiol.-Gastrointest. Liver Physiol. 2010, 299, G440–G448. [Google Scholar] [CrossRef]
- Lecomte, V.; Kaakoush, N.O.; Maloney, C.A.; Raipuria, M.; Huinao, K.D.; Mitchell, H.M.; Morris, M.J. Changes in Gut Microbiota in Rats Fed a High Fat Diet Correlate with Obesity-Associated Metabolic Parameters. PLoS ONE 2015, 10, e0126931. [Google Scholar] [CrossRef] [Green Version]
- Kovatcheva-Datchary, P.; Nilsson, A.; Akrami, R.; Lee, Y.S.; De Vadder, F.; Arora, T.; Hallen, A.; Martens, E.; Björck, I.; Bäckhed, F. Dietary Fiber-Induced Improvement in Glucose Metabolism Is Associated with Increased Abundance of Prevotella. Cell Metab. 2015, 22, 971–982. [Google Scholar] [CrossRef] [Green Version]
- Wu, G.D.; Chen, J.; Hoffmann, C.; Bittinger, K.; Chen, Y.-Y.; Keilbaugh, S.A.; Bewtra, M.; Knights, D.; Walters, W.A.; Knight, R.; et al. Linking Long-Term Dietary Patterns with Gut Microbial Enterotypes. Science 2011, 334, 105–108. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- So, D.; Whelan, K.; Rossi, M.; Morrison, M.; Holtmann, G.; Kelly, J.T.; Shanahan, E.R.; Staudacher, H.M.; Campbell, K.L. Dietary Fiber Intervention on Gut Microbiota Composition in Healthy Adults: A Systematic Review and Meta-Analysis. Am. J. Clin. Nutr. 2018, 107, 965–983. [Google Scholar] [CrossRef] [Green Version]
- Bibbò, S.; Ianiro, G.; Giorgio, V.; Scaldaferri, F.; Masucci, L.; Gasbarrini, A.; Cammarota, G. The Role of Diet on Gut Microbiota Composition. Eur. Rev. Med. Pharmacol. Sci. 2016, 20, 4742–4749. [Google Scholar] [PubMed]
- Jefferson, A.; Adolphus, K. The Effects of Intact Cereal Grain Fibers, Including Wheat Bran on the Gut Microbiota Composition of Healthy Adults: A Systematic Review. Front. Nutr. 2019, 6, 33. [Google Scholar] [CrossRef] [Green Version]
- Holscher, H.D. Dietary Fiber and Prebiotics and the Gastrointestinal Microbiota. Gut Microbes 2017, 8, 172–184. [Google Scholar] [CrossRef] [PubMed]
- Ramirez-Farias, C.; Slezak, K.; Fuller, Z.; Duncan, A.; Holtrop, G.; Louis, P. Effect of Inulin on the Human Gut Microbiota: Stimulation of Bifidobacterium Adolescentis and Faecalibacterium Prausnitzii. Br. J. Nutr. 2008, 101, 541–550. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De Vuyst, L.; Leroy, F. Cross-Feeding between Bifidobacteria and Butyrate-Producing Colon Bacteria Explains Bifdobacterial Competitiveness, Butyrate Production, and Gas Production. Int. J. Food Microbiol. 2011, 149, 73–80. [Google Scholar] [CrossRef] [PubMed]
- Brandscheid, C.; Schuck, F.; Reinhardt, S.; Schäfer, K.-H.; Pietrzik, C.U.; Grimm, M.; Hartmann, T.; Schwiertz, A.; Endres, K. Altered Gut Microbiome Composition and Tryptic Activity of the 5xFAD Alzheimer’s Mouse Model. J. Alzheimer’s Dis. 2017, 56, 775–788. [Google Scholar] [CrossRef] [PubMed]
- Wu, S.-C.; Cao, Z.-S.; Chang, K.-M.; Juang, J.-L. Intestinal Microbial Dysbiosis Aggravates the Progression of Alzheimer’s Disease in Drosophila. Nat. Commun. 2017, 8, 24. [Google Scholar] [CrossRef]
- Human Microbiome Project Consortium Structure, Function and Diversity of the Healthy Human Microbiome. Nature 2012, 486, 207–214. [CrossRef] [Green Version]
- Sun, B.-L.; Li, W.-W.; Wang, J.; Xu, Y.-L.; Sun, H.-L.; Tian, D.-Y.; Wang, Y.-J.; Yao, X.-Q. Gut Microbiota Alteration and Its Time Course in a Tauopathy Mouse Model. J. Alzheimer’s Dis. 2019, 70, 399–412. [Google Scholar] [CrossRef] [PubMed]
- Bäuerl, C.; Collado, M.C.; Diaz Cuevas, A.; Viña, J.; Pérez Martínez, G. Shifts in Gut Microbiota Composition in an APP/PSS1 Transgenic Mouse Model of Alzheimer’s Disease during Lifespan. Lett. Appl. Microbiol. 2018, 66, 464–471. [Google Scholar] [CrossRef] [PubMed]
- Zhuang, Z.-Q.; Shen, L.-L.; Li, W.-W.; Fu, X.; Zeng, F.; Gui, L.; Lü, Y.; Cai, M.; Zhu, C.; Tan, Y.-L.; et al. Gut Microbiota Is Altered in Patients with Alzheimer’s Disease. J. Alzheimer’s Dis. 2018, 63, 1337–1346. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.; Sun, G.; Feng, T.; Zhang, J.; Huang, X.; Wang, T.; Xie, Z.; Chu, X.; Yang, J.; Wang, H.; et al. Sodium Oligomannate Therapeutically Remodels Gut Microbiota and Suppresses Gut Bacterial Amino Acids-Shaped Neuroinflammation to Inhibit Alzheimer’s Disease Progression. Cell Res. 2019, 29, 787–803. [Google Scholar] [CrossRef]
- Crews, L.; Masliah, E. Molecular Mechanisms of Neurodegeneration in Alzheimer’s Disease. Hum. Mol. Genet. 2010, 19, R12–R20. [Google Scholar] [CrossRef] [PubMed]
- Sochocka, M.; Donskow-Łysoniewska, K.; Diniz, B.S.; Kurpas, D.; Brzozowska, E.; Leszek, J. The Gut Microbiome Alterations and Inflammation-Driven Pathogenesis of Alzheimer’s Disease—A Critical Review. Mol. Neurobiol. 2019, 56, 1841–1851. [Google Scholar] [CrossRef] [Green Version]
- Cattaneo, A.; Cattane, N.; Galluzzi, S.; Provasi, S.; Lopizzo, N.; Festari, C.; Ferrari, C.; Guerra, U.P.; Paghera, B.; Muscio, C.; et al. Association of Brain Amyloidosis with Pro-Inflammatory Gut Bacterial Taxa and Peripheral Inflammation Markers in Cognitively Impaired Elderly. Neurobiol. Aging 2017, 49, 60–68. [Google Scholar] [CrossRef] [Green Version]
- Hill, E.; Clifton, P.; Goodwill, A.M.; Dennerstein, L.; Campbell, S.; Szoeke, C. Dietary Patterns and β-Amyloid Deposition in Aging Australian Women. Alzheimer’s Dement. Transl. Res. Clin. Interv. 2018, 4, 535–541. [Google Scholar] [CrossRef] [PubMed]
- Nagpal, R.; Neth, B.J.; Wang, S.; Craft, S.; Yadav, H. Modified Mediterranean-Ketogenic Diet Modulates Gut Microbiome and Short-Chain Fatty Acids in Association with Alzheimer’s Disease Markers in Subjects with Mild Cognitive Impairment. EBioMedicine 2019, 47, 529–542. [Google Scholar] [CrossRef] [Green Version]
