Design and reporting of prebiotic and probiotic clinical trials in the context of diet and the gut microbiome.


Journal

Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869

Informations de publication

Date de publication:
Nov 2024
Historique:
received: 19 11 2023
accepted: 12 09 2024
medline: 31 10 2024
pubmed: 31 10 2024
entrez: 31 10 2024
Statut: ppublish

Résumé

Diet is a major determinant of the gastrointestinal microbiome composition and function, yet our understanding of how it impacts the efficacy of prebiotics and probiotics is limited. Here we examine current evidence of dietary influence on prebiotic and probiotic efficacy in human studies, including potential mechanisms. We propose that habitual diet be included as a variable in prebiotic and probiotic intervention studies. This recommendation is based on the potential mechanisms via which diet can affect study outcomes, either directly or through the gut microbiome. We consider the challenges and opportunities of dietary assessment in this context. Lastly, we provide recommendations for the design, conduct and reporting of human clinical trials of prebiotics and probiotics (and other biotic interventions) to account for any effect of diet and nutrition.

Identifiants

pubmed: 39478082
doi: 10.1038/s41564-024-01831-6
pii: 10.1038/s41564-024-01831-6
doi:

Substances chimiques

Prebiotics 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

2785-2794

Informations de copyright

© 2024. Springer Nature Limited.

