Dynamic in vitro models of the human gastrointestinal tract as relevant tools to assess the survival of probiotic strains and their interactions with gut microbiota

Microorganisms

Volumn 3, Issue 4, 2015, Pages 725-745

  Cordonnier, Charlotte ^a,b   Thévenot, Jonathan ^a,b   Etienne Mesmin, Lucie ^a,b   Denis, Sylvain ^a   Alric, Monique ^a   Livrelli, Valérie ^b,c   Blanquet Diot, Stéphanie ^a  

^a CRNH AUVERGNE   (France)

^b INSERM   (France)

^c UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

Author keywords

Food matrix; Human gastrointestinal tract; In vitro models; Intestinal microbiota; Probiotic; Saccharomyces cerevisiae; Survival

Indexed keywords

EID: 85014919479     PISSN: None     EISSN: 20762607     Source Type: Journal    
DOI: 10.3390/microorganisms3040725     Document Type: Article

References (52)

1. Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; 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. 2014, 11, 506–514.
2. Hatoum, R.; Labrie, S.; Fliss, I. Antimicrobial and probiotic properties of yeasts: From fundamental to novel applications. Front. Microbiol. 2012, 3, 1–12.
3. Kelesidis, T.; Pothoulakis, C. Efficacy and safety of the probiotic Saccharomyces boulardii for the prevention and therapy of gastrointestinal disorders. Therap. Adv. Gastroenterol. 2012, 5, 111–125.
4. Im, E.; Pothoulakis, C. Recent advances in Saccharomyces boulardii research. Gastroenterol. Clin. Biol. 2010, 34, S62–S70.
5. McFarland, L.V. Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J. Gastroenterol. 2010, 16, 2202–2222.
6. Foligné, B.; Dewulf, J.; Vandekerckove, P.; Pignède, G.; Pot, B. Probiotic yeasts: Anti-inflammatory potential of various non-pathogenic strains in experimental colitis in mice. World J. Gastroenterol. 2010, 16, 2134–2145.
7. Sivignon, A.; de Vallée, A.; Barnich, N.; Denizot, J.; Darcha, C.; Pignède, G.; Vandekerckove, P.; Darfeuille-Michaud, A. Saccharomyces cerevisiae CNCM I-3856 prevents colitis induces by AIEC bacteria in transgenic mouse model mimicking Crohn’s disease. Inflamm. Bowel Dis. 2015, 21, 276–286.
8. De Chambrun, G.P.; Neut, C.; Chau, A.; Cazaubiel, M.; Pelerin, F.; Justen, P.; Desreumaux, P. A randomized clinical trial of Saccharomyces cerevisiae versus placebo in the irritable bowel syndrome. Dig. Liver Dis. 2015, 47, 119–1
9. Zanello, G.; Berri, M.; Dupont, J.; Sizaret, P.Y.; D’Inca, R.; Salmon, H.; Meurens, F. Saccharomyces cerevisiae modulates immune gene expressions and inhibits ETEC-mediated ERK1/2 and p38 signaling pathways in intestinal epithelial cells. PLoS ONE 2011, doi:10.1371/journal.pone.0018573.
10. Etienne-Mesmin, L.; Livrelli, V.; Privat, M.; Denis, S.; Cardot, J.M.; Alric, M.; Blanquet-Diot, S. Effect of a new probiotic Saccharomyces cerevisiae strain on survival of Escherichia coli O157:H7 in a dynamic gastrointestinal model. Appl. Environ. Microb. 2011, 77, 1127–1131.
11. Thévenot, J.; Cordonnier, C.; Rougeron, A.; Le Goff, O.; Nguyen, H.T.T.; Denis, S.; Alric, M.; Livrelli, V.; Blanquet-Diot, S. Enterohemorrhagic Escherichia coli infection has donor-dependent effect on human gut microbiota and may be antagonized by probiotic yeast during interaction with Peyer’s patches. Appl. Microbiol. Biotechnol. 2015, 99, 1–14.
12. Thévenot, J.; Etienne-Mesmin, L.; Denis, S.; Chalancon, S.; Alric, M.; Livrelli, V.; Blanquet-Diot, S. Enterohemorrhagic Escherichia coli O157:H7 survival in an in vitro model of the human large intestine and interactions with probiotic yeasts and resident microbiota. Appl. Environ. Microbiol. 2013, 79, 1058–1064.
13. Blanquet-Diot, S.; Denis, S.; Chalancon, S.; Chaira, F.; Cardot, J.M.; Alric, M. Use of artificial digestive systems to investigate the biopharmaceutical factors influencing the survival of probiotic yeast during gastrointestinal transit in humans. Pharm. Res. 2012, 29, 1444–1453.
