In vitro Gastrointestinal Models for Prebiotic Carbohydrates: A Critical Review

Author(s): Oswaldo Hernandez-Hernandez*

Journal Name: Current Pharmaceutical Design

Volume 25 , Issue 32 , 2019


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Abstract:

Background: In the last decade, various consortia and companies have created standardized digestion protocols and gastrointestinal simulators, such as the protocol proposed by the INFOGEST Consortium, the simulator SHIME, the simulator simgi®, the TIM, etc. Most of them claim to simulate the entire human gastrointestinal tract. However, few results have been reported on the use of these systems with potential prebiotic carbohydrates.

Methods: This critical review addresses the existing data on the analysis of prebiotic carbohydrates by different in vitro gastrointestinal simulators, the lack of parameters that could affect the results, and recommendations for their enhancement.

Results: According to the reviewed data, there is a lack of a realistic approximation of the small intestinal conditions, mainly because of the absence of hydrolytic conditions, such as the presence of small intestinal brush border carbohydrases that can affect the digestibility of different carbohydrates, including prebiotics.

Conclusion: There is a necessity to standardize and enhance the small intestine simulators to study the in vitro digestibility of carbohydrates.

Keywords: Digestibility, lactase, maltase-glucoamylase, small intestine, sucrase-isomaltase, trehalase.

