Probiotics and prebiotics in intestinal health and disease: from biology to the clinic

Probiotics and prebiotics are microbiota-management tools for improving host health. They target gastrointestinal effects via the gut, although direct application to other sites such as the oral cavity, vaginal tract and skin is being explored. Here, we describe gut-derived effects in humans. In the past decade, research on the gut microbiome has rapidly accumulated and has been accompanied by increased interest in probiotics and prebiotics as a means to modulate the gut microbiota. Given the importance of these approaches for public health, it is timely to reiterate factual and supporting information on their clinical application and use. In this Review, we discuss scientific evidence on probiotics and prebiotics, including mechanistic insights into health effects. Strains of Lactobacillus, Bifidobacterium and Saccharomyces have a long history of safe and effective use as probiotics, but Roseburia spp., Akkermansia spp., Propionibacterium spp. and Faecalibacterium spp. show promise for the future. For prebiotics, glucans and fructans are well proven, and evidence is building on the prebiotic effects of other substances (for example, oligomers of mannose, glucose, xylose, pectin, starches, human milk and polyphenols).

Key points

This is a preview of subscription content, access via your institution

Access options

Access Nature and 54 other Nature Portfolio journals

Get Nature+, our best-value online-access subscription

cancel any time

Subscribe to this journal

Receive 12 print issues and online access

206,07 € per year

only 17,17 € per issue

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

The International Scientific Association of Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of postbiotics

