Comparative analysis of intestinal tract models

Annual Review of Food Science and Technology

Volumn 6, Issue , 2015, Pages 329-350

  Williams, C F ^a   Walton, G E ^b   Jiang, L ^a   Plummer, S ^a   Garaiova, I ^a   Gibson, G R ^b  

^a CULTECH LTD   (United Kingdom)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

Gut microbiome; Intervention studies; Intestinal models

Indexed keywords

FOOD TECHNOLOGY;

COMPARATIVE ANALYSIS; COMPLEX ECOSYSTEMS; GUT MICROBIOTA; HUMAN INTERVENTION; INTERVENTION STUDIES; INTESTINAL TRACT; MICROBIAL COMMUNITIES; MICROBIOME;

DIAGNOSIS;

ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL MODEL; AUDIOVISUAL EQUIPMENT; COMPARATIVE STUDY; HUMAN; IN VITRO STUDY; INTESTINE; MICROBIOLOGY; MICROFLORA;

ANIMALS; HUMANS; IN VITRO TECHNIQUES; INTESTINES; MICROBIOTA; MODELS, ANATOMIC; MODELS, ANIMAL;

EID: 84928480730     PISSN: 19411413     EISSN: 19411421     Source Type: Journal    
DOI: 10.1146/annurev-food-022814-015429     Document Type: Review

References (138)

1. Alander M, De Smet I, Nollet L, Verstraete W, von Wright A, Mattila-Sandholm T. 1999a. The effect of probiotic strains on the microbiota of the Simulator of the Human Intestinal Microbial Ecosystem (SHIME). Int. J. Food Microbiol. 46:71-79
2. AlanderM, Satokari R, Korpela R, Saxelin M, Vilpponen-Salmela T, et al. 1999b. Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl. Environ. Microbiol. 65:351-54
3. Asahara T, Nomoto K, Shimizu K, Watanuki M, Tanaka R. 2001. Increased resistance ofmice to Salmonella enterica serovar Typhimurium infection by synbiotic administration of Bifidobacteria and transgalactosylated oligosaccharides. J. Appl. Microbiol. 91:985-96
4. Bahrami B, Child MW, Macfarlane S, Macfarlane GT. 2011. Adherence and cytokine induction in Caco-2 cells by bacterial populations from a three-stage continuous-culture model of the large intestine. Appl. Environ. Microbiol. 77:2934-42
5. BallykM, Dung L, Jones DA. 1998. Effects of random motility on microbial growth and competition in a flow reactor. SIAM J. Appl. Math. 59:573-96
6. Ballyk M, Smith H. 1999. A model of microbial growth in a plug flow reactor with wall attachment. Math. Biosci. 158:95-126
7. Ballyk MM, Smith H. 2001. Microbial competition in reactors with wall attachment: a mathematical comparison of chemostat and plug flow models. Microb. Ecol. 41:210-21
8. Barry J-L, Hoebler C,MacfarlaneGT, Macfarlane S,Mathers JC, et al. 1995. Estimation of the fermentability of dietary fibre in vitro: a European interlaboratory study. Br. J. Nutr. 74:303-22
9. Bartosch S, Woodmansey EJ, Paterson JCM, McMurdoMET,Macfarlane GT. 2005. Microbiological effects of consuming a synbiotic containing Bifidobacterium bifidum, Bifidobacterium lactis and oligofructose in elderly persons, determined by real-time polymerase chain reaction and counting of viable bacteria. Clin. Infect. Dis. 40:28-37
10. Beards E, Tuohy K,GibsonG. 2010. Bacterial, SCFA and gas profiles of a range of food ingredients following in vitro fermentation by human colonic microbiota. Anaerobe 16:420-25
11. Berends BR, Urlings HA, Snijders JM, van Knapen F. 1996. Identification and quantification of risk factors in animal management and transport regarding Salmonella spp. in pigs. Int. J. Food Microbiol. 30:37-53
12. Berner AZ, Fuentes S, Dostal A, Payne AN, Gutierrez PV, et al. 2013. Novel Polyfermentor IntestinalModel (PolyFermS) for controlled ecological studies: validation and effect of pH. PLoS ONE 8:e77772