Références

Gill, S. K., Rossi, M., Bajka, B. & Whelan, K. Dietary fibre in gastrointestinal health and disease. Nat. Rev. Gastroenterol. Hepatol. 18, 101–116 (2021).
pubmed: 33208922 doi: 10.1038/s41575-020-00375-4
Gunn, D. et al. Contrasting effects of viscous and particulate fibers on colonic fermentation in vitro and in vivo, and their impact on intestinal water studied by MRI in a randomized trial. Am. J. Clin. Nutr. 112, 595–602 (2020).
pubmed: 32619212 doi: 10.1093/ajcn/nqaa173
Falony, G. et al. Population-level analysis of gut microbiome variation. Science 352, 560–564 (2016).
pubmed: 27126039 doi: 10.1126/science.aad3503
Singh, R. K. et al. Influence of diet on the gut microbiome and implications for human health. J. Transl. Med. 15, 73 (2017).
pubmed: 28388917 pmcid: 5385025 doi: 10.1186/s12967-017-1175-y
Gougoulias, C. et al. Changes in the intestinal microbiota after a short period of dietary over-indulgence, representative of a holiday or festival season. Food Sci. Technol. Bull. Funct. Foods 5, 51–59 (2009).
doi: 10.1616/1476-2137.15493
Kampmann, C., Dicksved, J., Engstrand, L. & Rautelin, H. Changes to human faecal microbiota after international travel. Travel Med. Infect. Dis. 44, 102199 (2021).
pubmed: 34781018 doi: 10.1016/j.tmaid.2021.102199
Sonnenburg, E. D. & Sonnenburg, J. L. Starving our microbial self: the deleterious consequences of a diet deficient in microbiota-accessible carbohydrates. Cell Metab. 20, 779–786 (2014).
pubmed: 25156449 pmcid: 4896489 doi: 10.1016/j.cmet.2014.07.003
Holmes, A. J. et al. Diet–microbiome interactions in health are controlled by intestinal nitrogen source constraints. Cell Metab. 25, 140–151 (2017).
pubmed: 27889387 doi: 10.1016/j.cmet.2016.10.021
Rodionov, D. A. et al. Micronutrient requirements and sharing capabilities of the human gut microbiome. Front. Microbiol. 10, 1316 (2019).
pubmed: 31275260 pmcid: 6593275 doi: 10.3389/fmicb.2019.01316
Leeming, E. R., Johnson, A. J., Spector, T. D. & Le Roy, C. I. Effect of diet on the gut microbiota: rethinking intervention duration. Nutrients 11, 2862 (2019).
pubmed: 31766592 doi: 10.3390/nu11122862
Johnson, A. J. et al. Daily sampling reveals personalizedd diet–microbiome associations in humans. Cell Host Microbe 25, 789–802.e5 (2019).
pubmed: 31194939 doi: 10.1016/j.chom.2019.05.005
Gehrig, J. L. et al. Effects of microbiota-directed foods in gnotobiotic animals and undernourished children. Science 365, eaau4732 (2019).
pubmed: 31296738 doi: 10.1126/science.aau4732
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).
pubmed: 28611480 doi: 10.1038/nrgastro.2017.75
Wilson, B. & Whelan, K. Prebiotic inulin-type fructans and galacto-oligosaccharides: definition, specificity, function, and application in gastrointestinal disorders. J. Gastroenterol. Hepatol. 32, 64–68 (2017).
pubmed: 28244671 doi: 10.1111/jgh.13700
So, D. et al. Dietary fiber intervention on gut microbiota composition in healthy adults: a systematic review and meta-analysis. Am. J. Clin. Nutr. 107, 965–983 (2018).
pubmed: 29757343 doi: 10.1093/ajcn/nqy041
Gibson, G. R., Beatty, E. R., Wang, X. & Cummings, J. H. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975–982 (1995).
pubmed: 7698613 doi: 10.1016/0016-5085(95)90192-2
Ramirez-Farias, C. et al. Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br. J. Nutr. 101, 541–550 (2009).
pubmed: 18590586 doi: 10.1017/S0007114508019880
Jackson, P. P. et al. Inulin-type fructans and 2′fucosyllactose alter both microbial composition and appear to alleviate stress-induced mood state in a working population compared to placebo (maltodextrin): the EFFICAD Trial, a randomized, controlled trial. Am. J. Clin. Nutr. 118, 938–955 (2023).
pubmed: 37657523 pmcid: 10636234 doi: 10.1016/j.ajcnut.2023.08.016
Dou, Y. et al. Effect of fructooligosaccharides supplementation on the gut microbiota in human: a systematic review and meta-analysis. Nutrients 14, 3298 (2022).
pubmed: 36014803 pmcid: 9413759 doi: 10.3390/nu14163298