- Neth, B.J.; Mintz, A.; Whitlow, C.; Jung, Y.; Solingapuram Sai, K.; Register, T.C.; Kellar, D.; Lockhart, S.N.; Hoscheidt, S.; Maldjian, J.; et al. Modified Ketogenic Diet Is Associated with Improved Cerebrospinal Fluid Biomarker Profile, Cerebral Perfusion, and Cerebral Ketone Body Uptake in Older Adults at Risk for Alzheimer’s Disease: A Pilot Study. Neurobiol. Aging 2020, 86, 54–63. [Google Scholar] [CrossRef] [PubMed]
- Butterfield, D.A.; Di Domenico, F.; Barone, E. Elevated Risk of Type 2 Diabetes for Development of Alzheimer Disease: A Key Role for Oxidative Stress in Brain. Biochim. Biophys. Acta (BBA) Mol. Basis Dis. 2014, 1842, 1693–1706. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kubis-Kubiak, A.; Dyba, A.; Piwowar, A. The Interplay between Diabetes and Alzheimer’s Disease-In the Hunt for Biomarkers. Int J Mol Sci 2020, 21, 2744. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chaudhuri, J.R.; Mridula, K.R.; Rathnakishore, C.; Anamika, A.; Samala, N.R.; Balaraju, B.; Bandaru, V.S. Association Serum S100B Protein in Alzheimer’s Disease: A Case Control Study from South India. Curr. Alzheimer Res. 2020, 17, 1095–1101. [Google Scholar] [CrossRef] [PubMed]
- Yu, H.; Li, H.; Liu, X.; Du, X.; Deng, B. Levels of Serum S100B Are Associated with Cognitive Dysfunction in Patients with Type 2 Diabetes. Aging 2020, 12, 4193–4203. [Google Scholar] [CrossRef]
- Zhao, L.; Zhang, F.; Ding, X.; Wu, G.; Lam, Y.Y.; Wang, X.; Fu, H.; Xue, X.; Lu, C.; Ma, J.; et al. Gut Bacteria Selectively Promoted by Dietary Fibers Alleviate Type 2 Diabetes. Science 2018, 359, 1151–1156. [Google Scholar] [CrossRef] [Green Version]
- Santos, C.Y.; Snyder, P.J.; Wu, W.-C.; Zhang, M.; Echeverria, A.; Alber, J. Pathophysiologic Relationship between Alzheimer’s Disease, Cerebrovascular Disease, and Cardiovascular Risk: A Review and Synthesis. Alzheimers Dement. 2017, 7, 69–87. [Google Scholar] [CrossRef] [Green Version]
- Tini, G.; Scagliola, R.; Monacelli, F.; La Malfa, G.; Porto, I.; Brunelli, C.; Rosa, G.M. Alzheimer’s Disease and Cardiovascular Disease: A Particular Association. Cardiol. Res. Pract. 2020, 2020, 2617970. [Google Scholar] [CrossRef] [PubMed]
- Moran, C.; Phan, T.G.; Srikanth, V.K. Cerebral Small Vessel Disease: A Review of Clinical, Radiological, and Histopathological Phenotypes. Int. J. Stroke 2012, 7, 36–46. [Google Scholar] [CrossRef]
- Thong, J.Y.J.; Hilal, S.; Wang, Y.; Soon, H.W.; Dong, Y.; Collinson, S.L.; Anh, T.T.; Ikram, M.K.; Wong, T.Y.; Venketasubramanian, N.; et al. Association of Silent Lacunar Infarct with Brain Atrophy and Cognitive Impairment. J. Neurol. Neurosurg. Psychiatry 2013, 84, 1219–1225. [Google Scholar] [CrossRef]
- Love, S.; Miners, J.S. Cerebrovascular Disease in Ageing and Alzheimer’s Disease. Acta Neuropathol. 2016, 131, 645–658. [Google Scholar] [CrossRef] [Green Version]
- Deckers, K.; Schievink, S.H.J.; Rodriquez, M.M.F.; van Oostenbrugge, R.J.; van Boxtel, M.P.J.; Verhey, F.R.J.; Köhler, S. Coronary Heart Disease and Risk for Cognitive Impairment or Dementia: Systematic Review and Meta-Analysis. PLoS ONE 2017, 12, e0184244. [Google Scholar] [CrossRef]
- Wolters, F.J.; Segufa, R.A.; Darweesh, S.K.L.; Bos, D.; Ikram, M.A.; Sabayan, B.; Hofman, A.; Sedaghat, S. Coronary Heart Disease, Heart Failure, and the Risk of Dementia: A Systematic Review and Meta-Analysis. Alzheimer’s Dement. 2018, 14, 1493–1504. [Google Scholar] [CrossRef] [PubMed]
- Stampfer, M.J.; Hu, F.B.; Manson, J.E.; Rimm, E.B.; Willett, W.C. Primary Prevention of Coronary Heart Disease in Women through Diet and Lifestyle. N. Engl. J. Med. 2000, 343, 16–22. [Google Scholar] [CrossRef] [PubMed]
- Rippe, J.M. Lifestyle Strategies for Risk Factor Reduction, Prevention, and Treatment of Cardiovascular Disease. Am. J. Lifestyle Med. 2019, 13, 204–212. [Google Scholar] [CrossRef] [PubMed]
- Kotseva, K.; De Backer, G.; De Bacquer, D.; Rydén, L.; Hoes, A.; Grobbee, D.; Maggioni, A.; Marques-Vidal, P.; Jennings, C.; Abreu, A.; et al. Lifestyle and Impact on Cardiovascular Risk Factor Control in Coronary Patients across 27 Countries: Results from the European Society of Cardiology ESC-EORP EUROASPIRE V Registry. Eur. J. Prev. Cardiol. 2019, 26, 824–835. [Google Scholar] [CrossRef]
- Ludwig, D.S.; Pereira, M.A.; Kroenke, C.H.; Hilner, J.E.; Horn, L.V.; Slattery, M.L.; David, R.; Jacobs, J. Dietary Fiber, Weight Gain, and Cardiovascular Disease Risk Factors in Young Adults. JAMA 1999, 282, 1539–1546. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mozaffarian, D.; Kumanyika, S.K.; Lemaitre, R.N.; Olson, J.L.; Burke, G.L.; Siscovick, D.S. Cereal, Fruit, and Vegetable Fiber Intake and the Risk of Cardiovascular Disease in Elderly Individuals. JAMA 2003, 289, 1659–1666. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lairon, D.; Arnault, N.; Bertrais, S.; Planells, R.; Clero, E.; Hercberg, S.; Boutron-Ruault, M.-C. Dietary Fiber Intake and Risk Factors for Cardiovascular Disease in French Adults. Am. J. Clin. Nutr. 2005, 82, 1185–1194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sahyoun, N.R.; Jacques, P.F.; Zhang, X.L.; Juan, W.; McKeown, N.M. Whole-Grain Intake Is Inversely Associated with the Metabolic Syndrome and Mortality in Older Adults. Am. J. Clin. Nutr. 2006, 83, 124–131. [Google Scholar] [CrossRef] [Green Version]
- Grooms, K.N.; Ommerborn, M.J.; Pham, D.Q.; Djoussé, L.; Clark, C.R. Dietary Fiber Intake and Cardiometabolic Risks among US Adults, NHANES 1999-2010. Am. J. Med. 2013, 126, 1059–1067.e4. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yan, Q.; Gu, Y.; Li, X.; Yang, W.; Jia, L.; Chen, C.; Han, X.; Huang, Y.; Zhao, L.; Li, P.; et al. Alterations of the Gut Microbiome in Hypertension. Front. Cell. Infect. Microbiol. 2017, 7, 381. [Google Scholar] [CrossRef] [Green Version]
