Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-28T13:40:58.878Z Has data issue: false hasContentIssue false
  • English
  • Français

Nourishing the gut microbiota: The potential of prebiotics in microbiota-gut-brain axis research

Published online by Cambridge University Press:  15 July 2019

Boushra Dalile ,
Kristin Verbeke ,
Lukas Van Oudenhove  and
Bram Vervliet Open the ORCID record for Bram Vervliet [Opens in a new window]
Boushra Dalile
Affiliation:
Laboratory of Digestion and Absorption, Translational Research in GastroIntestinal Disorders (TARGID), Department of Chronic Diseases, Metabolism, and Ageing, Faculty of Medicine, KU Leuven, 3000 Leuven, Belgium. boushra.dalile@kuleuven.bekristin.verbeke@kuleuven.behttps://www.kuleuven.be/wieiswie/en/person/00115135https://www.kuleuven.be/wieiswie/en/person/00018368
Kristin Verbeke
Affiliation:
Laboratory of Digestion and Absorption, Translational Research in GastroIntestinal Disorders (TARGID), Department of Chronic Diseases, Metabolism, and Ageing, Faculty of Medicine, KU Leuven, 3000 Leuven, Belgium. boushra.dalile@kuleuven.bekristin.verbeke@kuleuven.behttps://www.kuleuven.be/wieiswie/en/person/00115135https://www.kuleuven.be/wieiswie/en/person/00018368
Lukas Van Oudenhove
Affiliation:
Laboratory for Brain-Gut Axis Studies, Translational Research in GastroIntestinal Disorders (TARGID), Department of Chronic Diseases, Metabolism, and Ageing, Faculty of Medicine, KU Leuven, 3000 Leuven, Belgium. lukas.vanoudenhove@kuleuven.behttps://www.kuleuven.be/wieiswie/en/person/00027997
Bram Vervliet
Affiliation:
Laboratory of Biological Psychology, Faculty of Psychology and Educational Sciences, KU Leuven, 3000 Leuven, Belgium. bram.vervliet@kuleuven.behttps://www.kuleuven.be/wieiswie/en/person/00035504
Get access Rights & Permissions [Opens in a new window]

Abstract

Dietary fiber and prebiotics consistently modulate microbiota composition and function and hence may constitute a powerful tool in microbiota-gut-brain axis research. However, this is largely ignored in Hooks et al.’s analysis, which highlights the limitations of probiotics in establishing microbiome-mediated effects on neurobehavioral functioning and neglects discussing the potential of prebiotics in warranting the microbiota's role in such effects.

Type
Open Peer Commentary
Information
Behavioral and Brain Sciences , Volume 42 , 2019 , e69
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

1.

The authors declare no conflict of interest. The financial support for the PhD of Boushra Dalile is supported by an unrestricted grant from Nestec SA.

2.

Authors Kristin Verbeke, Lukas Van Oudenhove, and Bram Vervliet contributed equally to this work as senior authors.