Boets, E. et al. Quantification of in vivo colonic short chain fatty acid production from inulin. Nutrients 7, 8916–8929 (2015).
pubmed: 26516911 pmcid: 4663568 doi: 10.3390/nu7115440
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).
pubmed: 24912386 doi: 10.1038/nrgastro.2014.66
Sanders, M. E., Merenstein, D. J., Reid, G., Gibson, G. R. & Rastall, R. A. Probiotics and prebiotics in intestinal health and disease: from biology to the clinic. Nat. Rev. Gastroenterol. Hepatol. 16, 605–616 (2019).
pubmed: 31296969 doi: 10.1038/s41575-019-0173-3
Kristensen, N. B. et al. Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: a systematic review of randomized controlled trials. Genome Med. 8, 52 (2016).
pubmed: 27159972 doi: 10.1186/s13073-016-0300-5
Liang, D., Wu, F., Zhou, D., Tan, B. & Chen, T. Commercial probiotic products in public health: current status and potential limitations. Crit. Rev. Food Sci. Nutr. 64, 6455–6476 (2024).
pubmed: 36688290 doi: 10.1080/10408398.2023.2169858
Marco, M. L. et al. A classification system for defining and estimating dietary intake of live microbes in US adults and children. J. Nutr. 152, 1729–1736 (2022).
pubmed: 35583208 doi: 10.1093/jn/nxac074
Guarner F. et al. World Gastroenterology Organisation Global Guidelines: Probiotics and Prebiotics (World Gastroenterology Organisation, 2023).
McFarland, L. V., Evans, C. T. & Goldstein, E. J. C. Strain-specificity and disease-specificity of probiotic efficacy: a systematic review and meta-analysis. Front. Med. 5, 124 (2018).
doi: 10.3389/fmed.2018.00124
Wilson, B., Rossi, M., Dimidi, E. & Whelan, K. Prebiotics in irritable bowel syndrome and other functional bowel disorders in adults: a systematic review and meta-analysis of randomized controlled trials. Am. J. Clin. Nutr. 109, 1098–1111 (2019).
pubmed: 30949662 doi: 10.1093/ajcn/nqy376
Teo, Y. Q. J. et al. Effects of probiotics, prebiotics and synbiotics on anthropometric, cardiometabolic and inflammatory markers: an umbrella review of meta-analyses. Clin. Nutr. 43, 1563–1583 (2024).
pubmed: 38754308 doi: 10.1016/j.clnu.2024.05.019
Holscher, H. D. et al. Agave inulin supplementation affects the fecal microbiota of healthy adults participating in a randomized, double-blind, placebo-controlled, crossover trial. J. Nutr. 145, 2025–2032 (2015).
pubmed: 26203099 doi: 10.3945/jn.115.217331
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).
pubmed: 29307330 doi: 10.1017/S0007114517003440
Healey, G. et al. Validity and reproducibility of a habitual dietary fibre intake short food frequency questionnaire. Nutrients 8, 558 (2016).
pubmed: 27626442 pmcid: 5037543 doi: 10.3390/nu8090558
Holmes, Z. C. et al. Microbiota responses to different prebiotics are conserved within individuals and associated with habitual fiber intake. Microbiome 10, 114 (2022).
pubmed: 35902900 pmcid: 9336045 doi: 10.1186/s40168-022-01307-x
Eid, N. et al. Impact of palm date consumption on microbiota growth and large intestinal health: a randomised, controlled, cross-over, human intervention study. Br. J. Nutr. 114, 1226–1236 (2015).
pubmed: 26428278 doi: 10.1017/S0007114515002780
Shin, J. H. et al. Effect of Saengshik supplementation on the gut microbial composition of healthy Korean adults: a single-group pilot study. Front. Nutr. 8, 743620 (2021).
pubmed: 34746209 pmcid: 8568882 doi: 10.3389/fnut.2021.743620
Bergeron, N. et al. Diets high in resistant starch increase plasma levels of trimethylamine-N-oxide, a gut microbiome metabolite associated with CVD risk. Br. J. Nutr. 116, 2020–2029 (2016).
pubmed: 27993177 pmcid: 5885763 doi: 10.1017/S0007114516004165
Maier, T. V. et al. Impact of dietary resistant starch on the human gut microbiome, metaproteome, and metabolome. mBio 8, e01343-17 (2017).
pubmed: 29042495 pmcid: 5646248 doi: 10.1128/mBio.01343-17
Salonen, A. et al. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J. 8, 2218–2230 (2014).
pubmed: 24763370 pmcid: 4992075 doi: 10.1038/ismej.2014.63