- Kristensen, M.; Jensen, M.G.; Aarestrup, J.; Petersen, K.E.; Søndergaard, L.; Mikkelsen, M.S.; Astrup, A. Flaxseed Dietary Fibers Lower Cholesterol and Increase Fecal Fat Excretion, but Magnitude of Effect Depend on Food Type. Nutr. Metab. 2012, 9, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carvalho-Wells, A.L.; Helmolz, K.; Nodet, C.; Molzer, C.; Leonard, C.; McKevith, B.; Thielecke, F.; Jackson, K.G.; Tuohy, K.M. Determination of the in Vivo Prebiotic Potential of a Maize-Based Whole Grain Breakfast Cereal: A Human Feeding Study. Br. J. Nutr. 2010, 104, 1353–1356. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prosky, L.; Asp, N.G.; Schweizer, T.F.; DeVries, J.W.; Furda, I. Determination of Insoluble, Soluble, and Total Dietary Fiber in Foods and Food Products: Interlaboratory Study. J. Assoc. Off. Anal. Chem. 1988, 71, 1017–1023. [Google Scholar] [CrossRef] [PubMed]
- Schneeman, B.O. Soluble vs Insoluble Fiber: Different Physiological Responses. Food Technol. 1987, 41, 81–82. [Google Scholar]
- Pluta, R.; Ułamek-Kozioł, M.; Januszewski, S.; Czuczwar, S.J. Gut Microbiota and pro/Prebiotics in Alzheimer’s Disease. Aging 2020, 12, 5539–5550. [Google Scholar] [CrossRef]
- Chassard, C.; Delmas, E.; Robert, C.; Bernalier-Donadille, A. The Cellulose-Degrading Microbial Community of the Human Gut Varies According to the Presence or Absence of Methanogens. FEMS Microbiol. Ecol. 2010, 74, 205–213. [Google Scholar] [CrossRef]
- Chassard, C.; Delmas, E.; Robert, C.; Lawson, P.A.; Bernalier-Donadille, A. Ruminococcus Champanellensis Sp. Nov., a Cellulose-Degrading Bacterium from Human Gut Microbiota. Int. J. Syst. Evol. Microbiol. 2012, 62, 138–143. [Google Scholar] [CrossRef] [Green Version]
- Robert, C.; Chassard, C.; Lawson, P.A.; Bernalier-Donadille, A. Bacteroides Cellulosilyticus Sp. Nov., a Cellulolytic Bacterium from the Human Gut Microbial Community. Int. J. Syst. Evol. Microbiol. 2007, 57, 1516–1520. [Google Scholar] [CrossRef] [Green Version]
- Wedekind, K.J.; Mansfield, H.R.; Montgomery, L. Enumeration and Isolation of Cellulolytic and Hemicellulolytic Bacteria from Human Feces. Appl. Environ. Microbiol. 1988, 54, 1530–1535. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Niemi, P.; Aura, A.-M.; Maukonen, J.; Smeds, A.I.; Mattila, I.; Niemelä, K.; Tamminen, T.; Faulds, C.B.; Buchert, J.; Poutanen, K. Interactions of a Lignin-Rich Fraction from Brewer’s Spent Grain with Gut Microbiota in Vitro. J. Agric. Food Chem. 2013, 61, 6754–6762. [Google Scholar] [CrossRef]
- Ze, X.; Duncan, S.H.; Louis, P.; Flint, H.J. Ruminococcus Bromii Is a Keystone Species for the Degradation of Resistant Starch in the Human Colon. ISME J. 2012, 6, 1535–1543. [Google Scholar] [CrossRef]
- Liu, F.; Li, P.; Chen, M.; Luo, Y.; Prabhakar, M.; Zheng, H.; He, Y.; Qi, Q.; Long, H.; Zhang, Y. Fructooligosaccharide (FOS) and Galactooligosaccharide (GOS) Increase Bifidobacterium but Reduce Butyrate Producing Bacteria with Adverse Glycemic Metabolism in Healthy Young Population. Sci. Rep. 2017, 7, 11789. [Google Scholar] [CrossRef] [PubMed]
- Tarini, J.; Wolever, T.M.S. The Fermentable Fibre Inulin Increases Postprandial Serum Short-Chain Fatty Acids and Reduces Free-Fatty Acids and Ghrelin in Healthy Subjects. Appl. Physiol. Nutr. Metab. 2010, 35, 9–16. [Google Scholar] [CrossRef] [PubMed]
- Salazar, N.; Dewulf, E.M.; Neyrinck, A.M.; Bindels, L.B.; Cani, P.D.; Mahillon, J.; de Vos, W.M.; Thissen, J.-P.; Gueimonde, M.; de los Reyes-Gavilán, C.G.; et al. Inulin-Type Fructans Modulate Intestinal Bifidobacterium Species Populations and Decrease Fecal Short-Chain Fatty Acids in Obese Women. Clin. Nutr. 2015, 34, 501–507. [Google Scholar] [CrossRef]
- Cardelle-Cobas, A.; Corzo, N.; Olano, A.; Peláez, C.; Requena, T.; Ávila, M. Galactooligosaccharides Derived from Lactose and Lactulose: Influence of Structure on Lactobacillus, Streptococcus and Bifidobacterium Growth. Int. J. Food Microbiol. 2011, 149, 81–87. [Google Scholar] [CrossRef]
- Wang, Y.; Ames, N.P.; Tun, H.M.; Tosh, S.M.; Jones, P.J.; Khafipour, E. High Molecular Weight Barley β-Glucan Alters Gut Microbiota Toward Reduced Cardiovascular Disease Risk. Front. Microbiol. 2016, 7, 129. [Google Scholar] [CrossRef] [Green Version]
- Kristek, A.; Wiese, M.; Heuer, P.; Kosik, O.; Schär, M.Y.; Soycan, G.; Alsharif, S.; Kuhnle, G.G.C.; Walton, G.; Spencer, J.P.E. Oat Bran, but Not Its Isolated Bioactive β-Glucans or Polyphenols, Have a Bifidogenic Effect in an in Vitro Fermentation Model of the Gut Microbiota. Br. J. Nutr. 2019, 121, 549–559. [Google Scholar] [CrossRef] [PubMed]
- Shinohara, K.; Ohashi, Y.; Kawasumi, K.; Terada, A.; Fujisawa, T. Effect of Apple Intake on Fecal Microbiota and Metabolites in Humans. Anaerobe 2010, 16, 510–515. [Google Scholar] [CrossRef]
- Calame, W.; Weseler, A.R.; Viebke, C.; Flynn, C.; Siemensma, A.D. Gum Arabic Establishes Prebiotic Functionality in Healthy Human Volunteers in a Dose-Dependent Manner. Br. J. Nutr. 2008, 100, 1269–1275. [Google Scholar] [CrossRef]
- Maier, T.V.; Lucio, M.; Lee, L.H.; VerBerkmoes, N.C.; Brislawn, C.J.; Bernhardt, J.; Lamendella, R.; McDermott, J.E.; Bergeron, N.; Heinzmann, S.S.; et al. Impact of Dietary Resistant Starch on the Human Gut Microbiome, Metaproteome, and Metabolome. mBio 2017, 8, e01343-17. [Google Scholar] [CrossRef] [Green Version]
- Biedrzycka, E.; Bielecka, M. Prebiotic Effectiveness of Fructans of Different Degrees of Polymerization. Trends Food Sci. Technol. 2004, 15, 170–175. [Google Scholar] [CrossRef]
- Moro, G.; Minoli, I.; Mosca, M.; Fanaro, S.; Jelinek, J.; Stahl, B.; Boehm, G. Dosage-Related Bifidogenic Effects of Galacto- and Fructooligosaccharides in Formula-Fed Term Infants. J. Pediatric Gastroenterol. Nutr. 2002, 34, 291. [Google Scholar] [CrossRef]
- Austin, S.; Bénet, T.; Michaud, J.; Cuany, D.; Rohfritsch, P. Determination of β-Galactooligosaccharides by Liquid Chromatography. Available online: https://www.hindawi.com/journals/ijac/2014/768406/ (accessed on 12 February 2019).