13. Bernhardt H,Wellmer A, Zimmermann K, Knoke M. 1995. Growth of Candida albicans in normal and altered faecal flora in the model of continuous flow culture. Mycoses 38:265-70
14. Bielecka M, Biedrzycka E, Majkowska A. 2002. Selection of probiotics and prebiotics for synbiotics and confirmation of their in vivo effectiveness. Food Res. Int. 35:125-31
15. Björklund M, Ouwehand AC, Forssten SD, Nikkilä J, Tiihonen K, et al. 2012. Gut microbiota of healthy elderly NSAID users is selectively modified with the administration of Lactobacillus acidophilus NCFM and lactitol. Age 34:987-99
16. BouhnikY, Flourie B, Andrieux C, Bisetti N, Briet F,Rambaud JC. 1996. Effects of Bifidobacterium sp fermented milk ingested with or without inulin on colonic bifidobacteria and enzymatic activities in healthy humans. Eur. J. Clin. Nutr. 50:269-73
17. Boureau H, Hartmann L, Karjalainen T, Rowland I, Wilkinson MHF. 2000. Models to study colonisation and colonisation resistance. Microb. Ecol. Health D 2:247-58
18. Burr DH, Sugiyama H, Harvis G. 1982. Susceptibility to enteric botulinum colonization of antibiotic treated adult mice. Infect. Immun. 36:103-6
19. Cinquin C, Le Blay G, Fliss I, Lacroix C. 2004. Immobilization of infant fecal microbiota and utilization in an in vitro colonic fermentation model. Microb. Ecol. 48:128-38
20. Cinquin C, Le Blay G, Fliss I, Lacroix C. 2006. New three-stage in vitro model for infant colonic fermentation with immobilized fecal microbiota. FEMS Microbial. Ecol. 57:324-36
21. ColemanME, Dreesen DW,Wiegert RG. 1996. A simulation of microbial competition in the human colonic ecosystem. Appl. Environ. Microbiol. 62:3632-39
22. Cummings JH, Macfarlane GT. 1991. The control and consequences of bacterial fermentation in the human colon. J. Appl. Bacteriol. 70:443-59
23. de Graaf AA, Maathuis A, de Waard P, Deutz NEP, Dijkema C, et al. 2010. Profiling human gut bacterial metabolism and its kinetics using [U-13C]glucose and NMR. NMR Biomed. 23:2-12
24. de Graaf AA, Venema K. 2008. Gaining insight into microbial physiology in the large intestine: a special role for stable isotopes. Adv. Microb. Physiol. 53:73-168
25. de Jong P, Vissers MMM, van der Meer R, Bovee-Oudenhoven IMJ. 2007. In silico model as a tool for interpretation of intestinal infection studies. Appl. Environ. Microbiol. 73:508-15
26. Franks AH, Harmsen HJM, Raangs GC, Jansen GJ, Schut F, Welling GW. 1998. Variations of bacteria populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNAtargeted oligonucleotide probes. Environ. Microbiol. 64:3336-45
27. Freter R. 1983. Mechanisms that control the microflora in the large intestine. In Human Intestinal Microflora in Health and Disease, ed. D Hentges, pp. 33-54. New York: Academic
28. Gabridge MG. 1974. Parabiotic chamber for organ cultures: improved model. Appl. Microbiol. 28:774-77
29. Gerritsen J, Smidt H, Rijkers GT, de Vos WM. 2011. Intestinal microbiota in human health and disease: the impact of probiotics. Genes Nutr. 6:209-40
30. GibbonsDL, Spencer J. 2011. Mouse and human intestinal immunity: same ballpark, different players; different rules, same score. Mucosal Immunol. 4:148-57
31. Gibson GR, Cummings JH, Macfarlane GT. 1988. Use of a three-stage continuous culture system to study the effect ofmucin on dissimilatory sulfate reduction andmethanogenesis bymixed populations of human gut bacteria. Appl. Environ. Microbiol. 54:2750-55