Article Open access 04 May 2021

The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics

Article Open access 21 August 2020

The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on fermented foods

Article Open access 04 January 2021

Change history

References

  1. Food and Agriculture Organization of the United Nations & World Health Organization. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. FAOhttp://www.fao.org/3/a-a0512e.pdf (2001).
  2. Hill, C. et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol.11, 506–514 (2014). This Consensus Statement examines the definition, evolution, uses, types and health attributes of probiotics. PubMedGoogle Scholar
  3. Rook, G., Backhed, F., Levin, B. R., McFall-Ngai, M. J. & McLean, A. R. Evolution, human-microbe interactions, and life history plasticity. Lancet390, 521–530 (2017). This article discusses how some microorganisms have co-evolved with humans and have crucial roles in host physiology and metabolism, whereas others are intrusive. PubMedGoogle Scholar
  4. Reid, G. et al. Expanding the reach of probiotics through social enterprises. Benef. Microbes9, 707–715 (2018). CASPubMedGoogle Scholar
  5. Gibson, G. R. & Roberfroid, M. B. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr.125, 1401–1412 (1995). CASPubMedGoogle Scholar
  6. Gibson, G. R. et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol.14, 491–502 (2017). This Consensus Statement examines the definition, evolution, uses, types and health attributes of prebiotics. PubMedGoogle Scholar
  7. Collins, S. L. et al. Promising prebiotic candidate established by evaluation of lactitol, lactulose, raffinose, and oligofructose for maintenance of a Lactobacillus-dominated vaginal microbiota. Appl. Environ. Microbiol.84, e02200-17 (2018). PubMedPubMed CentralGoogle Scholar
  8. Rodriguez, J. M. et al. The composition of the gut microbiota throughout life, with an emphasis on early life. Microb. Ecol. Health Dis.26, 26050 (2015). PubMedGoogle Scholar
  9. Donaldson, G. P., Lee, S. M. & Mazmanian, S. K. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol.14, 20–32 (2016). CASPubMedGoogle Scholar
  10. Rowland, I. et al. Gut microbiota functions: metabolism of nutrients and other food components. Eur. J. Nutr.57, 1–24 (2018). CASPubMedGoogle Scholar
  11. Thursby, E. & Juge, N. Introduction to the human gut microbiota. Biochem. J.474, 1823–1836 (2017). This article provides current understanding of the development and composition of the human gut microbiota, and its effects on gut integrity and host health. CASPubMedGoogle Scholar
  12. Fava, F. et al. The type and quantity of dietary fat and carbohydrate alter faecal microbiome and short-chain fatty acid excretion in a metabolic syndrome ‘at-risk’ population. Int. J. Obes. (Lond.)37, 216–223 (2013). CASGoogle Scholar
  13. Dicks, L. M. T., Geldenhuys, J., Mikkelsen, L. S., Brandsborg, E. & Marcotte, H. Our gut microbiota: a long walk to homeostasis. Benef. Microbes9, 3–20 (2018). CASPubMedGoogle Scholar
  14. Dethlefsen, L. & Relman, D. A. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl Acad. Sci. U. S. A.108 (Suppl. 1), 4554–4561 (2011). CASPubMedGoogle Scholar
  15. Gagliardi, A. et al. Rebuilding the gut microbiota ecosystem. Int. J. Environ. Res. Public Health15, E1679 (2018). PubMedGoogle Scholar
  16. Hatton, G. B., Madla, C. M., Rabbie, S. C. & Basit, A. W. All disease begins in the gut: influence of gastrointestinal disorders and surgery on oral drug performance. Int. J. Pharm.548, 408–422 (2018). CASPubMedGoogle Scholar
  17. John, G. K. et al. Dietary alteration of the gut microbiome and its impact on weight and fat mass: a systematic review and meta-analysis. Genes (Basel)9, (E167 (2018). Google Scholar
  18. Yoshida, N., Yamashita, T. & Hirata, K. I. Gut microbiome and cardiovascular diseases. Diseases6, E56 (2018). PubMedGoogle Scholar
  19. Hansen, L. B. S. et al. A low-gluten diet induces changes in the intestinal microbiome of healthy Danish adults. Nat. Commun.9, 4630 (2018). PubMedPubMed CentralGoogle Scholar
  20. Parker, R. B. Probiotics, the other half of the antibiotic story. Anim. Nutr. Health29, 4–8 (1974). Google Scholar
  21. Havenaar, R. & Huis In’t Veld, J. M. J. in Lactic Acid Bacteria in Health and Disease Vol. 1 (ed. Wood, B. J. B.) 151–170 (Elsevier Applied Science Publishers, 1992).
  22. Ng, S. C. et al. Immunosuppressive effects via human intestinal dendritic cells of probiotic bacteria and steroids in the treatment of acute ulcerative colitis. Inflamm. Bowel Dis.16, 1286–1298 (2010). PubMedGoogle Scholar
  23. Mujagic, Z. et al. The effects of Lactobacillus plantarum on small intestinal barrier function and mucosal gene transcription; a randomized double-blind placebo controlled trial. Sci. Rep.7, 40128 (2017). CASPubMedPubMed CentralGoogle Scholar
  24. Del Piano, M. et al. The use of probiotics in healthy volunteers with evacuation disorders and hard stools: a double-blind, randomized, placebo-controlled study. J. Clin. Gastroenterol.44 (Suppl. 1), S30–S34 (2010). PubMedGoogle Scholar
  25. Reid, G., Gadir, A. A. & Dhir, R. Probiotics: reiterating what they are and what they are not. Front. Microbiol.10, 424 (2019). PubMedPubMed CentralGoogle Scholar
  26. Cabre, E. & Gassull, M. A. Probiotics for preventing relapse or recurrence in Crohn’s disease involving the ileum: are there reasons for failure? J. Crohns Colitis1, 47–52 (2007). PubMedGoogle Scholar
  27. Kelly, J. R. 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.61, 50–59 (2017). CASPubMedGoogle Scholar
  28. Panigrahi, P. et al. A randomized synbiotic trial to prevent sepsis among infants in rural India. Nature548, 407–412 (2017). CASPubMedGoogle Scholar
  29. Costeloe, K. et al. Bifidobacterium breve BBG-001 in very preterm infants: a randomised controlled phase 3 trial. Lancet387, 649–660 (2016). PubMedGoogle Scholar