14. Elashoff, J.D.; Reedy, T.J.; Meyer, J.H. Analysis of gastric emptying data. Gastroenterology 1982, 83, 1306–1312.
15. Minekus, M. The TNO Gastro-Intestinal Model (TIM). In The Impact of Food Bioactives on Health; Springer: Doetinchem, The Netherlands, 2015; pp. 37–46.
16. Minekus, M.; Marteau, P.; Havenaar, R.; Huis in’t Veld, J.H. A multi-compartmental dynamic computer-controlled model simulating the stomach and small intestine. ATLA 1995, 23, 197–209.
17. Macfarlane, G.; Macfarlane, S.; Gibson, G. Validation of a three-stage compound continuous culture system for investigating the effect of retention time on the ecology and metabolism of bacteria in the human colon. Microb. Ecol. 1998, 35, 180–187.
18. Yu, Z.; Morrison, M. Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques 2004, 36, 808–813.
19. Yu, Y.; Lee, C.; Kim, J.; Hwang, S. Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol. Bioeng. 2005, 89, 670–679.
20. Bacchetti De Gregoris, T.; Aldred, N.; Clare, A.S.; Burgess, J.G. Improvement of phylum-and class-specific primers for real-time PCR quantification of bacterial taxa. J. Microbiol. Meth. 2011, 86, 351–356.
21. Bartosch, S.; Fite, A.; Macfarlane, G.T.; McMurdo, M.E. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl. Environ. Microb. 2004, 70, 3575–3581.
22. Furet, J.P.; Firmesse, O.; Gourmelon, M.; Bridonneau, C.; Tap, J.; Mondot, S.; Doré, J.; Corthier, G. Comparative assessment of human and farm animal faecal microbiota using real-time quantitative PCR. FEMS Microbiol. Ecol. 2009, 68, 351–362.
23. Martinez-Medina, M.; Denizot, J.; Dreux, N.; Robin, F.; Billard, E.; Bonnet, R.; Darfeuille-Michaud, A.; Barnich, N. Western diet induces dysbiosis with increased E. coli in CEABAC10 mice, alters host barrier function favouring AIEC colonisation. Gut 2014, 63, 116–124.
24. Huijsdens, X.W.; Linskens, R.K.; Mak, M.; Meuwissen, S.G.; Vandenbroucke-Grauls, C.M.; Savelkoul, P.H. Quantification of bacteria adherent to gastrointestinal mucosa by real-time PCR. J. Clin. Microbiol. 2002, 40, 4423–4427.
25. Noguchi, K.; Gel, Y.R.; Brunner, E.; Konietschke, F. nparLD: An R software package for the nonparametric analysis of longitudinal data in factorial experiments. J. Stat. Softw. 2012, 50, 1–23.
26. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2014.
27. Konietschke, F.; Placzek, M.; Schaarschmidt, F.; Hothorn, L.A. nparcomp: An R software package for nonparametric multiple comparisons and simultaneous confidence intervals. J. Stat. Softw. 2015, 64, 1–17.
28. Kuznetsova, A.; Bruun Brockhoff, P.; Haubo Bojesen Christensen, R. lmerTest: Tests in Linear Mixed Effects Models, 2014; R package version 2.0-20. Avaliable online: https://cran.r-project.org/web/packages/lmerTest/index.html (accessed on 25 September 2015).
29. Guerra, A.; Etienne-Mesmin, L.; Livrelli, V.; Denis, S.; Blanquet-Diot, S.; Alric, M. Relevance and challenges in modeling human gastric and small intestinal digestion. Trends Biotechnol. 2012, 30, 591–600.
30. Payne, A.N.; Zihler, A.; Chassard, C.; Lacroix, C. Advances and perspectives in in vitro human gut fermentation modeling. Trends Biotechnol. 2012, 30, 17–25.
31. Do Espirito Santo, A.P.; Perego, P.; Converti, A.; Oliveira, M.N. Influence of food matrices on probiotic viability—A review focusing on the fruity bases. Trends Food Sci. Technol. 2011, 22, 377–385.
32. Possemiers, S.; Marzorati, M.; Verstraete, W.; van de Wiele, T. Bacteria and chocolate: a successful combination for probiotic delivery. Int. J. Food Microbiol. 2010, 141, 97–103.
33. Graff, S.; Chaumeil, J.C.; Boy, P.; Lai-Kuen, R.; Charrueau, C. Formulations for protecting the probiotic Saccharomyces boulardii from degradation in acidic condition. Biol. Pharm. Bull. 2008, 31, 266–272.
34. Ghelardi, E.; Celandroni, F.; Salvetti, S.; Gueye, S.; Lupetti, A.; Senesi, S. Survival and persistence of Bacillus clausii in the human gastrointestinal tract following oral administration as spore-based probiotic formulation. J. Appl. Microbiol. 2015, 119, 552–559.