Tap, J. et al. Gut microbiota richness promotes its stability upon increased dietary fibre intake in healthy adults. Environ. Microbiol. 17, 4954–4964 (2015).
pubmed: 26235304 doi: 10.1111/1462-2920.13006
Wastyk, H. C. et al. Randomized controlled trial demonstrates response to a probiotic intervention for metabolic syndrome that may correspond to diet. Gut Microbes 15, 2178794 (2023).
pubmed: 36803658 pmcid: 9980610 doi: 10.1080/19490976.2023.2178794
Hasain, Z. et al. Diet and pre-intervention washout modifies the effects of probiotics on gestational diabetes mellitus: a comprehensive systematic review and meta-analysis of randomized controlled trials. Nutrients 13, 3045 (2021).
pubmed: 34578921 pmcid: 8465224 doi: 10.3390/nu13093045
Swanson, K. S. et al. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nat. Rev. Gastroenterol. Hepatol. 17, 687–701 (2020).
pubmed: 32826966 pmcid: 7581511 doi: 10.1038/s41575-020-0344-2
Zhang, X. F. et al. Clinical effects and gut microbiota changes of using probiotics, prebiotics or synbiotics in inflammatory bowel disease: a systematic review and meta-analysis. Eur. J. Nutr. 60, 2855–2875 (2021).
pubmed: 33555375 doi: 10.1007/s00394-021-02503-5
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. Microbiome 6, 121 (2018).
pubmed: 29954454 pmcid: 6022452 doi: 10.1186/s40168-018-0494-4
De Giani, A. et al. Effects of inulin-based prebiotics alone or in combination with probiotics on human gut microbiota and markers of immune system: a randomized, double-blind, placebo-controlled study in healthy subjects. Microorganisms 10, 1256 (2022).
pubmed: 35744774 pmcid: 9229734 doi: 10.3390/microorganisms10061256
Wang, J., Zhang, J., Liu, W., Zhang, H. & Sun, Z. Metagenomic and metatranscriptomic profiling of Lactobacillus casei Zhang in the human gut. NPJ Biofilms Microbiomes 7, 55 (2021).
pubmed: 34210980 pmcid: 8249650 doi: 10.1038/s41522-021-00227-2
Marco, M. L. et al. Convergence in probiotic Lactobacillus gut-adaptive responses in humans and mice. ISME J. 4, 1481–1484 (2010).
pubmed: 20505752 doi: 10.1038/ismej.2010.61
Marco, M. L. et al. Lifestyle of Lactobacillus plantarum in the mouse caecum. Environ. Microbiol. 11, 2747–2757 (2009).
pubmed: 19638173 pmcid: 2978903 doi: 10.1111/j.1462-2920.2009.02001.x
Goh, Y. J., Barrangou, R. & Klaenhammer, T. R. In vivo transcriptome of Lactobacillus acidophilus and colonization impact on murine host intestinal gene expression. mBio 12, e03399-20 (2021).
pubmed: 33500337 pmcid: 7858073 doi: 10.1128/mBio.03399-20
Tachon, S., Lee, B. & Marco, M. L. Diet alters probiotic Lactobacillus persistence and function in the intestine. Environ. Microbiol. 16, 2915–2926 (2014).
pubmed: 24118739 doi: 10.1111/1462-2920.12297
Maldonado-Gómez, M. X. et al. Stable engraftment of Bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome. Cell Host Microbe 20, 515–526 (2016).
pubmed: 27693307 doi: 10.1016/j.chom.2016.09.001
O’Brien, C. E. et al. Early probiotic supplementation with B. infantis in breastfed infants leads to persistent colonization at 1 year. Pediatr. Res. 91, 627–636 (2022).
pubmed: 33762689 doi: 10.1038/s41390-020-01350-0
Yin, X., Lee, B., Zaragoza, J. & Marco, M. L. Dietary perturbations alter the ecological significance of ingested Lactobacillus plantarum in the digestive tract. Sci. Rep. 7, 7267 (2017).
pubmed: 28779118 doi: 10.1038/s41598-017-07428-w
Whitton, C. et al. A systematic review examining contributors to misestimation of food and beverage intake based on short-term self-report dietary assessment instruments administered to adults. Adv. Nutr. 13, 2620–2665 (2022).
pubmed: 36041186 doi: 10.1093/advances/nmac085
Macdiarmid, J. & Blundell, J. Assessing dietary intake: who, what and why of under-reporting. Nutr. Res. Rev. 11, 231–253 (1998).
pubmed: 19094249 doi: 10.1079/NRR19980017
Ovaskainen, M. L. et al. Accuracy in the estimation of food servings against the portions in food photographs. Eur. J. Clin. Nutr. 62, 674–681 (2008).
pubmed: 17440523 doi: 10.1038/sj.ejcn.1602758