  30. Sorbara, M. T. & Pamer, E. G. Interbacterial mechanisms of colonization resistance and the strategies pathogens use to overcome them. Mucosal Immunol.34, 1608 (2018). Google Scholar
  31. Chiu, L. et al. Protective microbiota: from localized to long-reaching co-immunity. Front. Immunol.8, 1678 (2017). PubMedPubMed CentralGoogle Scholar
  32. Maldonado-Gomez, M. X. et al. Stable engraftment of Bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome. Cell Host Microbe20, 515–526 (2016). CASPubMedGoogle Scholar
  33. Murphy, R. et al. Eczema-protective probiotic alters infant gut microbiome functional capacity but not composition: sub-sample analysis from a RCT. Benef. Microbes10, 5–17 (2019). CASPubMedGoogle Scholar
  34. Korpela, K. et al. Probiotic supplementation restores normal microbiota composition and function in antibiotic-treated and in caesarean-born infants. Microbiome6, 182 (2018). PubMedPubMed CentralGoogle Scholar
  35. Clarke, G. et al. Gut reactions: breaking down xenobiotic-microbiome interactions. Pharmacol. Rev.71, 198–224 (2019). PubMedGoogle Scholar
  36. Klaenhammer, T. R., Kleerebezem, M., Kopp, M. V. & Rescigno, M. The impact of probiotics and prebiotics on the immune system. Nat. Rev. Immunol.12, 728–734 (2012). Here, four experts discuss probiotics, prebiotics and immunity, then provide their thoughts on the future application as a disease therapy. CASPubMedGoogle Scholar
  37. Przemska-Kosicka, A. et al. Effect of a synbiotic on the response to seasonal influenza vaccination is strongly influenced by degree of immunosenescence. Immun. Ageing13, 6 (2016). PubMedPubMed CentralGoogle Scholar
  38. Vitetta, L., Saltzman, E. T., Thomsen, M., Nikov, T. & Hall, S. Adjuvant probiotics and the intestinal microbiome: enhancing vaccines and immunotherapy outcomes. Vaccines (Basel) 5, (E50 (2017). Google Scholar
  39. Childs, C. E. et al. Xylo-oligosaccharides alone or in synbiotic combination with Bifidobacterium animalis subsp. lactis induce bifidogenesis and modulate markers of immune function in healthy adults: a double-blind, placebo-controlled, randomised, factorial cross-over study. Br. J. Nutr.111, 1945–1956 (2014). CASPubMedGoogle Scholar
  40. Flint, H. J., Duncan, S. H., Scott, K. P. & Louis, P. Links between diet, gut microbiota composition and gut metabolism. Proc. Nutr. Soc.74, 13–22 (2015). CASPubMedGoogle Scholar
  41. Aoudia, N. et al. Biofilms of Lactobacillus plantarum and Lactobacillus fermentum: effect on stress responses, antagonistic effects on pathogen growth and immunomodulatory properties. Food Microbiol.53, 51–59 (2016). CASPubMedGoogle Scholar
  42. Rios-Covian, D. et al. Intestinal short chain fatty acids and their link with diet and human health. Front. Microbiol.7, 185 (2016). PubMedPubMed CentralGoogle Scholar
  43. Canfora, E. E., Jocken, J. W. & Blaak, E. E. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat. Rev. Endocrinol.11, 577–591 (2015). CASPubMedGoogle Scholar
  44. Sanna, S. et al. Causal relationships among the gut microbiome, short-chain fatty acids and metabolic diseases. Nat. Genet.51, 600–605 (2019). CASPubMedPubMed CentralGoogle Scholar
  45. Stefan, N., Fritsche, A., Schick, F. & Haring, H. U. Phenotypes of prediabetes and stratification of cardiometabolic risk. Lancet Diabetes Endocrinol.4, 789–798 (2016). PubMedGoogle Scholar
  46. van Baarlen, P., Wells, J. M. & Kleerebezem, M. Regulation of intestinal homeostasis and immunity with probiotic lactobacilli. Trends Immunol.34, 208–215 (2013). PubMedGoogle Scholar
  47. Hegarty, J. W., Guinane, C. M., Ross, R. P., Hill, C. & Cotter, P. D. Bacteriocin production: a relatively unharnessed probiotic trait? F1000Res.5, 2587 (2016). PubMedPubMed CentralGoogle Scholar
  48. Mokoena, M. P. Lactic acid bacteria and their bacteriocins: classification, biosynthesis and applications against uropathogens: a mini-review. Molecules22, E1255 (2017). PubMedGoogle Scholar
  49. Bali, V., Panesar, P. S., Bera, M. B. & Kennedy, J. F. Bacteriocins: recent trends and potential applications. Crit. Rev. Food Sci. Nutr.56, 817–834 (2016). CASPubMedGoogle Scholar
  50. Riviere, A., Selak, M., Lantin, D., Leroy, F. & De Vuyst, L. Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front. Microbiol.7, 979 (2016). PubMedPubMed CentralGoogle Scholar
  51. Abdulkadir, B. et al. Routine use of probiotics in preterm infants: longitudinal impact on the microbiome and metabolome. Neonatology109, (239–247 (2016). Google Scholar
  52. Fang, H. R., Zhang, G. Q., Cheng, J. Y. & Li, Z. Y. Efficacy of Lactobacillus-supplemented triple therapy for Helicobacter pylori infection in children: a meta-analysis of randomized controlled trials. Eur. J. Pediatr.178, 7–16 (2019). CASPubMedGoogle Scholar
  53. Sanders, M. E., Benson, A., Lebeer, S., Merenstein, D. J. & Klaenhammer, T. R. Shared mechanisms among probiotic taxa: implications for general probiotic claims. Curr. Opin. Biotechnol.49, 207–216 (2018). CASPubMedGoogle Scholar
  54. Petrova, M. I. et al. Comparative genomic and phenotypic analysis of the vaginal probiotic Lactobacillus rhamnosus GR-1. Front. Microbiol.9, 1278 (2018). PubMedPubMed CentralGoogle Scholar
  55. La Fata, G., Weber, P. & Mohajeri, M. H. Probiotics and the gut immune system: indirect regulation. Probiot. Antimicrob. Proteins10, 11–21 (2018). Google Scholar
  56. Han, X. et al. Lactobacillus rhamnosus GG prevents epithelial barrier dysfunction induced by interferon-gamma and fecal supernatants from irritable bowel syndrome patients in human intestinal enteroids and colonoids. Gut Microbes10, 59–76 (2019). CASPubMedGoogle Scholar
  57. Mack, D. R., Michail, S., Wei, S., McDougall, L. & Hollingsworth, M. A. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am. J. Physiol.276, G941–G950 (1999). CASPubMedGoogle Scholar
  58. Yan, F. et al. A Lactobacillus rhamnosus GG-derived soluble protein, p40, stimulates ligand release from intestinal epithelial cells to transactivate epidermal growth factor receptor. J. Biol. Chem.288, 30742–30751 (2013). CASPubMedPubMed CentralGoogle Scholar