32. Gietl E, Mengerink W, de Slegte J, Gibson G, Rastall R, van den Heuvel E. 2012. Factors involved in the in vitro fermentability of short carbohydrates in static faecal batch cultures. Int. J. Carbohydr. Chem. 2012:197809
33. Gill SR, Pop M, DeBoy RT, Eckberg PB, Turnbaugh PJ, et al. 2006. Metagenomic analysis of the human distal gut microbiome. Science 312:1355-59
34. Gmeiner M, KneifelW, Kulbe KD,Wouters R, De Boever P, Nollet L, et al. 2000. Influence of a synbiotic mixture consisting of Lactobacillus acidophilus 74-2 and a fructooligosaccharide preparation on themicrobial ecology sustained in a simulation of the human intestinal microbial ecosystem (SHIME reactor). Appl. Microbiol. Biotechnol. 53:219-23
35. Gorbach SL, Barza M, Giulaiano M, Jacobus NV. 1988. Colonization resistance of the human intestinal microflora: testing the hypothesis in normal volunteers. Eur. J. Clin. Microbiol. Infect. Dis. 7:98-102
36. Grant AJ, Woodward J, Maskell DJ. 2006. Development of an ex vivo organ culture model using human gastro-intestinal tissue and Campylobacter jejuni. FEMS Microbiol. Lett. 263:240-43
37. Grootaert C, Van den Abbeele P,Marzorati M, BroekaertWF, Courtin CM, et al. 2009. Comparison of prebiotic effects of arabinoxylan oligosaccharides and inulin in a simulator of the human intestinal microbial ecosystem. FEMS Microbiol. Ecol. 69:231-42
38. Gumienna M, Lasik M, Czarnecki Z. 2011. Bioconversion of grape and chokeberry wine polyphenols during simulated gastrointestinal in vitro digestion. Int. J. Food Sci. Nutr. 62:226-33
39. Hansen SR, Hubbell SP. 1980. Single-nutrient microbial competition: qualitative agreement between experimental and theoretically forecast outcomes. Science 207:1491-93
40. Hatanaka M, Nakamura Y, Maathuis AJH, Venema K, Murota I, Yamamoto N. 2012. Influence of Bacillus subtilis C-3102 on microbiota in a dynamic in vitro model of the gastrointestinal tract simulating human conditions. Benef. Microbes 3:229-36
41. Hazenberg MP, Bakker M, Verschoor-Burggraaf A. 1981. Effects of the human intestinal flora on germ-free mice. J. Appl. Bacteriol. 50:95-106
42. Hicks S, Candy DCA, Phillips AD. 1996. Adhesion of enteroaggressive Escherichia coli to pediatric intestinal mucosa in vitro. Infect. Immun. 64:4751-60
43. HobdenMR, Martin-Morales A, Gúerin-Deremaux L,Wils D, Costabile A, et al. 2013. In vitro fermentation of NUTRIOSE R FB06, a wheat dextrin soluble fibre, in a continuous culture human colonic model system. PLoS ONE 8:e77128
44. HolzapfelWH, Haberer P, Snel J, SchilingerU,Huis in't Veld JHJ. 1998. Overview of gut flora and probiotics. Int. J. Food Microbiol. 41:85-101
45. Jones DA, Le D, Smith H, Kojouharov HV. 2002. Bacterial wall attachment in a flow reactor. SIAM J. Appl. Math. 62:1728-71
46. Jones DA, Smith H. 2000. Microbial competition for nutrient and wall sites in plug flow. SIAM J. Appl.Math. 60:1576-600
47. Kamada N, Seo S-U, Chen GY, Nú ñez G. 2013. Role of the gut microbiota in immunity and inflammatory disease. Nat. Rev. Immunol. 13:321-35
48. Kim HJ, Huh D, Hamilton G, Ingber DE. 2012. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab. Chip 12:1265-74
49. Kim HJ, Ingber DE. 2013. Gut-on-a-chip microenvironment induces human intestinal cells to undergo villus differentiation. Integr. Biol. 5:1130-40