- Grabarics, M.; Csernák, O.; Balogh, R.; Béni, S. Analytical Characterization of Human Milk Oligosaccharides—Potential Applications in Pharmaceutical Analysis. J. Pharm. Biomed. Anal. 2017, 146, 168–178. [Google Scholar] [CrossRef] [PubMed]
- Zivkovic, A.; Lewis, Z.; German, B.; Mills, D. Establishment of a Milk-Oriented-Microbiota (MOM) in Early Life: How Babies Meet Their MOMs. Food Rev. Int. 2013, 5, 1–13. [Google Scholar] [CrossRef]
- Zivkovic, A.M.; German, J.B.; Lebrilla, C.B.; Mills, D.A. Human Milk Glycobiome and Its Impact on the Infant Gastrointestinal Microbiota. Proc. Natl. Acad. Sci. USA 2011, 108, 4653–4658. [Google Scholar] [CrossRef] [Green Version]
- Kleessen, B.; Bunke, H.; Tovar, K.; Noack, J.; Sawatzki, G. Influence of Two Infant Formulas and Human Milk on the Development of the Faecal Flora in Newborn Infants. Acta Paediatr. 1995, 84, 1347–1356. [Google Scholar] [CrossRef] [PubMed]
- Martín, R.; Langa, S.; Reviriego, C.; Jimínez, E.; Marín, M.L.; Xaus, J.; Fernández, L.; Rodríguez, J.M. Human Milk Is a Source of Lactic Acid Bacteria for the Infant Gut. J. Pediatrics 2003, 143, 754–758. [Google Scholar] [CrossRef] [PubMed]
- Marques, T.M.; Wall, R.; Ross, R.P.; Fitzgerald, G.F.; Ryan, C.A.; Stanton, C. Programming Infant Gut Microbiota: Influence of Dietary and Environmental Factors. Curr. Opin. Biotechnol. 2010, 21, 149–156. [Google Scholar] [CrossRef]
- Zhang, Y.; Wang, P.; Xia, C.; Wu, Z.; Zhong, Z.; Xu, Y.; Zeng, Y.; Liu, H.; Liu, R.; Liao, M. Fructooligosaccharides Supplementation Mitigated Chronic Stress-Induced Intestinal Barrier Impairment and Neuroinflammation in Mice. J. Funct. Foods 2020, 72, 104060. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Johansson, L.; Karesoja, M.; Ekholm, P.; Virkki, L.; Tenhu, H. Comparison of the Solution Properties of (1→3),(1→4)-β-d-Glucans Extracted from Oats and Barley. LWT Food Sci. Technol. 2008, 41, 180–184. [Google Scholar] [CrossRef]
- Regand, A.; Chowdhury, Z.; Tosh, S.M.; Wolever, T.M.S.; Wood, P. The Molecular Weight, Solubility and Viscosity of Oat Beta-Glucan Affect Human Glycemic Response by Modifying Starch Digestibility. Food Chem. 2011, 129, 297–304. [Google Scholar] [CrossRef] [PubMed]
- Lazaridou, A.; Biliaderis, C.G. Molecular Aspects of Cereal β-Glucan Functionality: Physical Properties, Technological Applications and Physiological Effects. J. Cereal Sci. 2007, 46, 101–118. [Google Scholar] [CrossRef]
- Arena, M.P.; Caggianiello, G.; Fiocco, D.; Russo, P.; Torelli, M.; Spano, G.; Capozzi, V. Barley β-Glucans-Containing Food Enhances Probiotic Performances of Beneficial Bacteria. Int. J. Mol. Sci. 2014, 15, 3025–3039. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mohnen, D. Pectin Structure and Biosynthesis. Curr. Opin. Plant Biol. 2008, 11, 266–277. [Google Scholar] [CrossRef] [PubMed]
- Wei, Y.; Gong, J.; Zhu, W.; Tian, H.; Ding, C.; Gu, L.; Li, N.; Li, J. Pectin Enhances the Effect of Fecal Microbiota Transplantation in Ulcerative Colitis by Delaying the Loss of Diversity of Gut Flora. BMC Microbiol. 2016, 16, 255. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Churms, S.C.; Merrifield, E.H.; Stephen, A.M. Some New Aspects of the Molecular Structure of Acacia Senegal Gum (Gum Arabic). Carbohydr. Res. 1983, 123, 267–279. [Google Scholar] [CrossRef]
- Sanchez, C.; Schmitt, C.; Kolodziejczyk, E.; Lapp, A.; Gaillard, C.; Renard, D. The Acacia Gum Arabinogalactan Fraction Is a Thin Oblate Ellipsoid: A New Model Based on Small-Angle Neutron Scattering and Ab Initio Calculation. Biophys. J. 2008, 94, 629–639. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roediger, W.E. Role of Anaerobic Bacteria in the Metabolic Welfare of the Colonic Mucosa in Man. Gut 1980, 21, 793–798. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cummings, J.H.; Pomare, E.W.; Branch, W.J.; Naylor, C.P.; Macfarlane, G.T. Short Chain Fatty Acids in Human Large Intestine, Portal, Hepatic and Venous Blood. Gut 1987, 28, 1221–1227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kau, A.L.; Ahern, P.P.; Griffin, N.W.; Goodman, A.L.; Gordon, J.I. Human Nutrition, the Gut Microbiome and the Immune System. Nature 2011, 474, 327–336. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Slavin, J. Fiber and Prebiotics: Mechanisms and Health Benefits. Nutrients 2013, 5, 1417–1435. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lupton, J.R. Microbial Degradation Products Influence Colon Cancer Risk: The Butyrate Controversy. J. Nutr. 2004, 134, 479–482. [Google Scholar] [CrossRef] [Green Version]
- van Limpt, C.; Crienen, A.; Vriesema, A.; Knol, J. 134 Effect of Colonic Short Chain Fatty Acids, Lactate and PH on The Growth of Common Gut Pathogens. Pediatric Res. 2004, 56, 487. [Google Scholar] [CrossRef] [Green Version]
- Parada Venegas, D.; De la Fuente, M.K.; Landskron, G.; González, M.J.; Quera, R.; Dijkstra, G.; Harmsen, H.J.M.; Faber, K.N.; Hermoso, M.A. Short Chain Fatty Acids (SCFAs)-Mediated Gut Epithelial and Immune Regulation and Its Relevance for Inflammatory Bowel Diseases. Front. Immunol. 2019, 10, 277. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dass, N.B.; John, A.K.; Bassil, A.K.; Crumbley, C.W.; Shehee, W.R.; Maurio, F.P.; Moore, G.B.T.; Taylor, C.M.; Sanger, G.J. The Relationship between the Effects of Short-Chain Fatty Acids on Intestinal Motility in Vitro and GPR43 Receptor Activation. Neurogastroenterol. Motil. 2007, 19, 66–74. [Google Scholar] [CrossRef]