  59. Stadlbauer, V. et al. Lactobacillus casei Shirota supplementation does not restore gut microbiota composition and gut barrier in metabolic syndrome: a randomized pilot study. PLOS ONE10, e0141399 (2015). PubMedPubMed CentralGoogle Scholar
  60. Kim, N., Yun, M., Oh, Y. J. & Choi, H. J. Mind-altering with the gut: modulation of the gut-brain axis with probiotics. J. Microbiol.56, 172–182 (2018). CASPubMedGoogle Scholar
  61. Janik, R. et al. Magnetic resonance spectroscopy reveals oral Lactobacillus promotion of increases in brain GABA, N-acetyl aspartate and glutamate. Neuroimage125, 988–995 (2016). CASPubMedGoogle Scholar
  62. Reid, G. Disentangling what we know about microbes and mental health. Front. Endocrinol.10, 81 (2019). Google Scholar
  63. Liang, S. et al. Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress. Neuroscience310, 561–577 (2015). CASPubMedGoogle Scholar
  64. Kotz, C. M., Furne, J. K., Savaiano, D. A. & Levitt, M. D. Factors affecting the ability of a high beta-galactosidase yogurt to enhance lactose absorption. J. Dairy Sci.77, 3538–3544 (1994). CASPubMedGoogle Scholar
  65. Costabile, A. et al. An in vivo assessment of the cholesterol-lowering efficacy of Lactobacillus plantarum ECGC 13110402 in normal to mildly hypercholesterolaemic adults. PLOS ONE12, e0187964 (2017). PubMedPubMed CentralGoogle Scholar
  66. European Food Safety Authority Panel on Dietetic Products. Scientific opinion on the substantiation of health claims related to live yoghurt cultures and improved lactose digestion (ID 1143, 2976) pursuant to article 13(1) of regulation (EC) No 1924/2006. EFSA J.8, 1763 (2010). Google Scholar
  67. Li, D., Wang, P., Wang, P., Hu, X. & Chen, F. The gut microbiota: a treasure for human health. Biotechnol. Adv.34, 1210–1224 (2016). PubMedGoogle Scholar
  68. Kasubuchi, M., Hasegawa, S., Hiramatsu, T., Ichimura, A. & Kimura, I. Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients7, 2839–2849 (2015). CASPubMedPubMed CentralGoogle Scholar
  69. Verbeke, K. A. et al. Towards microbial fermentation metabolites as markers for health benefits of prebiotics. Nutr. Res. Rev.28, 42–66 (2015). CASPubMedPubMed CentralGoogle Scholar
  70. David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature505, 559–563 (2014). CASPubMedGoogle Scholar
  71. Fogliano, V. et al. In vitro bioaccessibility and gut biotransformation of polyphenols present in the water-insoluble cocoa fraction. Mol. Nutr. Food Res.55 (Suppl. 1), S44–S55 (2011). CASPubMedGoogle Scholar
  72. Falony, G. et al. In vitro kinetic analysis of fermentation of prebiotic inulin-type fructans by Bifidobacterium species reveals four different phenotypes. Appl. Environ. Microbiol.75, 454–461 (2009). CASPubMedGoogle Scholar
  73. Riviere, A., Selak, M., Geirnaert, A., Van den Abbeele, P. & De Vuyst, L. Complementary mechanisms for degradation of inulin-type fructans and arabinoxylan oligosaccharides among bifidobacterial strains suggest bacterial cooperation. Appl. Environ. Microbiol.84, e02893-17 (2018). CASPubMedPubMed CentralGoogle Scholar
  74. Flint, H. J., Scott, K. P., Duncan, S. H., Louis, P. & Forano, E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes3, 289–306 (2012). PubMedPubMed CentralGoogle Scholar
  75. Hamaker, B. R. & Tuncil, Y. E. A perspective on the complexity of dietary fiber structures and their potential effect on the gut microbiota. J. Mol. Biol.426, 3838–3850 (2014). CASPubMedGoogle Scholar
  76. Ze, X., Le Mougen, F., Duncan, S. H., Louis, P. & Flint, H. J. Some are more equal than others: the role of “keystone” species in the degradation of recalcitrant substrates. Gut Microbes4, 236–240 (2013). PubMedPubMed CentralGoogle Scholar
  77. 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.6, 1535–1543 (2012). CASPubMedPubMed CentralGoogle Scholar
  78. Hosseini, E., Grootaert, C., Verstraete, W. & Van de Wiele, T. Propionate as a health-promoting microbial metabolite in the human gut. Nutr. Rev.69, 245–258 (2011). PubMedGoogle Scholar
  79. Louis, P. & Flint, H. J. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol. Lett.294, 1–8 (2009). CASPubMedGoogle Scholar
  80. Falony, G., Calmeyn, T., Leroy, F. & De Vuyst, L. Coculture fermentations of Bifidobacterium species and Bacteroides thetaiotaomicron reveal a mechanistic insight into the prebiotic effect of inulin-type fructans. Appl. Environ. Microbiol.75, 2312–2319 (2009). CASPubMedPubMed CentralGoogle Scholar
  81. Scott, K. P., Martin, J. C., Duncan, S. H. & Flint, H. J. Prebiotic stimulation of human colonic butyrate-producing bacteria and bifidobacteria, in vitro. FEMS Microbiol. Ecol.87, 30–40 (2014). CASPubMedGoogle Scholar
  82. Flint, H. J., Duncan, S. H. & Louis, P. The impact of nutrition on intestinal bacterial communities. Curr. Opin. Microbiol.38, 59–65 (2017). CASPubMedGoogle Scholar
  83. Chen, T. et al. Fiber-utilizing capacity varies in Prevotella- versus Bacteroides-dominated gut microbiota. Sci. Rep.7, 2594 (2017). PubMedPubMed CentralGoogle Scholar
  84. Wu, Q. et al. Fermentation properties of isomaltooligosaccharides are affected by human fecal enterotypes. Anaerobe48, 206–214 (2017). CASPubMedGoogle Scholar
  85. Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature464, 59–65 (2010). CASPubMedPubMed CentralGoogle Scholar
  86. Frank, D. N. et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl Acad. Sci. U. S. A.104, 13780–13785 (2007). CASPubMedPubMed CentralGoogle Scholar
  87. Larsen, N. et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLOS ONE5, e9085 (2010). PubMedPubMed CentralGoogle Scholar
  88. Qin, J. et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature490, 55–60 (2012). This study provides a definition and description of the minimal gut metagenome and bacterial genome in terms of functions. CASPubMedGoogle Scholar
  89. Karlsson, F. H. et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature498, 99–103 (2013). CASPubMedGoogle Scholar