50. Klinger A, Orzekowsky-Schroeder R, von Smolinski D, Blessenohl M, Schueth A. 2012. Complex morphology and functional dynamics of vital murine intestinal mucosa revealed by autofluorescence 2-photon microscopy. Histochem. Cell Biol. 137:269-78
51. Kontula P, Jaskari J, Nollet L, De Smet I, von Wright A. 1998. The colonization of a simulator of the human intestinal microbial ecosystem by a probiotic strain fed on a fermented oat bran product: effects on the gastrointestinal microbiota. Appl. Microbiol. Biotechnol. 50:246-52
52. Kovatcheva-Datchary P, Egert M, Maathuis A, Rajilíc-Stojanovíc M, de Graaf AA, et al. 2009. Linking phylogenetic identities of bacteria to starch fermentation in an in vitro model of the large intestine by RNA-based stable isotope probing. Environ. Microbiol. 11:914-26
53. Laird BD, Van de WieleTR, CorriveauMC, Jamieson HE, Parsons MB, et al. 2007. Gastrointestinal microbes increase arsenic bioaccessibility of ingested mine tailings using the simulator of the human intestinal microbial ecosystem. Environ. Sci. Technol. 41:5542-47
54. Lawson DJ, Holtrop G, Flint H. 2011. Bayesian analysis of non-linear differential equation models with application to a gut microbial ecosystem. Biom. J. 53:543-56
55. LesmesU, BeardsEJ, Gibson GR,TuohyKM, Shimoni E. 2008. Effects of resistant starch type III polymorphs on human colon microbiota and short chain fatty acids in human gut models. J. Agric. Food Chem. 56:5415-21
56. Likotrafiti E, Tuohy KM, Gibson GR, Rastall RA. 2014. An in vitro study of the effect of probiotics, prebiotics and synbiotics on the elderly faecal microbiota. Anaerobe 27:50-55
57. Maathuis AJH,KellerD, Farmer S. 2010. Survival andmetabolic activity of the GanedenBC30 strain of Bacillus coagulans in a dynamic in vitro model of the stomach and small intestine. Benef. Microbes 1:31-36
58. Maathuis AJH, van den Heuvel EG, Schoterman MHC, Venema K. 2012. Galacto-oligosaccharides have prebiotic activity in a dynamic in vitro colon model using a 13C-labelling technique. J. Nutr. 142:1205-12
59. Maccaferri S, Vitali B, Klinder A, Kolida S, Ndagijimana M, et al. 2010. Rifaximin modulates the colonic microbiota of patients with Crohn's disease: an in vitro approach using a continuous culture colonic model system. J. Antimicrob. Chemother. 65:2556-65
60. Macfarlane GT, Gibson GR, Cummings JH. 1992. Comparison of fermentation reactions in different regions of the human colon. J. Appl. Bacteriol. 72:57-64
61. Macfarlane GT, Macfarlane S, Gibson GR. 1998. 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. 35:180-87
62. Macfarlane GT, Macfarlane S. 2007. Models for intestinal fermentation: association between food components, delivery systems, bioavailability and functional interactions in the gut. Curr. Opin. Biotech. 18:156-62
63. Macfarlane S,WoodmanseyEJ, MacfarlaneGT. 2005. Colonization ofmucin by human intestinal bacteria and establishment of biofilm communities in a two-stage continuous culture system. Appl. Environ. Microbiol. 71:7483-92
64. Maia OB, Duarte R, Silva AM, Cara DC, Nicoli JR. 2001. Evaluation of the components of a commercial probiotic in gnotobiotic mice experimentally challenged with Salmonella enterica subsp. enterica ser. Typhimurium. Vet. Microbiol. 79:183-89
65. Mäkeläinen H, Mäkivuokko H, Salminen S, Rautonen N, Ouwehand AC. 2007. The effects of polydextrose and xylitol on microbial community and activity in a 4-stage colon simulator. J. Food Sci. 72:153-59