35. Cheow, W.S.; Kiew, T.Y.; Hadinoto, K. Controlled release of Lactobacillus rhamnosus biofilm probiotics from alginate-locust bean gum microcapsules. Carbohydr. Polym. 2014, 103, 587–595.
36. R○ system. J. Pharm. Sci. 2015, 104, 2855–2863.
37. Murray, R.; Eddy, D.E.; Bartoli, W.P.; Paul, G.L. Gastric emptying of water and isocaloric carbohydrate solutions consumed at rest. Med. Sci. Sports Exerc. 1994, 26, 725–732.
38. Worsøe, J.; Fynne, L.; Gregersen, T.; Schlageter, V.; Christensen, L.A.; Dahlerup, J.F.; Rijkhoff, N.J.; Laurberg, S.; Krogh, K. Gastric transit and small intestinal transit time and motility assessed by a magnet tracking system. BMC Gastroenterol. 2011, 11, 1–10.
39. Mattioli, G. Pancreatic secretory response to ordinary meals: Studies with pure pancreatic juice. Gastroenterology 1988, 94, 426–433.
40. Northfield, T.; McColl, I. Postprandial concentrations of free and conjugated bile acids down the length of the normal human small intestine. Gut 1973, 14, 513–518.
41. Vertzoni, M.; Archontaki, H.; Reppas, C. Determination of intralumenal individual bile acids by HPLC with charged aerosol detection. J. Lipid Res. 2008, 49, 2690–2695.
42. Elmer, G.; McFarland, L.; Surawicz, C.; Danko, L.; Greenberg, R. Behaviour of Saccharomyces boulardii in recurrent Clostridium difficile disease patients. Aliment. Pharmacol. Ther. 1999, 13, 1663–1668.
43. Minelli, E.B.; Benini, A. Relationship between number of bacteria and their probiotic effects. Microb. Ecol. Health Dis. 2008, 20, 180–183.
44. Klein, S.M.; Elmer, G.W.; McFarland, L.V.; Surawicz, C.M.; Levy, R.H. Recovery and elimination of the biotherapeutic agent, Saccharomyces boulardii, in healthy human volunteers. Pharm. Res. 1993, 10, 1615–1619.
45. Pecquet, S.; Guillaumin, D.; Tancrede, C.; Andremont, A. Kinetics of Saccharomyces cerevisiae elimination from the intestines of human volunteers and effect of this yeast on resistance to microbial colonization in gnotobiotic mice. Appl. Environ. Microbiol. 1991, 57, 3049–3051.
46. Fietto, J.L.; Araújo, R.S.; Valadão, F.N.; Fietto, L.G.; Brandão, R.L.; Neves, M.J.; Gomes, F.C.; Nicoli, J.R.; Castro, I.M. Molecular and physiological comparisons between Saccharomyces cerevisiae and Saccharomyces boulardii. Can. J. Microbiol. 2004, 50, 615–621.
47. Graff, S.; Chaumeil, J.C.; Boy, P.; Lai-Kuen, R.; Charrueau, C. Influence of pH conditions on the viability of Saccharomyces boulardii yeast. J. Gen. Appl. Microbiol. 2008, 54, 221–227.
48. Swidsinski, A.; Loening-Baucke, V.; Kirsch, S.; Doerffel, Y. Functional biostructure of colonic microbiota (central fermenting area, germinal stock area and separating mucus layer) in healthy subjects and patients with diarrhea treated with Saccharomyces boulardii. Gastroenterol. Clin. Biol. 2010, 34, S79–S92.
49. Vanhoutte, T.; de Preter, V.; de Brandt, E.; Verbeke, K.; Swings, J.; Huys, G. Molecular monitoring of the fecal microbiota of healthy human subjects during administration of lactulose and Saccharomyces boulardii. Appl. Environ. Microbiol. 2006, 72, 5990–5997.
50. Bolnick, D.I.; Snowberg, L.K.; Hirsch, P.E.; Lauber, C.L.; Parks, B.; Lusis, A.J.; Knight, R.; Caporaso, J.G.; Svanbäck, R. Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat. Commun. 2014, 5, 1–13.
51. Schneider, S.M.; Girard-Pipau, F.; Filippi, J.; Hébuterne, X.; Moyse, D.; Hinojosa, G.C.; Pompei, A.; Rampal, P. Effects of Saccharomyces boulardii on fecal short-chain fatty acids and microflora in patients on long-term total enteral nutrition. World J. Gastroenterol. 2005, 11, 6165–6169.
52. Everard, A.; Matamoros, S.; Geurts, L.; Delzenne, N.M.; Cani, P.D. Saccharomyces boulardii administration changes gut microbiota and reduces hepatic steatosis, low-grade inflammation, and fat mass in obese and type 2 diabetic db/db mice. MBio 2014, 5, e01011–e01014.