  90. Carroll, I. M., Chang, Y. H., Park, J., Sartor, R. B. & Ringel, Y. Luminal and mucosal-associated intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Gut Pathog.2, 19 (2010). PubMedPubMed CentralGoogle Scholar
  91. Krogius-Kurikka, L. et al. Microbial community analysis reveals high level phylogenetic alterations in the overall gastrointestinal microbiota of diarrhoea-predominant irritable bowel syndrome sufferers. BMC Gastroenterol.9, 95 (2009). PubMedPubMed CentralGoogle Scholar
  92. Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature444, 1027–1031 (2006). PubMedGoogle Scholar
  93. Zhang, H. et al. Human gut microbiota in obesity and after gastric bypass. Proc. Natl Acad. Sci. U. S. A.106, 2365–2370 (2009). CASPubMedPubMed CentralGoogle Scholar
  94. Ha, C. W., Lam, Y. Y. & Holmes, A. J. Mechanistic links between gut microbial community dynamics, microbial functions and metabolic health. World J. Gastroenterol.20, 16498–16517 (2014). CASPubMedPubMed CentralGoogle Scholar
  95. Moya, A. & Ferrer, M. Functional redundancy-induced stability of gut microbiota subjected to disturbance. Trends Microbiol.24, 402–413 (2016). CASPubMedGoogle Scholar
  96. Fooks, L. J. & Gibson, G. R. In vitro investigations of the effect of probiotics and prebiotics on selected human intestinal pathogens. FEMS Microbiol. Ecol.39, 67–75 (2002). CASPubMedGoogle Scholar
  97. Tzortzis, G., Baillon, M. L., Gibson, G. R. & Rastall, R. A. Modulation of anti-pathogenic activity in canine-derived Lactobacillus species by carbohydrate growth substrate. J. Appl. Microbiol.96, 552–559 (2004). CASPubMedGoogle Scholar
  98. Vulevic, J., Drakoularakou, A., Yaqoob, P., Tzortzis, G. & Gibson, G. R. Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. Am. J. Clin. Nutr.88, 1438–1446 (2008). CASPubMedGoogle Scholar
  99. Vulevic, J. et al. Influence of galacto-oligosaccharide mixture (B-GOS) on gut microbiota, immune parameters and metabonomics in elderly persons. Br. J. Nutr.114, 586–595 (2015). CASPubMedGoogle Scholar
  100. Moro, G. et al. A mixture of prebiotic oligosaccharides reduces the incidence of atopic dermatitis during the first six months of age. Arch. Dis. Child.91, 814–819 (2006). CASPubMedPubMed CentralGoogle Scholar
  101. Ivakhnenko, O. S. & Nyankovskyy, S. L. Effect of the specific infant formula mixture of oligosaccharides on local immunity and development of allergic and infectious disease in young children: randomized study. Pediatr. Pol.88, 398–404 (2013). Google Scholar
  102. Arslanoglu, S. et al. Early neutral prebiotic oligosaccharide supplementation reduces the incidence of some allergic manifestations in the first 5 years of life. J. Biol. Regul. Homeost. Agents26, 49–59 (2012). CASPubMedGoogle Scholar
  103. Diaz de Barboza, G. & Guizzardi, S. & Tolosa de Talamoni, N. Molecular aspects of intestinal calcium absorption. World J. Gastroenterol.21, 7142–7154 (2015). CASPubMedPubMed CentralGoogle Scholar
  104. Goss, S. L., Lemons, K. A., Kerstetter, J. E. & Bogner, R. H. Determination of calcium salt solubility with changes in pH and P(CO(2)), simulating varying gastrointestinal environments. J. Pharm. Pharmacol.59, 1485–1492 (2007). PubMedGoogle Scholar
  105. Abrams, S. A., Griffin, I. J., Hawthorne, K. M. & Ellis, K. J. Effect of prebiotic supplementation and calcium intake on body mass index. J. Pediatr.151, 293–298 (2007). CASPubMedGoogle Scholar
  106. Abrams, S. A., Griffin, I. J. & Hawthorne, K. M. Young adolescents who respond to an inulin-type fructan substantially increase total absorbed calcium and daily calcium accretion to the skeleton. J. Nutr.137, 2524S–2526S (2007). CASPubMedGoogle Scholar
  107. Whisner, C. M. et al. Galacto-oligosaccharides increase calcium absorption and gut bifidobacteria in young girls: a double-blind cross-over trial. Br. J. Nutr.110, 1292–1303 (2013). CASPubMedGoogle Scholar
  108. Chonan, O., Matsumoto, K. & Watanuki, M. Effect of galactooligosaccharides on calcium absorption and preventing bone loss in ovariectomized rats. Biosci. Biotechnol. Biochem.59, 236–239 (1995). CASPubMedGoogle Scholar
  109. Kanauchi, O., Andoh, A. & Mitsuyama, K. Effects of the modulation of microbiota on the gastrointestinal immune system and bowel function. J. Agric. Food Chem.61, 9977–9983 (2013). CASPubMedGoogle Scholar
  110. Hurst, N. R., Kendig, D. M., Murthy, K. S. & Grider, J. R. The short chain fatty acids, butyrate and propionate, have differential effects on the motility of the guinea pig colon. Neurogastroenterol. Motil.26, 1586–1596 (2014). CASPubMedPubMed CentralGoogle Scholar
  111. Lamsal, B. P. Production, health aspects and potential food uses of dairy prebiotic galactooligosaccharides. J. Sci. Food Agric.92, 2020–2028 (2012). CASPubMedGoogle Scholar
  112. Hager, A.-S. et al. Influence of the soluble fibres inulin and oat β-glucan on quality of dough and bread. Eur. Food Res. Technol.232, 405–413 (2011). CASGoogle Scholar
  113. Collado Yurrita, L., San Mauro Martin, I., Ciudad-Cabanas, M. J., Calle-Puron, M. E. & Hernandez Cabria, M. Effectiveness of inulin intake on indicators of chronic constipation; a meta-analysis of controlled randomized clinical trials. Nutr. Hosp.30, 244–252 (2014). PubMedGoogle Scholar
  114. Buddington, R. K., Kapadia, C., Neumer, F. & Theis, S. Oligofructose provides laxation for irregularity associated with low fiber intake. Nutrients9, E1372 (2017). PubMedGoogle Scholar
  115. Krumbeck, J. A. et al. Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics. Microbiome6, 121 (2018). PubMedPubMed CentralGoogle Scholar
  116. Cani, P. D. et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes56, 1761–1772 (2007). CASPubMedGoogle Scholar
  117. Cani, P. D. et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes57, 1470–1481 (2008). CASPubMedGoogle Scholar
  118. Cani, P. D. et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut58, 1091–1103 (2009). CASPubMedGoogle Scholar