66. Mäkeläinen H, Forssten S, Saarinen M, Stowell J, Rautonen N, Ouwehand AC. 2009. Xylo-oligosaccharides enhance the growth of bifidobacteria and B. lactis in a simulated colon model. Benef. Microbes 1:81-91
67. Mäkivuokko H, Saarinen M, Ouwehand A, Rautonen N. 2006. Effects of lactose on colon microbial community structure and function in a four-stage continuous culture system. Biosci. Biotechnol. Biochem. 70:2056-63
68. Mäkivuokko H, Nurmi J, Nurminen P, Stowell J, Rautonen N. 2005. In vitro effects on polydextrose by colonic bacteria and caco-2 cell cyclooxygenase gene expression. Nutr. Cancer 52:94-104
69. Malinen E, Mätt ö J, Salmitie M, Alander M, Saarela M, Palva A. 2002. PCR-ELISA II: analysis of bifidobacterium populations in human faecal samples from a consumption trial with Bifidobacterium lactis Bb-12 and a galacto-oligosaccharide preparation. Syst. Appl. Microbiol. 25:249-58
70. Marteau P, Minekus M, Havenaar R, Huis In't Veld JHJ. 1997. Survival of lactic acid bacteria in a dynamic model of the stomach and small intestine: validation and the effects of bile. J. Dairy Sci. 80:1031-37
71. Marteau P, Pochart P, Doré J, Béra-Maillet C, Vernalier A, Corthier G. 2001. Comparative study of bacterial groups within the human cecal and fecal microbiota. Appl. Environ. Microbiol. 67:4929-42
72. Martinez RCR, Aynaou A-E, Albrecht S, Schols HA, DeMartinis ECP. 2011. In vitro evaluation of gastrointestinal survival of Lactobacillus amylovorus DSM 16698 alone and combined with galactooligoaccharides, milk and/or Bifidobacterium animalis subsp. lactis Bb-12. Int. J. Food Microbiol. 149:152-58
73. Marzorati M, Possemiers S, Van Den Abbeele P, Van De Wiele B, Vanhoecke B, Verstraete W. 2010. Technology and method to study microbial growth and adhesion to host-related surface and the hostmicrobiota interactions. WO Patent 2010/118857 A2, Ghent Univ. Belgium
74. Marzorati M, Vanhoecke B, Ryck TD, Sadabad MS, Pinheiro I. 2014. The HIMTM module: a new tool to study the host-microbiota interaction in the human gastrointestinal tract in vitro. BMC Microbiol. 14:133
75. Mestas J, Hughes CCW. 2004. Of mice and not men: differences between mouse and human immunology. J. Immunol. 172:2731-38
76. Miller TL, Wolin MJ. 1981. Fermentation by the human large intestine microbial community in an in vitro semicontinuous culture system. Appl. Environ. Microbiol. 42:400-7
77. Minekus M, Marteau P, Havenaar R, Huis In't Veld JHJ. 1995. A multicompartmental dynamic computercontrolled model simulating the stomach and small intestine. Altern. Lab Anim. 23:197-209
78. MinekusM, Smeets-PeetersM, Bernalier A,Marol-Bonnin S,Havenaar R, et al. 1999. A computer-controlled system to simulate conditions of the large intestine with peristaltic mixing, water absorption and absorption of fermentation products. Appl. Microbiol. Biotechnol. 53:108-14
79. Molly K, Woestyne MV, Verstraete W. 1993. Development of 5-step multichamber reactor as a simulation of the human intestinal microbial ecosystem. Appl. Microbiol. Biotechnol. 39:254-58
80. Muñoz-Tamayo R, Laroche B,Walter É, Doré J, Leclerc M. 2010. Mathematical modelling of carbohydrate degradation by human colonic microbiota. J. Theor. Biol. 266:189-201
81. Muñ oz-Tamayo R, Laroche B, Walter É , Doré J, Duncan SH, et al. 2011. Kinetic modelling of lactate utilization and butyrate production by key human colonic bacterial species. FEMS Microbiol. Ecol. 76:615-24