- Thangaraju, M.; Cresci, G.A.; Liu, K.; Ananth, S.; Gnanaprakasam, J.P.; Browning, D.D.; Mellinger, J.D.; Smith, S.B.; Digby, G.J.; Lambert, N.A.; et al. GPR109A Is a G-Protein–Coupled Receptor for the Bacterial Fermentation Product Butyrate and Functions as a Tumor Suppressor in Colon. Cancer Res. 2009, 69, 2826–2832. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Docampo, M.D.; Stein-Thoeringer, C.K.; Lazrak, A.; Burgos da Silva, M.D.; Cross, J.; van den Brink, M.R.M. Expression of the Butyrate/Niacin Receptor, GPR109a on T Cells Plays an Important Role in a Mouse Model of Graft Versus Host Disease. Blood 2018, 132, 61. [Google Scholar] [CrossRef]
- Fu, S.-P.; Wang, J.-F.; Xue, W.-J.; Liu, H.-M.; Liu, B.; Zeng, Y.-L.; Li, S.-N.; Huang, B.-X.; Lv, Q.-K.; Wang, W.; et al. Anti-Inflammatory Effects of BHBA in Both in Vivo and in Vitro Parkinson’s Disease Models Are Mediated by GPR109A-Dependent Mechanisms. J. Neuroinflammation 2015, 12, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Singh, N.; Gurav, A.; Sivaprakasam, S.; Brady, E.; Padia, R.; Shi, H.; Thangaraju, M.; Prasad, P.D.; Manicassamy, S.; Munn, D.H.; et al. Activation of Gpr109a, Receptor for Niacin and the Commensal Metabolite Butyrate, Suppresses Colonic Inflammation and Carcinogenesis. Immunity 2014, 40, 128–139. [Google Scholar] [CrossRef] [Green Version]
- Bellono, N.W.; Bayrer, J.R.; Leitch, D.B.; Castro, J.; Zhang, C.; O’Donnell, T.A.; Brierley, S.M.; Ingraham, H.A.; Julius, D. Enterochromaffin Cells Are Gut Chemosensors That Couple to Sensory Neural Pathways. Cell 2017, 170, 185–198.e16. [Google Scholar] [CrossRef] [Green Version]
- Chen, Z.; Luo, J.; Li, J.; Kim, G.; Stewart, A.; Urban, J.F.; Huang, Y.; Chen, S.; Wu, L.-G.; Chesler, A.; et al. Interleukin-33 Promotes Serotonin Release from Enterochromaffin Cells for Intestinal Homeostasis. Immunity 2021, 54, 151–163.e6. [Google Scholar] [CrossRef] [PubMed]
- Yano, J.M.; Yu, K.; Donaldson, G.P.; Shastri, G.G.; Ann, P.; Ma, L.; Nagler, C.R.; Ismagilov, R.F.; Mazmanian, S.K.; Hsiao, E.Y. Indigenous Bacteria from the Gut Microbiota Regulate Host Serotonin Biosynthesis. Cell 2015, 161, 264–276. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Clarke, G.; Grenham, S.; Scully, P.; Fitzgerald, P.; Moloney, R.D.; Shanahan, F.; Dinan, T.G.; Cryan, J.F. The Microbiome-Gut-Brain Axis during Early Life Regulates the Hippocampal Serotonergic System in a Sex-Dependent Manner. Mol. Psychiatry 2013, 18, 666–673. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Berger, M.; Gray, J.A.; Roth, B.L. The Expanded Biology of Serotonin. Annu. Rev. Med. 2009, 60, 355–366. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brambilla, P.; Perez, J.; Barale, F.; Schettini, G.; Soares, J.C. GABAergic Dysfunction in Mood Disorders. Mol. Psychiatry 2003, 8, 721–737. [Google Scholar] [CrossRef] [Green Version]
- Strandwitz, P.; Kim, K.H.; Terekhova, D.; Liu, J.K.; Sharma, A.; Levering, J.; McDonald, D.; Dietrich, D.; Ramadhar, T.R.; Lekbua, A.; et al. GABA-Modulating Bacteria of the Human Gut Microbiota. Nat. Microbiol. 2019, 4, 396–403. [Google Scholar] [CrossRef] [PubMed]
- Zheng, P.; Zeng, B.; Liu, M.; Chen, J.; Pan, J.; Han, Y.; Liu, Y.; Cheng, K.; Zhou, C.; Wang, H.; et al. The Gut Microbiome from Patients with Schizophrenia Modulates the Glutamate-Glutamine-GABA Cycle and Schizophrenia-Relevant Behaviors in Mice. Sci. Adv. 2019, 5, eaau8317. [Google Scholar] [CrossRef] [Green Version]
- Strandwitz, P. Neurotransmitter Modulation by the Gut Microbiota. Brain Res. 2018, 1693, 128–133. [Google Scholar] [CrossRef]
- Sherry, C.L.; Kim, S.S.; Dilger, R.N.; Bauer, L.L.; Moon, M.L.; Tapping, R.I.; Fahey, G.C.; Tappenden, K.A.; Freund, G.G. Sickness Behavior Induced by Endotoxin Can Be Mitigated by the Dietary Soluble Fiber, Pectin, through up-Regulation of IL-4 and Th2 Polarization. Brain Behav. Immun. 2010, 24, 631–640. [Google Scholar] [CrossRef] [Green Version]
- Matt, S.M.; Allen, J.M.; Lawson, M.A.; Mailing, L.J.; Woods, J.A.; Johnson, R.W. Butyrate and Dietary Soluble Fiber Improve Neuroinflammation Associated With Aging in Mice. Front. Immunol. 2018, 9, 1832. [Google Scholar] [CrossRef] [PubMed]
- Yap, Y.A.; Mariño, E. An Insight Into the Intestinal Web of Mucosal Immunity, Microbiota, and Diet in Inflammation. Front Immunol 2018, 9, 2617. [Google Scholar] [CrossRef]
- Schroeder, B.O.; Birchenough, G.M.H.; Ståhlman, M.; Arike, L.; Johansson, M.E.V.; Hansson, G.C.; Bäckhed, F. Bifidobacteria or Fiber Protects against Diet-Induced Microbiota-Mediated Colonic Mucus Deterioration. Cell Host Microbe 2018, 23, 27–40.e7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Desai, M.S.; Seekatz, A.M.; Koropatkin, N.M.; Kamada, N.; Hickey, C.A.; Wolter, M.; Pudlo, N.A.; Kitamoto, S.; Terrapon, N.; Muller, A.; et al. A Dietary Fiber-Deprived Gut Microbiota Degrades the Colonic Mucus Barrier and Enhances Pathogen Susceptibility. Cell 2016, 167, 1339–1353.e21. [Google Scholar] [CrossRef] [Green Version]