Hebert, J. R. et al. Gender differences in social desirability and social approval bias in dietary self-report. Am. J. Epidemiol. 146, 1046–1055 (1997).
pubmed: 9420529 doi: 10.1093/oxfordjournals.aje.a009233
Armet, A. M. et al. Rethinking healthy eating in light of the gut microbiome. Cell Host Microbe 30, 764–785 (2022).
pubmed: 35679823 doi: 10.1016/j.chom.2022.04.016
Cotillard, A. et al. A posteriori dietary patterns better explain variations of the gut microbiome than individual markers in the American Gut Project. Am. J. Clin. Nutr. 115, 432–443 (2022).
pubmed: 34617562 doi: 10.1093/ajcn/nqab332
Power, S. E., O’Toole, P. W., Stanton, C., Ross, R. P. & Fitzgerald, G. F. Intestinal microbiota, diet and health. Br. J. Nutr. 111, 387–402 (2014).
pubmed: 23931069 doi: 10.1017/S0007114513002560
Whelan, K., Bancil, A. S., Lindsay, J. O. & Chassaing, B. Ultra-processed foods and food additives in gut health and disease. Nat. Rev. Gastroenterol. Hepatol. 21, 406–427 (2024).
pubmed: 38388570 doi: 10.1038/s41575-024-00893-5
Bingham, S. A. The dietary assessment of individuals: methods, accuracy, new techniques and recommendations. Nutr. Abstr. Rev. 57, 705–742 (1987).
Bingham, S. A. et al. Validation of weighed records and other methods of dietary assessment using the 24 h urine nitrogen technique and other biological markers. Br. J. Nutr. 73, 531–550 (1995).
pubmed: 7794870 doi: 10.1079/BJN19950057
Brussaard, J. H. et al. A European food consumption survey method—conclusions and recommendations. Eur. J. Clin. Nutr. 56, S89–S94 (2002).
pubmed: 12082521 doi: 10.1038/sj.ejcn.1601432
Stote, K. S., Radecki, S. V., Moshfegh, A. J., Ingwersen, L. A. & Baer, D. J. The number of 24 h dietary recalls using the US Department of Agriculture’s automated multiple-pass method required to estimate nutrient intake in overweight and obese adults. Public Health Nutr. 14, 1736–1742 (2011).
pubmed: 21414246 doi: 10.1017/S1368980011000358
Petrone, B. L. et al. Diversity of plant DNA in stool is linked to dietary quality, age, and household income. Proc. Natl Acad. Sci. USA 120, e2304441120 (2023).
pubmed: 37368926 doi: 10.1073/pnas.2304441120
Collins, C., McNamara, A. E. & Brennan, L. Role of metabolomics in identification of biomarkers related to food intake. Proc. Nutr. Soc. 78, 189–196 (2019).
pubmed: 30767789 doi: 10.1017/S002966511900048X
Schulz, K. F., Altman, D. G. & Moher, D. CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. Br. Med. J. 340, c332 (2010).
doi: 10.1136/bmj.c332
Shane, A. L. et al. Guide to designing, conducting, publishing and communicating results of clinical studies involving probiotic applications in human participants. Gut Microbes 1, 243–253 (2010).
pubmed: 21327031 doi: 10.4161/gmic.1.4.12707
Shanahan, E. R., McMaster, J. J. & Staudacher, H. M. Conducting research on diet–microbiome interactions: a review of current challenges, essential methodological principles, and recommendations for best practice in study design. J. Hum. Nutr. Diet. 34, 631–644 (2021).
pubmed: 33639033 doi: 10.1111/jhn.12868
Kaczmarek, J. L., Musaad, S. M. & Holscher, H. D. Time of day and eating behaviors are associated with the composition and function of the human gastrointestinal microbiota. Am. J. Clin. Nutr. 106, 1220–1231 (2017).
pubmed: 28971851 doi: 10.3945/ajcn.117.156380
Maifeld, A. et al. Fasting alters the gut microbiome reducing blood pressure and body weight in metabolic syndrome patients. Nat. Commun. 12, 1970 (2021).
pubmed: 33785752 pmcid: 8010079 doi: 10.1038/s41467-021-22097-0
Xiao, C. et al. Associations of dietary diversity with the gut microbiome, fecal metabolites, and host metabolism: results from 2 prospective Chinese cohorts. Am. J. Clin. Nutr. 116, 1049–1058 (2022).
pubmed: 36100971 pmcid: 9535526 doi: 10.1093/ajcn/nqac178
Su, J. et al. Remodeling of the gut microbiome during Ramadan-associated intermittent fasting. Am. J. Clin. Nutr. 113, 1332–1342 (2021).
pubmed: 33842951 pmcid: 8106760 doi: 10.1093/ajcn/nqaa388
Sanders, M. E. et al. Effects of genetic, processing, or product formulation changes on efficacy and safety of probiotics. Ann. NY Acad. Sci. 1309, 1–18 (2014).