82. Mysore JV, Duhamel GE. 1994. Morphometric analysis of enteric lesions in C3H/HeN mice inoculated with Serpulina hyodysentericae serotypes 2 and 4 with or without oral streptomycin pretreatment. Can. J. Vet. Res. 58:281-86
83. Naylor TA, Connolly PC, Martini LG, Elder DP, Minekus M, et al. 2006. Use of a gastrointestinal model and GastroPLUSTM for the prediction of in vivo performance. Ind. Pharm. 12:9-12
84. Nielsen EM, Schlundt J. 1992. Use of norfloxacin to study colonization ability of Escherichia coli in in vivo and in vitro models of the porcine gut. Antimicrob. Agents Chemother. 36:401-7
85. NilssonU,Nyman M. 2007. Carboxylic acids in the hindgut of rats fed highly soluble inulin and Bifidobacterium lactis (Bb-12), Lactobacillus salivarius (UCC500) or Lactobacillus rhamnosus (GG). Scan. J. Food Nutr. 51:13-21
86. Oufir LE, Barry JL, Flouríe B, Cherbut C, Cloarec D, et al. 2000. Relationships between transit time in man and in vitro fermentation of dietary fiber by fecal bacteria. Eur. J. Clin. Nutr. 54:603-9
87. Ouwehand AC,Kirijavainen PV,Grönlund M-M, Isolauri E, Salminen SJ. 1999. Adhesion of probiotic microorganisms to intestinal mucus. Int. Dairy J. 9:623-30
88. Ouwehand AC, Suomalainen T, Tölkko S, Salminen S. 2002. In vitro adhesion of propionic acid bacteria to human intestinal mucus. Le Lait 82:123-30
89. Payne AN, Zihler A, Chassard C, Lacroix C. 2012. Advances and perspectives in in vitro human gut fermentation modelling. Trends Biotechnol. 30:17-25
90. Pazzaglia G, Winoto I, Jennings G. 1994. Oral challenge with Aeromonas in protein-malnourished mice. J. Diarrhoeal Dis. Res. 12:108-12
91. Petrof EO, Gloor GB, Vanner SJ, Weese SJ, Carter D, et al. 2013. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: "RePOOPulating" the gut. Microbiome 1:3
92. Phillips ML. 2009. Gut reaction: environmental effects on the human microbiota. Environ. Health Perspect. 117:198-205
93. Pinto M, Robine-Leon S, Appay MD, Kendinger M, Triadou N, et al. 1983. Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol. Cell 47:323-30
94. Pirt SH. 1974. The theory of fed batch culture with reference to the penicillin fermentation. J. Appl. Chem. Biotechnol. 24:415-24
95. Pompei A, Cordisco L, Raimondi S, Amaretti A, PagnoniUM, et al. 2008. In vitro comparison of the prebiotic effects of two inulin-type fructans. Anaerobe 14:280-86
96. Possemiers S, Bolca S, Grootaert C, Heyerick A, Decroos K. 2006. The prenylflavonoid isoxanthohumol from hops (Humulus lupulus L.) is activated into the potent phytoestrogen 8-prenylnaringenin in vitro and in the human intestine. J. Nutr. 136:1862-67
97. Probert HM, Gibson GR. 2004. Development of a fermentation system to model sessile bacterial populations in the human colon. Biofilms 1:13-19
98. Qin J, Ruigiang L, Raes J, Arumugam M, Solvsten B, et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59-65
99. Quigley EM. 2010. Prebiotics and probiotics;modifying andmining the microbiota. Pharmacol. Res. 61:213-18
100. Quigley ME, Englyst HN. 1992. Determination of neutral sugars and hexosamines by high-performance liquid chromatography with pulsed amperometric detection. Analyst 117:1715-18
101. Raibaud P, Ducluzeau R, Dubos F, Hudault S, Bewa H, Muller MC. 1980. Implantation of bacteria from the digestive tract of man and various animals into gnotobiotic mice. Am. J. Clin. Nutr. 33:2440-47
102. Rajilíc-Stojanovíc M, Heilig HGHJ, Molenaar D, Kajander K, Surakka A, et al. 2009. Development and application of the human intestinal tract chip, a phylogeneticmicroarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ. Microbiol. 11:1736-51