- Ruas-Madiedo, P.; Gueimonde, M.; Fernández-García, M.; de los Reyes-Gavilán, C.G.; Margolles, A. Mucin Degradation by Bifidobacterium Strains Isolated from the Human Intestinal Microbiota. Appl. Environ. Microbiol. 2008, 74, 1936–1940. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yoshihara, T.; Oikawa, Y.; Kato, T.; Kessoku, T.; Kobayashi, T.; Kato, S.; Misawa, N.; Ashikari, K.; Fuyuki, A.; Ohkubo, H.; et al. The Protective Effect of Bifidobacterium Bifidum G9-1 against Mucus Degradation by Akkermansia Muciniphila Following Small Intestine Injury Caused by a Proton Pump Inhibitor and Aspirin. Gut Microbes 2020, 11, 1385–1404. [Google Scholar] [CrossRef] [PubMed]
- Ottman, N.; Geerlings, S.Y.; Aalvink, S.; de Vos, W.M.; Belzer, C. Action and Function of Akkermansia Muciniphila in Microbiome Ecology, Health and Disease. Best Pract. Res. Clin. Gastroenterol. 2017, 31, 637–642. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Plovier, H.; Everard, A.; Druart, C.; Depommier, C.; Van Hul, M.; Geurts, L.; Chilloux, J.; Ottman, N.; Duparc, T.; Lichtenstein, L.; et al. A Purified Membrane Protein from Akkermansia Muciniphila or the Pasteurized Bacterium Improves Metabolism in Obese and Diabetic Mice. Nat. Med. 2017, 23, 107–113. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Depommier, C.; Everard, A.; Druart, C.; Plovier, H.; Van Hul, M.; Vieira-Silva, S.; Falony, G.; Raes, J.; Maiter, D.; Delzenne, N.M.; et al. Supplementation with Akkermansia Muciniphila in Overweight and Obese Human Volunteers: A Proof-of-Concept Exploratory Study. Nat. Med. 2019, 25, 1096–1103. [Google Scholar] [CrossRef]
- Xu, Y.; Wang, N.; Tan, H.-Y.; Li, S.; Zhang, C.; Feng, Y. Function of Akkermansia Muciniphila in Obesity: Interactions With Lipid Metabolism, Immune Response and Gut Systems. Front. Microbiol. 2020, 11, 219. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heintz-Buschart, A.; Pandey, U.; Wicke, T.; Sixel-Döring, F.; Janzen, A.; Sittig-Wiegand, E.; Trenkwalder, C.; Oertel, W.H.; Mollenhauer, B.; Wilmes, P. The Nasal and Gut Microbiome in Parkinson’s Disease and Idiopathic Rapid Eye Movement Sleep Behavior Disorder. Mov. Disord. 2018, 33, 88–98. [Google Scholar] [CrossRef] [Green Version]
- Cani, P.D. Human Gut Microbiome: Hopes, Threats and Promises. Gut 2018, 67, 1716–1725. [Google Scholar] [CrossRef]
- Peng, L.; He, Z.; Chen, W.; Holzman, I.R.; Lin, J. Effects of Butyrate on Intestinal Barrier Function in a Caco-2 Cell Monolayer Model of Intestinal Barrier. Pediatric Res. 2007, 61, 37–41. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, H.-B.; Wang, P.-Y.; Wang, X.; Wan, Y.-L.; Liu, Y.-C. Butyrate Enhances Intestinal Epithelial Barrier Function via Up-Regulation of Tight Junction Protein Claudin-1 Transcription. Dig. Dis. Sci. 2012, 57, 3126–3135. [Google Scholar] [CrossRef] [PubMed]
- Peng, L.; Li, Z.-R.; Green, R.S.; Holzman, I.R.; Lin, J. Butyrate Enhances the Intestinal Barrier by Facilitating Tight Junction Assembly via Activation of AMP-Activated Protein Kinase in Caco-2 Cell Monolayers. J. Nutr. 2009, 139, 1619–1625. [Google Scholar] [CrossRef] [PubMed]
- Bourassa, M.W.; Alim, I.; Bultman, S.J.; Ratan, R.R. Butyrate, Neuroepigenetics and the Gut Microbiome: Can a High Fiber Diet Improve Brain Health? Neurosci. Lett. 2016, 625, 56–63. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Friedland, R.P.; Budinger, T.F.; Ganz, E.; Yano, Y.; Mathis, C.A.; Koss, B.; Ober, B.A.; Huesman, R.H.; Derenzo, S.E. Regional Cerebral Metabolic Alterations in Dementia of the Alzheimer Type: Positron Emission Tomography with [18F]Fluorodeoxyglucose. J. Comput. Assist. Tomogr. 1983, 7, 590–598. [Google Scholar] [CrossRef]
- Mosconi, L.; Pupi, A.; De Leon, M.J. Brain Glucose Hypometabolism and Oxidative Stress in Preclinical Alzheimer’s Disease. Ann. N. Y. Acad. Sci. 2008, 1147, 180–195. [Google Scholar] [CrossRef] [PubMed]
- Shimada, Y.; Kinoshita, M.; Harada, K.; Mizutani, M.; Masahata, K.; Kayama, H.; Takeda, K. Commensal Bacteria-Dependent Indole Production Enhances Epithelial Barrier Function in the Colon. PLoS ONE 2013, 8, e80604. [Google Scholar] [CrossRef] [Green Version]
- Venkatesh, M.; Mukherjee, S.; Wang, H.; Li, H.; Sun, K.; Benechet, A.P.; Qiu, Z.; Maher, L.; Redinbo, M.R.; Phillips, R.S.; et al. Symbiotic Bacterial Metabolites Regulate Gastrointestinal Barrier Function via the Xenobiotic Sensor PXR and Toll-like Receptor 4. Immunity 2014, 41, 296–310. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, J.; Zhang, L.; Wu, T.; Li, Y.; Zhou, X.; Ruan, Z. Indole-3-Propionic Acid Improved the Intestinal Barrier by Enhancing Epithelial Barrier and Mucus Barrier. J. Agric. Food Chem. 2021, 69, 1487–1495. [Google Scholar] [CrossRef] [PubMed]
- Gheorghe, C.E.; Martin, J.A.; Manriquez, F.V.; Dinan, T.G.; Cryan, J.F.; Clarke, G. Focus on the Essentials: Tryptophan Metabolism and the Microbiome-Gut-Brain Axis. Curr. Opin. Pharmacol. 2019, 48, 137–145. [Google Scholar] [CrossRef] [PubMed]