  119. Kellow, N. J., Coughlan, M. T. & Reid, C. M. Metabolic benefits of dietary prebiotics in human subjects: a systematic review of randomised controlled trials. Br. J. Nutr.111, 1147–1161 (2014). CASPubMedGoogle Scholar
  120. Beserra, B. T. et al. A systematic review and meta-analysis of the prebiotics and synbiotics effects on glycaemia, insulin concentrations and lipid parameters in adult patients with overweight or obesity. Clin. Nutr.34, 845–858 (2015). CASPubMedGoogle Scholar
  121. Liu, F., Prabhakar, M., Ju, J., Long, H. & Zhou, H. W. Effect of inulin-type fructans on blood lipid profile and glucose level: a systematic review and meta-analysis of randomized controlled trials. Eur. J. Clin. Nutr.71, 9–20 (2017). CASPubMedGoogle Scholar
  122. Guo, Z. et al. Effects of inulin on the plasma lipid profile of normolipidemic and hyperlipidemic subjects: a meta-analysis of randomized controlled trials. Clin. Lipidol7, 215–222 (2012). CASGoogle Scholar
  123. Vulevic, J., Juric, A., Tzortzis, G. & Gibson, G. R. A mixture of trans-galactooligosaccharides reduces markers of metabolic syndrome and modulates the fecal microbiota and immune function of overweight adults. J. Nutr.143, 324–331 (2013). CASPubMedGoogle Scholar
  124. Dewulf, E. M. et al. Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut62, 1112–1121 (2013). CASPubMedGoogle Scholar
  125. Bhatia, S. et al. Galacto-oligosaccharides may directly enhance intestinal barrier function through the modulation of goblet cells. Mol. Nutr. Food Res.59, 566–573 (2015). CASPubMedGoogle Scholar
  126. Akbari, P. et al. Characterizing microbiota-independent effects of oligosaccharides on intestinal epithelial cells: insight into the role of structure and size: structure-activity relationships of non-digestible oligosaccharides. Eur. J. Nutr.56, 1919–1930 (2017). CASPubMedGoogle Scholar
  127. Neyrinck, A. M. et al. Intestinal sucrase as a novel target contributing to the regulation of glycemia by prebiotics. PLOS ONE11, e0160488 (2016). PubMedPubMed CentralGoogle Scholar
  128. Stoddart, L. A., Smith, N. J. & Milligan, G. International Union of Pharmacology. LXXI. Free fatty acid receptors FFA1, -2, and -3: pharmacology and pathophysiological functions. Pharmacol. Rev.60, 405–417 (2008). CASPubMedGoogle Scholar
  129. Bolognini, D. et al. Chemogenetics defines receptor-mediated functions of short chain free fatty acids. Nat. Chem. Biol.15, 489–498 (2019). CASPubMedGoogle Scholar
  130. Chambers, E. S., Morrison, D. J. & Frost, G. Control of appetite and energy intake by SCFA: what are the potential underlying mechanisms? Proc. Nutr. Soc.74, 328–336 (2015). CASPubMedGoogle Scholar
  131. Mithieux, G. Metabolic effects of portal vein sensing. Diabetes Obes. Metab.16 (Suppl. 1), 56–60 (2014). CASPubMedGoogle Scholar
  132. Frost, G. et al. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat. Commun.5, 3611 (2014). CASPubMedGoogle Scholar
  133. Jackson, S. A. et al. Improving end-user trust in the quality of commercial probiotic products. Front. Microbiol.10, 739 (2019). PubMedPubMed CentralGoogle Scholar
  134. AlFaleh, K. & Anabrees, J. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst. Rev.4, CD005496 (2014). Google Scholar
  135. Vanderhoof, J. A. et al. Lactobacillus GG in the prevention of antibiotic-associated diarrhea in children. J. Pediatr.135, 564–568 (1999). CASPubMedGoogle Scholar
  136. Szajewska, H., Albrecht, P. & Topczewska-Cabanek, A. Randomized, double-blind, placebo-controlled trial: effect of Lactobacillus GG supplementation on Helicobacter pylori eradication rates and side effects during treatment in children. J. Pediatr. Gastroenterol. Nutr.48, 431–436 (2009). CASPubMedGoogle Scholar
  137. Goldenberg, J. Z. et al. Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database Syst. Rev.4, CD004827 (2015). Google Scholar
  138. Eskesen, D. et al. Effect of the probiotic strain Bifidobacterium animalis subsp. lactis, BB-12®, on defecation frequency in healthy subjects with low defecation frequency and abdominal discomfort: a randomised, double-blind, placebo-controlled, parallel-group trial. Br. J. Nutr.114, 1638–1646 (2015). CASPubMedPubMed CentralGoogle Scholar
  139. Yang, Y. X. et al. Effect of a fermented milk containing Bifidobacterium lactis DN-173010 on Chinese constipated women. World J. Gastroenterol.14, 6237–6243 (2008). PubMedPubMed CentralGoogle Scholar
  140. Sung, V. et al. Lactobacillus reuteri to treat infant colic: a meta-analysis. Pediatrics141, e20171811 (2018). PubMedGoogle Scholar
  141. Mardini, H. E. & Grigorian, A. Y. Probiotic mix VSL#3 is effective adjunctive therapy for mild to moderately active ulcerative colitis: a meta-analysis. Inflamm. Bowel Dis.20, 1562–1567 (2014). PubMedGoogle Scholar
  142. Whorwell, P. J. et al. Efficacy of an encapsulated probiotic Bifidobacterium infantis 35624 in women with irritable bowel syndrome. Am. J. Gastroenterol.101, 1581–1590 (2006). PubMedGoogle Scholar
  143. Szajewska, H. et al. Systematic review with meta-analysis: Lactobacillus rhamnosus GG for treating acute gastroenteritis in children - a 2019 update. Aliment. Pharmacol. Ther.49, 1376–1384 (2019). PubMedGoogle Scholar
  144. Goldenberg, J. Z. et al. Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children. Cochrane Database Syst. Rev.12, CD006095 (2017). PubMedGoogle Scholar
  145. King, S. et al. Does probiotic consumption reduce antibiotic utilization for common acute infections? A systematic review and meta-analysis. Eur. J. Public Health29, 494–499 (2019). PubMedGoogle Scholar
  146. Cruchet, S. et al. The use of probiotics in pediatric gastroenterology: a review of the literature and recommendations by Latin-American experts. Paediatr. Drugs17, 199–216 (2015). PubMedPubMed CentralGoogle Scholar
  147. Cameron, D. et al. Probiotics for gastrointestinal disorders: proposed recommendations for children of the Asia-Pacific region. World J. Gastroenterol.23, 7952–7964 (2017). PubMedPubMed CentralGoogle Scholar