103. Rajilíc-Stojanovíc M, Maathuis A, Heilig HGHJ, Venema K, de Vos WM, Smidt H. 2010. Evaluating the microbial diversity of an in vitro model of the human large intestine by phylogenetic microarray analysis. Microbiology 156:3270-81
104. Reis PM, Raab TW, Chuat JY, LeserME, Miller R, et al. 2008. Influence of surfactants on lipase fat digestion in a model gastro-intestinal system. Food Biophys. 3:370-81
105. Rinttilä T, Kassinen A,Malinen E, Krogius L, Palva A. 2004. Development of an extensive set of 16S rDNAtargeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J. Appl. Microbiol. 97:1166-77
106. Rufener WH Jr, Nelson WO, Wolin MJ. 1963. Maintenance of the rumen microbial population. Appl. Microbiol. 11:196-201
107. Rumney CJ, Rowland IR. 1992. In vivo and in vitro models of the human colonic flora. Crit. Rev. Food Sci. Nutr. 31:299-331
108. Salminen S, Bouley C, Boutron-Ruault MC, Cummings JH, Franck A, et al. 1998. Functional food science and gastrointestinal physiology and function. Br. J. Nutr. 80:S147-71
109. Sannasiddappa TH, Costabile A, Gibson GR, Clarke SR. 2011. The influence of Staphylococcus aureus on gut microbial ecology in an in vitro continuous culture human colonic model system. PLoS ONE 6:e23227
110. Satokari RM, Vaughan EE, Akkermans ADL, Saarela M, de Vos W. 2001. Bifidobacterial diversity in human feces detected by genus-specific PCRand denaturing gradient gel electrophoresis. Appl. Environ.Microbiol. 67:504-13
111. Saulnier DMA, Gibson GR, Kolida S. 2008. In vitro effects of selected synbiotics on the human faecal microbiota composition. FEMS Microbiol. Ecol. 66:516-27
112. Sekirov I, Russell SL, Antunes CM, Finlay BB. 2010. Gut microbiota in health and disease. Physiol. Rev. 90:859-904
113. Slyter LL, Nelson WO,Wolin MJ. 1964. Modifications of a device for maintenance of the rumen microbial population in continuous culture. Appl. Microbiol. 12:374-77
114. Stemmons ED, Smith H. 2000. Competition in a chemostat with wall attachment. SIAM J. Appl. Math. 61:567-95
115. Temmerman R, Swings J. 2004. Identification of lactic acid bacteria: culture-dependent and cultureindependent methods. Trends Food Sci. Tech. 15:348-59
116. Tlaskalová-Hogenová H, Stepánková R, Kozákova H, Hudcovic T, Vannucci L, et al. 2011. The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell. Mol. Immun. 8:100-20
117. Tremoleda JL, Kerton A, Gsell W. 2012. Anaesthesia and physiology monitoring during in vivo imaging of laboratory rodents: considerations on experimental outcomes and animal welfare. EJNMMI Res. 2:44
118. Tsilingiri K, Barbosa T, Penna G, Caprioli F, Sonzogni A, et al. 2012. Probiotic and postbiotic activity in health and disease: comparison on a novel polarised ex-vivo organ culture model. Gut 61:1007-15
119. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. 2009. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 1:6ra14
120. Van de Wiele T, Boeckaert C, Verstraete W, Siciliano S. 2003. Oral exposure PAH: bioactivation processes in the human gut. Commun. Agric. Appl. Biol. Sci. 68:3-6
121. Van de Wiele T, Boon N, Possemiers S, Jacobs H, Verstraete W. 2004. Prebiotic effects of chicory inulin in the simulator of the human intestinal microbial ecosystem. FEMS Microbio. Ecol. 51:143-53