- Pappolla, M.A.; Perry, G.; Fang, X.; Zagorski, M.; Sambamurti, K.; Poeggeler, B. Indoles as Essential Mediators in the Gut-Brain Axis. Their Role in Alzheimer’s Disease. Neurobiol. Dis. 2021, 156, 105403. [Google Scholar] [CrossRef] [PubMed]
- Hwang, I.K.; Yoo, K.-Y.; Li, H.; Park, O.K.; Lee, C.H.; Choi, J.H.; Jeong, Y.-G.; Lee, Y.L.; Kim, Y.-M.; Kwon, Y.-G.; et al. Indole-3-Propionic Acid Attenuates Neuronal Damage and Oxidative Stress in the Ischemic Hippocampus. J. Neurosci. Res. 2009, 87, 2126–2137. [Google Scholar] [CrossRef]
- Bozner, P.; Grishko, V.; LeDoux, S.P.; Wilson, G.L.; Chyan, Y.-C.; Pappolla, M.A. The Amyloid β Protein Induces Oxidative Damage of Mitochondrial DNA. J. Neuropathol. Exp. Neurol. 1997, 56, 1356–1362. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Poeggeler, B.; Sambamurti, K.; Siedlak, S.L.; Perry, G.; Smith, M.A.; Pappolla, M.A. A Novel Endogenous Indole Protects Rodent Mitochondria and Extends Rotifer Lifespan. PLoS ONE 2010, 5, e10206. [Google Scholar] [CrossRef] [Green Version]
- Jaglin, M.; Rhimi, M.; Philippe, C.; Pons, N.; Bruneau, A.; Goustard, B.; Daugé, V.; Maguin, E.; Naudon, L.; Rabot, S. Indole, a Signaling Molecule Produced by the Gut Microbiota, Negatively Impacts Emotional Behaviors in Rats. Front. Neurosci. 2018, 12, 216. [Google Scholar] [CrossRef]
- Ohtsuki, S.; Asaba, H.; Takanaga, H.; Deguchi, T.; Hosoya, K.; Otagiri, M.; Terasaki, T. Role of Blood–Brain Barrier Organic Anion Transporter 3 (OAT3) in the Efflux of Indoxyl Sulfate, a Uremic Toxin: Its Involvement in Neurotransmitter Metabolite Clearance from the Brain. J. Neurochem. 2002, 83, 57–66. [Google Scholar] [CrossRef]
- Watanabe, K.; Watanabe, T.; Nakayama, M. Cerebro-Renal Interactions: Impact of Uremic Toxins on Cognitive Function. NeuroToxicology 2014, 44, 184–193. [Google Scholar] [CrossRef]
- Molinero, N.; Ruiz, L.; Sánchez, B.; Margolles, A.; Delgado, S. Intestinal Bacteria Interplay with Bile and Cholesterol Metabolism: Implications on Host Physiology. Front. Physiol. 2019, 10, 185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, I.; Ahn, S.-H.; Inagaki, T.; Choi, M.; Ito, S.; Guo, G.L.; Kliewer, S.A.; Gonzalez, F.J. Differential Regulation of Bile Acid Homeostasis by the Farnesoid X Receptor in Liver and Intestine. J. Lipid Res. 2007, 48, 2664–2672. [Google Scholar] [CrossRef] [Green Version]
- MahmoudianDehkordi, S.; Arnold, M.; Nho, K.; Ahmad, S.; Jia, W.; Xie, G.; Louie, G.; Kueider-Paisley, A.; Moseley, M.A.; Thompson, J.W.; et al. Altered Bile Acid Profile Associates with Cognitive Impairment in Alzheimer’s Disease—An Emerging Role for Gut Microbiome. Alzheimer’s Dement. 2019, 15, 76–92. [Google Scholar] [CrossRef] [PubMed]
- Bennett, D.A.; Buchman, A.S.; Boyle, P.A.; Barnes, L.L.; Wilson, R.S.; Schneider, J.A. Religious Orders Study and Rush Memory and Aging Project. J. Alzheimers Dis. 2018, 64, S161–S189. [Google Scholar] [CrossRef]
- Zhu, C.; Sawrey-Kubicek, L.; Beals, E.; Rhodes, C.H.; Houts, H.E.; Sacchi, R.; Zivkovic, A.M. Human Gut Microbiome Composition and Tryptophan Metabolites Were Changed Differently by Fast Food and Mediterranean Diet in 4 Days: A Pilot Study. Nutr. Res. 2020, 77, 62–72. [Google Scholar] [CrossRef]
- Hebert, J.C.; Radford-Smith, D.E.; Probert, F.; Ilott, N.; Chan, K.W.; Anthony, D.C.; Burnet, P.W.J. Mom’s Diet Matters: Maternal Prebiotic Intake in Mice Reduces Anxiety and Alters Brain Gene Expression and the Fecal Microbiome in Offspring. Brain Behav. Immun. 2021, 91, 230–244. [Google Scholar] [CrossRef] [PubMed]
- Burokas, A.; Arboleya, S.; Moloney, R.D.; Peterson, V.L.; Murphy, K.; Clarke, G.; Stanton, C.; Dinan, T.G.; Cryan, J.F. Targeting the Microbiota-Gut-Brain Axis: Prebiotics Have Anxiolytic and Antidepressant-like Effects and Reverse the Impact of Chronic Stress in Mice. Biol. Psychiatry 2017, 82, 472–487. [Google Scholar] [CrossRef] [PubMed]
- Chunchai, T.; Thunapong, W.; Yasom, S.; Wanchai, K.; Eaimworawuthikul, S.; Metzler, G.; Thiennimitr, P.; Sirilun, S.; Chaiyasut, C.; Lungkaphin, A.; et al. PREBIOTICS, PROBIOTICS OR SYNBIOTICS THERAPY RESTORES COGNITIVE DECLINE IN OBESE RATS. Alzheimer’s Dement. 2017, 13, P1265–P1266. [Google Scholar] [CrossRef]
- Liu, Q.; Xi, Y.; Wang, Q.; Liu, J.; Li, P.; Meng, X.; Liu, K.; Chen, W.; Liu, X.; Liu, Z. Mannan Oligosaccharide Attenuates Cognitive and Behavioral Disorders in the 5xFAD Alzheimer’s Disease Mouse Model via Regulating the Gut Microbiota-Brain Axis. Brain Behav. Immun. 2021, 95, 330–343. [Google Scholar] [CrossRef]
- Grimaldi, R.; Gibson, G.R.; Vulevic, J.; Giallourou, N.; Castro-Mejía, J.L.; Hansen, L.H.; Leigh Gibson, E.; Nielsen, D.S.; Costabile, A. A Prebiotic Intervention Study in Children with Autism Spectrum Disorders (ASDs). Microbiome 2018, 6, 133. [Google Scholar] [CrossRef] [PubMed]
- Silk, D.B.A.; Davis, A.; Vulevic, J.; Tzortzis, G.; Gibson, G.R. Clinical Trial: The Effects of a Trans-Galactooligosaccharide Prebiotic on Faecal Microbiota and Symptoms in Irritable Bowel Syndrome. Aliment. Pharmacol. Ther. 2009, 29, 508–518. [Google Scholar] [CrossRef] [PubMed]