References

Azpiroz, F., Dubray, C., Bernalier-Donadille, A., Cardot, J. M., Accarino, A., Serra, J., Wagner, A., Respondek, F. & Dapoigny, M. (2017) Effects of scFOS on the composition of fecal microbiota and anxiety in patients with irritable bowel syndrome: A randomized, double blind, placebo controlled study. Neurogastroenterology and Motility 29(2):e12911. Available at: https://doi.org/10.1111/nmo.12911.Google Scholar
Bindels, L. B., Delzenne, N. M., Cani, P. D. & Walter, J. (2015) Towards a more comprehensive concept for prebiotics. Nature Reviews Gastroenterology and Hepatology 12:303. Available at: https://doi.org/10.1038/nrgastro.2015.47.Google Scholar
Burokas, A., Arboleya, S., Moloney, R. D., Peterson, V. L., Murphy, K., Clarke, G., Stanton, C., Dinan, T. G. & Cryan, J. F. (2017) Targeting the microbiota-gut-brain axis: Prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biological Psychiatry 82(7):472–87. Available at: https://doi.org/10.1016/j.biopsych.2016.12.031.Google Scholar
Dalile, B., Van Oudenhove, L., Vervliet, B. & Verbeke, K. (2019) The role of short-chain fatty acids in microbiota-gut-brain communication. Nature Reviews Gastroenterology and Hepatology. https://doi.org/10.1038/s41575-019-0157-3.Google Scholar
Davis, L. M. G., Martínez, I., Walter, J., Goin, C. & Hutkins, R. W. (2011) Barcoded pyrosequencing reveals that consumption of galactooligosaccharides results in a highly specific bifidogenic response in humans. PLoS ONE 6(9):e25200. Available at: https://doi.org/10.1371/journal.pone.0025200.Google Scholar
den Besten, G., van Eunen, K., Groen, A. K., Venema, K., Reijngoud, D.-J. & Bakker, B. M. (2013) The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. Journal of Lipid Research 54(9):2325–40. Available at: https://doi.org/10.1194/jlr.R036012.Google Scholar
Everard, A., Lazarevic, V., Derrien, M., Girard, M., Muccioli, G. G., Neyrinck, A. M., Possemiers, S., Van Holle, A., François, P., de Vos, W. M., Delzenne, N. M., Schrenzel, J. & Cani, P. D. (2011) Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60(11):2775–86. Available at: https://doi.org/10.2337/db11-0227.Google Scholar
Everard, A., Lazarevic, V., Gaïa, N., Johansson, M., Ståhlman, M., Backhed, F., Delzenne, N. M., Schrenzel, J., François, P. & Cani, P. D. (2014) Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. ISME Journal 8:2116–30. Available at: https://doi.org/10.1038/ismej.2014.45.Google Scholar
Falony, G., Joossens, M., Vieira-Silva, S., Wang, J., Darzi, Y., Faust, K., Kurilshikov, A., Bonder, M. J., Valles-Colomer, M., Vandeputte, D., Tito, R. Y., Chaffron, S., Rymenans, L., Verspecht, C., De Sutter, L., Lima-Mendez, G., D'Hoe, K., Jonckheere, K., Homola, D., Garcia, R., Tigchelaar, E. F., Eeckhaudt, L., Fu, J., Henckaerts, L., Zhernakova, A., Wijmenga, C. & Raes, J. (2016) Population-level analysis of gut microbiome variation. Science 352(6285):560–64. Available at: https://doi.org/10.1126/science.aad3503.Google Scholar
Farhangi, M. A., Javid, A. Z., Sarmadi, B., Karimi, P. & Dehghan, P. (2017) A randomized controlled trial on the efficacy of resistant dextrin, as functional food, in women with type 2 diabetes: Targeting the hypothalamic-pituitary-adrenal axis and immune system. Clinical Nutrition. Available at: https://doi.org/10.1016/j.clnu.2017.06.005.Google Scholar
Forsatkar, M. N., Nematollahi, M. A., Rafiee, G., Farahmand, H. & Lawrence, C. (2017) Effects of the prebiotic mannan-oligosaccharide on the stress response of feed deprived zebrafish (Danio rerio). Physiology and Behavior 180:70–77. Available at: https://doi.org/10.1016/j.physbeh.2017.08.010.Google Scholar
Gibson, G. R., Hutkins, R., Sanders, M. E., Prescott, S. L., Reimer, R. A., Salminen, S. J., Scott, K., Swanson, K. S., Cani, P. D., Verbeke, K. & Reid, G. (2017) Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nature Reviews Gastroenterology and Hepatology 14(8):491–502. Available at: https://doi.org/10.1038/nrgastro.2017.75.Google Scholar
Gronier, B., Savignac, H. M., Di Miceli, M., Idriss, S. M., Tzortzis, G., Anthony, D. & Burnet, P. W. J. (2018) Increased cortical neuronal responses to NMDA and improved attentional set-shifting performance in rats following prebiotic (B-GOS®) ingestion. European Neuropsychopharmacology 28(1):211–24. Available at: https://doi.org/10.1016/j.euroneuro.2017.11.001.Google Scholar
Holscher, H. D., Caporaso, J. G., Hooda, S., Brulc, J. M., Fahey, G. C. Jr. & Swanson, K. S. (2015) Fiber supplementation influences phylogenetic structure and functional capacity of the human intestinal microbiome: Follow-up of a randomized controlled trial. American Journal of Clinical Nutrition 101(1):55–64. Available at: https://doi.org/10.3945/ajcn.114.092064.Google Scholar