pubmed: 24571253 doi: 10.1111/nyas.12363
Marteau, P. & Shanahan, F. Basic aspects and pharmacology of probiotics: an overview of pharmacokinetics, mechanisms of action and side-effects. Best Pr. Res. Clin. Gastroenterol. 17, 725–740 (2003).
doi: 10.1016/S1521-6918(03)00055-6
Segers, A. & Depoortere, I. Circadian clocks in the digestive system. Nat. Rev. Gastroenterol. Hepatol. 18, 239–251 (2021).
pubmed: 33531700 doi: 10.1038/s41575-020-00401-5
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).
pubmed: 28228425 doi: 10.3945/ajcn.116.140947
Suez, J. et al. Personalized microbiome-driven effects of non-nutritive sweeteners on human glucose tolerance. Cell 185, 3307–3328.e19 (2022).
pubmed: 35987213 doi: 10.1016/j.cell.2022.07.016
Chassaing, B. et al. Randomized controlled-feeding study of dietary emulsifier carboxymethylcellulose reveals detrimental impacts on the gut microbiota and metabolome. Gastroenterology 162, 743–756 (2022).
pubmed: 34774538 doi: 10.1053/j.gastro.2021.11.006
Dunn, S. et al. Validation of a food frequency questionnaire to measure intakes of inulin and oligofructose. Eur. J. Clin. Nutr. 65, 402–408 (2011).
pubmed: 21179053 doi: 10.1038/ejcn.2010.272
Turpin, W. et al. Mediterranean-like dietary pattern associations with gut microbiome composition and subclinical gastrointestinal inflammation. Gastroenterology 163, 685–698 (2022).
pubmed: 35643175 doi: 10.1053/j.gastro.2022.05.037
Terpou, A. et al. Probiotics in food systems: significance and emerging strategies towards improved viability and delivery of enhanced beneficial value. Nutrients 11, 1591 (2019).
pubmed: 31337060 pmcid: 6683253 doi: 10.3390/nu11071591
Jackson, P. P. J., Wijeyesekera, A., Theis, S., van Harsselaar, J. & Rastall, R. A. Food for thought! Inulin-type fructans: does the food matrix matter? J. Funct. Foods 90, 104987 (2022).
doi: 10.1016/j.jff.2022.104987
Jackson, P. P. J., Wijeyesekera, A., Theis, S., Van Harsselaar, J. & Rastall, R. A. Effects of food matrix on the prebiotic efficacy of inulin-type fructans: a randomised trial. Benef. Microbes 14, 317–334 (2023).
pubmed: 38661345 doi: 10.1163/18762891-20220120
Min, M., Bunt, C. R., Mason, S. L. & Hussain, M. A. Non-dairy probiotic food products: an emerging group of functional foods. Crit. Rev. Food Sci. Nutr. 59, 2626–2641 (2019).
pubmed: 29630845 doi: 10.1080/10408398.2018.1462760
Cunningham, M. et al. Applying probiotics and prebiotics in new delivery formats—is the clinical evidence transferable? Trends Food Sci. Technol. 112, 495–506 (2021).
doi: 10.1016/j.tifs.2021.04.009
Sanders, M. E. & Marco, M. L. Food formats for effective delivery of probiotics. Annu. Rev. Food Sci. Technol. 1, 65–85 (2010).
pubmed: 22129330 doi: 10.1146/annurev.food.080708.100743
Gomand, F. et al. Food matrix design for effective lactic acid bacteria delivery. Annu. Rev. Food Sci. Technol. 10, 285–310 (2019).
pubmed: 30633562 doi: 10.1146/annurev-food-032818-121140

Auteurs

Kevin Whelan (K)

Department of Nutritional Sciences, King's College London, London, UK. kevin.whelan@kcl.ac.uk.

Margaret Alexander (M)

Department of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI, USA.

Claire Gaiani (C)

Laboratoire d'Ingenierie des Biomolecules, Université de Lorraine, Nancy, France.
Institut Universitaire de France, Paris, France.

Genelle Lunken (G)

Department of Pediatrics, University of British Columbia, Vancouver, Canada.

Andrew Holmes (A)

School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia.
Charles Perkins Centre, University of Sydney, Sydney, New South Wales, Australia.

Heidi M Staudacher (HM)

Food and Mood Centre, IMPACT Institute, Deakin University, Melbourne, Victoria, Australia.

Stephan Theis (S)

BENEO-Institute, Obrigheim, Germany.

Maria L Marco (ML)

Department of Food Science and Technology, University of California, Davis, Davis, CA, USA. mmarco@ucdavis.edu.

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