- Azpiroz, F.; Dubray, C.; Bernalier-Donadille, A.; Cardot, J.-M.; Accarino, A.; Serra, J.; Wagner, A.; Respondek, F.; Dapoigny, M. Effects of ScFOS on the Composition of Fecal Microbiota and Anxiety in Patients with Irritable Bowel Syndrome: A Randomized, Double Blind, Placebo Controlled Study. Neurogastroenterol. Motil. 2017, 29, e12911. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, A.P.; 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. [Google Scholar] [CrossRef]
- Leyrolle, Q.; Cserjesi, R.; Mulders, M.D.; Zamariola, G.; Hiel, S.; Gianfrancesco, M.A.; Portheault, D.; Amadieu, C.; Bindels, L.B.; Leclercq, S.; et al. Prebiotic Effect on Mood in Obese Patients Is Determined by the Initial Gut Microbiota Composition: A Randomized, Controlled Trial. Brain Behav. Immun. 2021, 94, 289–298. [Google Scholar] [CrossRef] [PubMed]
- Gibson, G.R.; Beatty, E.R.; Wang, X.; Cummings, J.H. Selective Stimulation of Bifidobacteria in the Human Colon by Oligofructose and Inulin. Gastroenterology 1995, 108, 975–982. [Google Scholar] [CrossRef]
- Savignac, H.M.; Kiely, B.; Dinan, T.G.; Cryan, J.F. Bifidobacteria Exert Strain-Specific Effects on Stress-Related Behavior and Physiology in BALB/c Mice. Neurogastroenterol. Motil. 2014, 26, 1615–1627. [Google Scholar] [CrossRef]
- Savignac, H.M.; Tramullas, M.; Kiely, B.; Dinan, T.G.; Cryan, J.F. Bifidobacteria Modulate Cognitive Processes in an Anxious Mouse Strain. Behav. Brain Res. 2015, 287, 59–72. [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] [PubMed] [Green Version]
- Talbott, S.; Talbott, J. Effect of BETA 1, 3/1, 6 GLUCAN on Upper Respiratory Tract Infection Symptoms and Mood State in Marathon Athletes. J. Sports Sci. Med. 2009, 8, 509–515. [Google Scholar]
- Talbott, S.M.; Talbott, J.A. Baker’s Yeast Beta-Glucan Supplement Reduces Upper Respiratory Symptoms and Improves Mood State in Stressed Women. J. Am. Coll. Nutr. 2012, 31, 295–300. [Google Scholar] [CrossRef] [PubMed]
- Best, T.; Kemps, E.; Bryan, J. Saccharide Effects on Cognition and Well-Being in Middle-Aged Adults: A Randomized Controlled Trial. Dev. Neuropsychol. 2009, 35, 66–80. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Best, T.; Howe, P.; Bryan, J.; Buckley, J.; Scholey, A. Acute Effects of a Dietary Non-Starch Polysaccharide Supplement on Cognitive Performance in Healthy Middle-Aged Adults. Nutr. Neurosci. 2015, 18, 76–86. [Google Scholar] [CrossRef] [PubMed]
- Berding, K.; Long-Smith, C.M.; Carbia, C.; Bastiaanssen, T.F.S.; van de Wouw, M.; Wiley, N.; Strain, C.R.; Fouhy, F.; Stanton, C.; Cryan, J.F.; et al. A Specific Dietary Fibre Supplementation Improves Cognitive Performance-an Exploratory Randomised, Placebo-Controlled, Crossover Study. Psychopharmacology 2021, 238, 149–163. [Google Scholar] [CrossRef] [PubMed]
- Prasad, S.; Dhiman, R.K.; Duseja, A.; Chawla, Y.K.; Sharma, A.; Agarwal, R. Lactulose Improves Cognitive Functions and Health-Related Quality of Life in Patients with Cirrhosis Who Have Minimal Hepatic Encephalopathy. Hepatology 2007, 45, 549–559. [Google Scholar] [CrossRef] [PubMed]
Fiber Types | Main Features | Natural/Food Sources | Associated Gut Microbiota | References |
---|---|---|---|---|
Cellulose | Bulking | Plant cell wall | Ruminococcus spp. Bacteroides spp. | [78,79,80] |
Hemicellulose | Bulking | Plant cell wall | Butyrivibrio spp. Clostridium spp. Bacteroides spp. | [81] |
Lignin | Bulking | Plant cell wall | Bifidobacterium spp. | [82] |
Resistant Starch | Fermentable | Seeds and unprocessed whole grains | Bifidobacterium spp. Ruminococcus spp. | [83] |
Fructan | ||||
Fructo-oligosaccharide (FOS) | Fermentable | Jerusalem artichoke, chicory, and the Blue Agave | Bifidobacterium spp. | [84] |
Inulin | Fermentable | Wheat, bananas, asparagus, Jerusalem artichoke, and chicory | Bifidobacterium spp. | [85,86] |
Galacto-oligosaccharide (GOS) | Fermentable | Enzymatic conversion of lactose, added in infant formula | Bifidobacterium spp. Lactobacillus spp. | [87] |
β-glucan | Viscous, Fermentable | Bran of cereals such as oats and barley | Bacteroides spp. Prevotella spp. Bifidobacterium spp. | [88,89] |
Pectin | Viscous, Fermentable | Pears, apples, berries, and oranges | Bifidobacterium spp. Lactobacillus spp. Enterococcus spp. | [90] |
Gums (gum arabic) | Viscous, Fermentable | Substances that are secreted from plant cells in response to injury (gum arabic) | Bifidobacterium spp. Lactobacillus spp. Bacteroides spp. | [91] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kang, J.W.; Zivkovic, A.M. The Potential Utility of Prebiotics to Modulate Alzheimer’s Disease: A Review of the Evidence. Microorganisms 2021, 9, 2310. https://doi.org/10.3390/microorganisms9112310
Kang JW, Zivkovic AM. The Potential Utility of Prebiotics to Modulate Alzheimer’s Disease: A Review of the Evidence. Microorganisms. 2021; 9(11):2310. https://doi.org/10.3390/microorganisms9112310
Chicago/Turabian StyleKang, Jea Woo, and Angela M. Zivkovic. 2021. "The Potential Utility of Prebiotics to Modulate Alzheimer’s Disease: A Review of the Evidence" Microorganisms 9, no. 11: 2310. https://doi.org/10.3390/microorganisms9112310
APA StyleKang, J. W., & Zivkovic, A. M. (2021). The Potential Utility of Prebiotics to Modulate Alzheimer’s Disease: A Review of the Evidence. Microorganisms, 9(11), 2310. https://doi.org/10.3390/microorganisms9112310