122. Van de Wiele T, Boon N, Possemiers S, Jacobs H, Verstraete W. 2007. Inulin-type fructans of longer degree of polymerization exert more pronounced in vitro prebiotic effects. J. Appl. Microbiol. 102:452-60
123. Van den Abbeele P, Grootaert C, Possemiers S, VerstraeteW, Verbeken K, Van de Wiele T. 2009. In vitro model to study the modulation of the mucin-adhered bacterial community. Appl. Microbiol. Biotechnol. 83:349-59
124. Van den Abbeele P,Grootaert C, MarzoratiM, Possemiers S, VerstraeteW, et al. 2010. Microbial community development in a dynamic gut model is reproducible, colon region specific, and selective for Bacteroidetes and Clostridium Cluster IX. Appl. Environ. Microbiol. 76:5237-46
125. Van denAbbeele P,Gérard P,Rabot S, BruneauA,ElAidy S, et al. 2011. Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats. Environ. Microbiol. 13:2667-80
126. Van den Abbeele P, Roos S, Eeckhaut V, MacKenzie DA, Derde M, et al. 2012. Incorporating a mucosal environment in a dynamic gut model results in a more representative colonization by lactobacilli. Microb. Biotechnol. 5:106-15
127. Van den Abbeele P,VenemaK, Van de WieleT,VerstraeteW, Possemiers S. 2013. Different human gut models reveal the distinct fermentation patterns of arabinoxylan versus inulin. J. Agric. Food Chem. 61:9819-27
128. Van der Waaij D, Van der Waaij BD. 1990. The colonization resistance of the digestive tract in different animal species and in man; a comparative study. Epidemiol. Infect. 105:237-43
129. Venema K, Maathuis AJH, Steijart MN, de Graaf AA. 2012. Use of 13C-labelled carbohydrates to trace microbial metabolism in the colon; light in the tunnel! FASEB J. 26:638.1
130. Vermeiren J, Possemiers S, Marzorati M, Van de Wiele T. 2011. The gut microbiota as target for innovative drug development: perspectives and a case study of inflammatory bowel disease. In Drug Development-A Case Study Based Insight into Modern Strategies, ed. C Rundfeldt, pp. 1-33. Ghent, Belg.: InTech
131. Wang X, Gibson GR. 1993. Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J. Appl. Bacteriol. 75:373-80
132. Weigert R, Porat-ShliomN, Amomphimoltham P. 2013. Imaging cell biology in live animals: ready for prime time. J. Cell Biol. 201:969-79
133. Wieser A, Guggenberfer C, Pritsch M, Heesemann J, Schubert S. 2011. A novel ex vivo set-up for dynamic long-term characterization of processes on mucosal interfaces by confocal imaging and simultaneous cytokine measurements. Cell Microbiol. 13:742-51
134. Wilkinson MHF. 2002a. Model intestinal microflora in computer simulation (MIMICS). MIMICS Tech. Rep. MIMICS Cellular Automation Program Design and Performance Testing, University of Groningen, The Netherlands. http://www.cs.rug.nl/michael/techrep1.pdf
135. Wilkinson MHF. 2002b. Model intestinal microflora in computer simulation (MIMICS). MIMICS Tech. Rep. Ordinary Differential Equations for ModellingBacterial Interactions in theGut,University of Groningen, The Netherlands. http://www.cs.rug.nl/michael/techrep2.pdf
136. Wilkinson MHF. 2002c. Model intestinal microflora in computer simulation: a simulation and modeling package for host-microflora interactions. IEEE Trans. Biomed. Eng. 49:1077-85
137. Xu J, Gordon JI. 2003. Inaugural article: honor thy symbionts. Proc. Natl. Acad. Sci. USA 100:10452-59
138. Zoetendal EG, Akkermans ADL, de Vos WM. 1998. Communities of active bacteria samples reveals stable and host-specific analysis of 16S rRNA from Human fecal temperature gradient gel electrophoresis. Appl. Environ. Microbiol. 64:3854-59