  148. Hao, Q., Dong, B. R. & Wu, T. Probiotics for preventing acute upper respiratory tract infections. Cochrane Database Syst. Rev.9, CD006895 (2015). Google Scholar
  149. King, S., Glanville, J., Sanders, M. E., Fitzgerald, A. & Varley, D. Effectiveness of probiotics on the duration of illness in healthy children and adults who develop common acute respiratory infectious conditions: a systematic review and meta-analysis. Br. J. Nutr.112, 41–54 (2014). CASPubMedPubMed CentralGoogle Scholar
  150. Yang, L. et al. Inflammation and intestinal metaplasia of the distal esophagus are associated with alterations in the microbiome. Gastroenterology137, 588–597 (2009). PubMedGoogle Scholar
  151. Szymanski, H. & Szajewska, H. Lack of efficacy of Lactobacillus reuteri DSM 17938 for the treatment of acute gastroenteritis: a randomized controlled trial. Pediatr. Infect. Dis. J.https://doi.org/10.1097/INF.0000000000002355 (2019). ArticlePubMedGoogle Scholar
  152. van den Akker, C. H. P. et al. Probiotics for preterm infants: a strain-specific systematic review and network meta-analysis. J. Pediatr. Gastroenterol. Nutr.67, 103–122 (2018). PubMedGoogle Scholar
  153. Arslanoglu, S., Moro, G. E. & Boehm, G. Early supplementation of prebiotic oligosaccharides protects formula-fed infants against infections during the first 6 months of life. J. Nutr.137, 2420–2424 (2007). CASPubMedGoogle Scholar
  154. Arslanoglu, S. et al. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life. J. Nutr.138, 1091–1095 (2008). CASPubMedGoogle Scholar
  155. Boehm, G. et al. Prebiotics in infant formulas. J. Clin. Gastroenterol.38, S76–S79 (2004). CASPubMedGoogle Scholar
  156. Shahramian, I. et al. The effects of prebiotic supplementation on weight gain, diarrhoea, constipation, fever and respiratory tract infections in the first year of life. J. Paediatr. Child Health54, 875–880 (2018). PubMedGoogle Scholar
  157. Drakoularakou, A., Tzortzis, G., Rastall, R. A. & Gibson, G. R. A double-blind, placebo-controlled, randomized human study assessing the capacity of a novel galacto-oligosaccharide mixture in reducing travellers’ diarrhoea. Eur. J. Clin. Nutr.64, 146–152 (2010). CASPubMedGoogle Scholar
  158. Micka, A., Siepelmeyer, A., Holz, A., Theis, S. & Schon, C. Effect of consumption of chicory inulin on bowel function in healthy subjects with constipation: a randomized, double-blind, placebo-controlled trial. Int. J. Food Sci. Nutr.68, 82–89 (2017). CASPubMedGoogle Scholar
  159. European Food Safety Authority Panel on Dietetic Products. Scientific opinion on the substantiation of a health claim related to “native chicory inulin” and maintenance of normal defecation by increasing stool frequency pursuant to article 13.5 of regulation (EC) No 1924/2006. EFSA J.13, 3951 (2015). Google Scholar
  160. Hume, M. P., Nicolucci, A. C. & Reimer, R. A. Prebiotic supplementation improves appetite control in children with overweight and obesity: a randomized controlled trial. Am. J. Clin. Nutr.105, 790–799 (2017). CASPubMedGoogle Scholar
  161. Nicolucci, A. C. et al. Prebiotics reduce body fat and alter intestinal microbiota in children who are overweight or with obesity. Gastroenterology153, 711–722 (2017). PubMedGoogle Scholar
  162. Pol, K., de Graaf, C., Meyer, D. & Mars, M. The efficacy of daily snack replacement with oligofructose-enriched granola bars in overweight and obese adults: a 12-week randomised controlled trial. Br. J. Nutr.119, 1076–1086 (2018). CASPubMedGoogle Scholar
  163. Liber, A. & Szajewska, H. Effect of oligofructose supplementation on body weight in overweight and obese children: a randomised, double-blind, placebo-controlled trial. Br. J. Nutr.112, 2068–2074 (2014). CASPubMedGoogle Scholar
  164. European Food Safety Authority Panel on Dietetic Products. Scientific opinion on the substantiation of a health claim related to non-digestible carbohydrates and a reduction of post-prandial glycaemic responses pursuant to article 13(5) of regulation (EC) No 1924/2006. EFSA J.12, 3513 (2015). Google Scholar
  165. Lightowler, H., Thondre, S., Holz, A. & Theis, S. Replacement of glycaemic carbohydrates by inulin-type fructans from chicory (oligofructose, inulin) reduces the postprandial blood glucose and insulin response to foods: report of two double-blind, randomized, controlled trials. Eur. J. Nutr.57, 1259–1268 (2018). CASPubMedGoogle Scholar
  166. Olbjorn, C. et al. Fecal microbiota profiles in treatment-naive pediatric inflammatory bowel disease - associations with disease phenotype, treatment, and outcome. Clin. Exp. Gastroenterol.12, 37–49 (2019). PubMedPubMed CentralGoogle Scholar
  167. Backhed, F. et al. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe12, 611–622 (2012). PubMedGoogle Scholar
  168. Dey, M. Toward a personalized approach in prebiotics research. Nutrients9, 92 (2017). PubMed CentralGoogle Scholar
  169. Healey, G. et al. Habitual dietary fibre intake influences gut microbiota response to an inulin-type fructan prebiotic: a randomised, double-blind, placebo-controlled, cross-over, human intervention study. Br. J. Nutr.119, 176–189 (2018). CASPubMedGoogle Scholar
  170. Tandon, D. et al. A prospective randomized, double-blind, placebo-controlled, dose-response relationship study to investigate efficacy of fructo-oligosaccharides (FOS) on human gut microflora. Sci. Rep.9, 5473 (2019). PubMedPubMed CentralGoogle Scholar
  171. Bian, G. et al. The gut microbiota of healthy aged Chinese is similar to that of the healthy young. mSphere2, e00327–17 (2017). PubMedPubMed CentralGoogle Scholar
  172. Gloor, G. B., Macklaim, J. M., Pawlowsky-Glahn, V. & Egozcue, J. J. Microbiome datasets are compositional: and this is not optional. Front. Microbiol.8, 2224 (2017). PubMedPubMed CentralGoogle Scholar
  173. Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature486, 222–227 (2012). This study considers the gut microbiome in evaluating human development, nutritional needs, physiological variations and the effects of westernization. CASPubMedPubMed CentralGoogle Scholar