Jones, J. M. (2014) CODEX-aligned dietary fiber definitions help to bridge the ‘fiber gap.’ Nutrition Journal 13(1):34. Available at: https://doi.org/10.1186/1475-2891-13-34.Google Scholar
Kao, A. C., Spitzer, S., Anthony, D. C., Lennox, B. & Burnet, P. W. J. (2018) Prebiotic attenuation of olanzapine-induced weight gain in rats: Analysis of central and peripheral biomarkers and gut microbiota. Translational Psychiatry 8(1):66. Available at: https://doi.org/10.1038/s41398-018-0116-8.Google Scholar
Martínez, I., Kim, J., Duffy, P. R., Schlegel, V. L. & Walter, J. (2010) Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PLoS ONE 5(11):e15046. Available at: https://doi.org/10.1371/journal.pone.0015046.Google Scholar
Mika, A., Day, H. E., Martinez, A., Rumian, N. L., Greenwood, B. N., Chichlowski, M., Berg, B. M. & Fleshner, M. (2017) Early life diets with prebiotics and bioactive milk fractions attenuate the impact of stress on learned helplessness behaviours and alter gene expression within neural circuits important for stress resistance. European Journal of Neuroscience 45(3):342–57. Available at: https://doi.org/10.1111/ejn.13444.Google Scholar
Mika, A., Gaffney, M., Roller, R., Hills, A., Bouchet, C. A., Hulen, K. A., Thompson, R. S., Chichlowski, M., Berg, B. M., Fleshner, M. & Fleshner, M. (2018) Feeding the developing brain: Juvenile rats fed diet rich in prebiotics and bioactive milk fractions exhibit reduced anxiety-related behavior and modified gene expression in emotion circuits. Neuroscience Letters 677:103–109. Available at: https://doi.org/10.1016/j.neulet.2018.01.052.Google Scholar
Savignac, H. M., Corona, G., Mills, H., Chen, L., Spencer, J. P., Tzortzis, G. & Burnet, P. W. (2013) Prebiotic feeding elevates central brain derived neurotrophic factor, N-methyl-d-aspartate receptor subunits and d-serine. Neurochemistry International 63(8):756–64. Available at: https://doi.org/10.1016/j.neuint.2013.10.006.Google Scholar
Savignac, H. M., Couch, Y., Stratford, M., Bannerman, D. M., Tzortzis, G., Anthony, D. C. & Burnet, P. W. J. (2016) Prebiotic administration normalizes lipopolysaccharide (LPS)-induced anxiety and cortical 5-HT2A receptor and IL1-β levels in male mice. Brain, Behavior, and Immunity 52:120–31. Available at: https://doi.org/10.1016/j.bbi.2015.10.007.Google Scholar
Schmidt, K., Cowen, P. J., Harmer, C. J., Tzortzis, G., Errington, S. & Burnet, P. W. (2015) Prebiotic intake reduces the waking cortisol response and alters emotional bias in healthy volunteers. Psychopharmacology 232(10):1793–801. Available at: https://doi.org/10.1007/s00213-014-3810-0.Google Scholar
So, D., Whelan, K., Rossi, M., Morrison, M., Holtmann, G., Kelly, J. T., Shanahan, E. R., Staudacher, H. M. & Campbell, K. L. (2018) Dietary fiber intervention on gut microbiota composition in healthy adults: A systematic review and meta-analysis. American Journal of Clinical Nutrition 107(6):965–83. Available at: https://doi.org/10.1093/ajcn/nqy041.Google Scholar
Tan, J., McKenzie, C., Potamitis, M., Thorburn, A. N., Mackay, C. R. & Macia, L. (2014) The role of short-chain fatty acids in health and disease. Advances in Immunology 121:91–119. Available at: https://doi.org/10.1016/b978-0-12-800100-4.00003-9.Google Scholar
Thompson, R. S., Roller, R., Mika, A., Greenwood, B. N., Knight, R., Chichlowski, M., Berg, B. M. & Fleshner, M. (2016) Dietary prebiotics and bioactive milk fractions improve NREM sleep, enhance REM sleep rebound and attenuate the stress-induced decrease in diurnal temperature and gut microbial alpha diversity. Frontiers in Behavioral Neuroscience 10:240. Available at: https://doi.org/10.3389/fnbeh.2016.00240.Google Scholar
Vandeputte, D., Falony, G., Vieira-Silva, S., Wang, J., Sailer, M., Theis, S., Verbeke, K. & Raes, J. (2017a) Prebiotic inulin-type fructans induce specific changes in the human gut microbiota. Gut 66(11):1968–74. Available at: https://doi.org/10.1136/gutjnl-2016-313271.Google Scholar
Walker, A. W., Ince, J., Duncan, S. H., Webster, L. M., Holtrop, G., Ze, X., Brown, D., Stares, M. D., Scott, P., Bergerat, A., Louis, P., McIntosh, F., Johnstone, A. M., Lobley, G. E., Parkhill, J. & Flint, H. J. (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME Journal 5:220–30. Available at: https://doi.org/10.1038/ismej.2010.118.Google Scholar
Williams, S., Chen, L., Savignac, H. M., Tzortzis, G., Anthony, D. C. & Burnet, P. W. (2016) Neonatal prebiotic (BGOS) supplementation increases the levels of synaptophysin, GluN2A-subunits and BDNF proteins in the adult rat hippocampus. Synapse 70(3):121–24. Available at: https://doi.org/10.1002/syn.21880.Google Scholar
Ze, X., Le Mougen, F., Duncan, S. H., Louis, P. & Flint, H. J. (2013) Some are more equal than others: The role of “keystone” species in the degradation of recalcitrant substrates. Gut Microbes 4(3):236–40. Available at: https://doi.org/10.4161/gmic.23998.Google Scholar