  174. Marques, T. M. et al. Programming infant gut microbiota: influence of dietary and environmental factors. Curr. Opin. Biotechnol.21, 149–156 (2010). CASPubMedGoogle Scholar
  175. Claesson, M. J. et al. Gut microbiota composition correlates with diet and health in the elderly. Nature488, 178–184 (2012). CASPubMedGoogle Scholar
  176. Clarke, S. F. et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut63, 1913–1920 (2014). CASPubMedGoogle Scholar
  177. Engen, P. A., Green, S. J., Voigt, R. M., Forsyth, C. B. & Keshavarzian, A. The gastrointestinal microbiome: alcohol effects on the composition of intestinal microbiota. Alcohol Res.37, 223–236 (2015). PubMedPubMed CentralGoogle Scholar
  178. Jostins, L. et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature491, 119–124 (2012). CASPubMedPubMed CentralGoogle Scholar
  179. Picoraro, J. A. & LeLeiko, N. S. Omes of inflammatory bowel disease: a primer for clinicians. J. Pediatr. Gastroenterol. Nutr.66, 374–377 (2018). PubMedGoogle Scholar
  180. Weiser, M. et al. Molecular classification of Crohn’s disease reveals two clinically relevant subtypes. Gut67, 36–42 (2018). CASPubMedGoogle Scholar
  181. Bourreille, A. et al. Saccharomyces boulardii does not prevent relapse of Crohn’s disease. Clin. Gastroenterol. Hepatol.11, 982–987 (2013). PubMedGoogle Scholar
  182. Van Gossum, A. et al. Multicenter randomized-controlled clinical trial of probiotics (Lactobacillus johnsonii, LA1) on early endoscopic recurrence of Crohn’s disease after ileo-caecal resection. Inflamm. Bowel Dis.13, 135–142 (2007). PubMedGoogle Scholar
  183. Tursi, A. et al. Treatment of relapsing mild-to-moderate ulcerative colitis with the probiotic VSL#3 as adjunctive to a standard pharmaceutical treatment: a double-blind, randomized, placebo-controlled study. Am. J. Gastroenterol.105, 2218–2227 (2010). PubMedPubMed CentralGoogle Scholar
  184. O’Toole, P. W., Marchesi, J. R. & Hill, C. Next-generation probiotics: the spectrum from probiotics to live biotherapeutics. Nat. Microbiol.2, 17057 (2017). PubMedGoogle Scholar
  185. Ridaura, V. K. et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science341, 1241214 (2013). PubMedGoogle Scholar
  186. van Nood, E. et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med.368, 407–415 (2013). PubMedGoogle Scholar
  187. Lee, C. H. et al. Frozen versus fresh fecal microbiota transplantation and clinical resolution of diarrhea in patients with recurrent Clostridium difficile infection: a randomized clinical trial. JAMA315, 142–149 (2016). CASPubMedGoogle Scholar
  188. Kelly, C. R. et al. Effect of fecal microbiota transplantation on recurrence in multiply recurrent Clostridium difficile infection: a randomized trial. Ann. Intern. Med.165, 609–616 (2016). PubMedPubMed CentralGoogle Scholar
  189. Halkjaer, S. I. et al. Faecal microbiota transplantation alters gut microbiota in patients with irritable bowel syndrome: results from a randomised, double-blind placebo-controlled study. Gut67, 2107–2115 (2018). CASPubMedGoogle Scholar
  190. Delaune, V. et al. Fecal microbiota transplantation: a promising strategy in preventing the progression of non-alcoholic steatohepatitis and improving the anti-cancer immune response. Expert Opin. Biol. Ther.18, 1061–1071 (2018). PubMedGoogle Scholar
  191. Moayyedi, P. et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology149, 102–109 (2015). PubMedGoogle Scholar
  192. Gupta, S., Allen-Vercoe, E. & Petrof, E. O. Fecal microbiota transplantation: in perspective. Therap. Adv. Gastroenterol.9, 229–239 (2016). PubMedPubMed CentralGoogle Scholar
  193. Reid, G. et al. How do probiotics and prebiotics function at distant sites? Benef. Microbes8, 521–533 (2017). An ISAPP working group article that looks at how microbiome programming in early life influences the gut microbiota communication with distant sites, such as airways, heart and brain, and influences metabolism. CASPubMedGoogle Scholar
  194. Hiippala, K. et al. The potential of gut commensals in reinforcing intestinal barrier function and alleviating inflammation. Nutrients10, E988 (2018). PubMedGoogle Scholar
  195. Crusell, M. K. W. et al. Gestational diabetes is associated with change in the gut microbiota composition in third trimester of pregnancy and postpartum. Microbiome6, 89 (2018). PubMedPubMed CentralGoogle Scholar
  196. Cousin, F. J. et al. The probiotic Propionibacterium freudenreichii as a new adjuvant for TRAIL-based therapy in colorectal cancer. Oncotarget7, 7161–7178 (2016). PubMedPubMed CentralGoogle Scholar
  197. Zullo, B. A. & Ciafardini, G. Evaluation of physiological properties of yeast strains isolated from olive oil and their in vitro probiotic trait. Food Microbiol.78, 179–187 (2019). CASPubMedGoogle Scholar
  198. Gonzalez-Rodriguez, I. et al. Catabolism of glucose and lactose in Bifidobacterium animalis subsp. lactis, studied by 13C nuclear magnetic resonance. Appl. Environ. Microbiol.79, 7628–7638 (2013). CASPubMedPubMed CentralGoogle Scholar
  199. Kostinek, M. et al. Characterisation and biochemical properties of predominant lactic acid bacteria from fermenting cassava for selection as starter cultures. Int. J. Food Microbiol.114, 342–351 (2007). CASPubMedGoogle Scholar
  200. Hancock, T., Capon, A., Dooris, M. & Patrick, R. One planet regions: planetary health at the local level. Lancet Planet. Health1, e92–e93 (2017). PubMedGoogle Scholar
  201. Garchitorena, A. et al. Disease ecology, health and the environment: a framework to account for ecological and socio-economic drivers in the control of neglected tropical diseases. Philos. Trans. R. Soc. B.372, 20160128 (2017). Google Scholar

Acknowledgements

Reviewer information

Nature Reviews Gastroenterology & Hepatology thanks H. Szajewska, and the other, anonymous, reviewer(s), for their contribution to the peer review of this work.