[1]
Gibson GR, Hutkins R, Sanders ME, 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 2017; 14(8): 491-502.
[http://dx.doi.org/10.1038/nrgastro.2017.75] [PMID: 28611480]
[2]
Leemhuis H, Dobruchowska JM, Ebbelaar M, et al. Isomalto/malto-polysaccharide, a novel soluble dietary fiber made via enzymatic conversion of starch. J Agric Food Chem 2014; 62(49): 12034-44.
[http://dx.doi.org/10.1021/jf503970a] [PMID: 25412115]
[3]
Khodaei N, Fernandez B, Fliss I, Karboune S. Digestibility and prebiotic properties of potato rhamnogalacturonan I polysaccharide and its galactose-rich oligosaccharides/oligomers. Carbohydr Polym 2016; 136: 1074-84.
[http://dx.doi.org/10.1016/j.carbpol.2015.09.106] [PMID: 26572449]
[4]
Ferreira-Lazarte A, Gallego-Lobillo P, Moreno FJ, Villamiel M, Hernandez-Hernandez O. In vitro digestibility of galactooligosaccharides: Effect of the structural features on their intestinal degradation. J Agric Food Chem 2019; 67(16): 4662-70.
[http://dx.doi.org/10.1021/acs.jafc.9b00417] [PMID: 30986057]
[5]
So D, Whelan K, Rossi M, et al. Dietary fiber intervention on gut microbiota composition in healthy adults: A systematic review and meta-analysis. Am J Clin Nutr 2018; 107(6): 965-83.
[http://dx.doi.org/10.1093/ajcn/nqy041] [PMID: 29757343]
[6]
Hernandez-Hernandez O, Moreno FJ, Kolida S, Rastall RA, Sanz ML. Effect of glycation of bovine β-lactoglobulin with galactooligosaccharides on the growth of human faecal bacteria. Int Dairy J 2011; 21(12): 949-52.
[http://dx.doi.org/10.1016/j.idairyj.2011.06.002]
[7]
Hernández-Hernández O, Marín-Manzano MC, Rubio LA, Moreno FJ, Sanz ML, Clemente A. Monomer and linkage type of galacto-oligosaccharides affect their resistance to ileal digestion and prebiotic properties in rats. J Nutr 2012; 142(7): 1232-9.
[http://dx.doi.org/10.3945/jn.111.155762] [PMID: 22649257]
[8]
Marín-Manzano MC, Abecia L, Hernández-Hernández O, et al. Galacto-oligosaccharides derived from lactulose exert a selective stimulation on the growth of Bifidobacterium animalis in the large intestine of growing rats. J Agric Food Chem 2013; 61(31): 7560-7.
[http://dx.doi.org/10.1021/jf402218z] [PMID: 23855738]
[9]
Alegría A, Garcia-llatas G, Cilla A. In vitro intestinal tissue models: General introduction Impact Food Bioact Heal Vitr Ex Vivo. Model 2015; pp. 239-44.
[10]
Brodkorb A, Egger L, Alminger M, et al. INFOGEST static in vitro simulation of gastrointestinal food digestion. Nat Protoc 2019; 14(4): 991-1014.
[http://dx.doi.org/10.1038/s41596-018-0119-1] [PMID: 30886367]
[11]
Shin H, Seo DH, Seo J, Lamothe LM, Yoo SH, Lee BH. Optimization of in vitro carbohydrate digestion by mammalian mucosal α-glucosidases and its applications to hydrolyze the various sources of starches. Food Hydrocoll 2019; 87: 470-6.
[http://dx.doi.org/10.1016/j.foodhyd.2018.08.033]
[12]
Ferreira-Lazarte A, Montilla A, Mulet-Cabero AI, et al. Study on the digestion of milk with prebiotic carbohydrates in a simulated gastrointestinal model. J Funct Foods 2017; 33: 149-54.
[http://dx.doi.org/10.1016/j.jff.2017.03.031]
[13]
Ferreira-Lazarte A, Olano A, Villamiel M, Moreno FJ. Assessment of in vitro digestibility of dietary carbohydrates using rat small intestinal extract. J Agric Food Chem 2017; 65(36): 8046-53.
[http://dx.doi.org/10.1021/acs.jafc.7b01809] [PMID: 28793770]
[14]
Nobre C, do Nascimento AKC, Silva SP, et al. Process development for the production of prebiotic fructo-oligosaccharides by Penicillium citreonigrum. Bioresour Technol 2019; 282: 464-74.
[http://dx.doi.org/10.1016/j.biortech.2019.03.053] [PMID: 30897484]
[15]
Nobre C, Sousa SC, Silva SP, et al. In vitro digestibility and fermentability of fructo-oligosaccharides produced by Aspergillus ibericus. J Funct Foods 2018; 46: 278-87.
[http://dx.doi.org/10.1016/j.jff.2018.05.004]
[16]
Yang Y, Zhao C, Diao M, et al. The prebiotic activity of simulated gastric and intestinal digesta of polysaccharides from the Hericium erinaceus. Molecules 2018; 23(12): 3158.
[http://dx.doi.org/10.3390/molecules23123158] [PMID: 30513668]
[17]
Sivieri K, Morales MLV, Saad SMI, Adorno MAT, Sakamoto IK, Rossi EA. Prebiotic effect of fructooligosaccharide in the simulator of the human intestinal microbial ecosystem (SHIME® model). J Med Food 2014; 17(8): 894-901.
[http://dx.doi.org/10.1089/jmf.2013.0092] [PMID: 24654949]
[18]
Shi Y, Liu J, Yan Q, You X, Yang S, Jiang Z. In vitro digestibility and prebiotic potential of curdlan (1→3)-β-d-glucan oligosaccharides in Lactobacillus species. Carbohydr Polym 2018; 188: 17-26.
[http://dx.doi.org/10.1016/j.carbpol.2018.01.085] [PMID: 29525154]
[19]
Hu Y, Winter V, Chen XY, Gänzle MG. Effect of acceptor carbohydrates on oligosaccharide and polysaccharide synthesis by dextransucrase DsrM from Weissella cibaria. Food Res Int 2017; 99(Pt 1): 603-11.
[http://dx.doi.org/10.1016/j.foodres.2017.06.026] [PMID: 28784523]
[20]
Moon JS, Joo W, Ling L, Choi HS, Han NS. In vitro digestion and fermentation of sialyllactoses by infant gut microflora. J Funct Foods 2016; 21: 497-506.
[http://dx.doi.org/10.1016/j.jff.2015.12.002]
[21]
Ferreira-Lazarte A, Moreno FJ, Cueva C, Gil-Sánchez I, Villamiel M. Behaviour of citrus pectin during its gastrointestinal digestion and fermentation in a dynamic simulator (simgi®). Carbohydr Polym 2019; 207: 382-90.
[http://dx.doi.org/10.1016/j.carbpol.2018.11.088] [PMID: 30600020]
[22]
Pham VT, Mohajeri MH. The application of in vitro human intestinal models on the screening and development of pre- and probiotics. Benef Microbes 2018; 9(5): 725-42.
[http://dx.doi.org/10.3920/BM2017.0164] [PMID: 29695182]
[23]
Raoult D. The study of microbiota needs both microbiologists and medical doctors. Clin Microbiol Infect 2017; 23(8): 500-1.
[http://dx.doi.org/10.1016/j.cmi.2017.03.002] [PMID: 28285978]
[24]
Donaldson GP, Lee SM, Mazmanian SK. Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 2016; 14(1): 20-32.
[http://dx.doi.org/10.1038/nrmicro3552] [PMID: 26499895]
[25]
Thuenemann EC. In vitro intestinal tissue models: General introduction Impact Food Bioact Heal Vitr Ex Vivo. Model 2015; pp. 239-44.
[26]
Verhoeckx K, Cotter P, López-Expósito I, et al. The impact of food bioactives on health: In vitro and ex vivo models. 1st ed. Cham: Springer 2015.
[http://dx.doi.org/10.1007/978-3-319-16104-4]
[27]
Minekus M. The TNO Gastro-Intestinal Model (TIM). In: The Impact of Food Bioactives on Health: In Vitro and Ex Vivo Models In: 2015; pp. 239-44.
[28]
Van De Wiele T, Van Den Abbeele P, Ossieur W, et al. The simulator of the human intestinal microbial ecosystem (SHIME®). In: The Impact of Food Bioactives on Health: In Vitro and Ex Vivo Models In: 2015; pp. 239-44.
[29]
Gil-Sánchez I, Cueva C, Sanz-Buenhombre M, Guadarrama A, Moreno-Arribas MV, Bartolomé B. Dynamic gastrointestinal digestion of grape pomace extracts: Bioaccessible phenolic metabolites and impact on human gut microbiota. J Food Compos Anal 2018; 68: 41-52.
[http://dx.doi.org/10.1016/j.jfca.2017.05.005]
[30]
Bellmann S, Minekus M, Zeijdner E, Verwei M, Sanders P. TIM-Carbo: A rapid, cost-efficient and reliable in vitro method for glycemic response after carbohydrate ingestion. In: Dietary fibre: New frontiers for food and health van der Kamp J-W, Jones JM, McCleary BV (Eds); Wageningen Academic Publishers;. Wageningen, Netherlands;. 2010; pp. 467-73.
[31]
Julio-Gonzalez LC, Hernández-Hernández O, Moreno FJ, Olano A, Corzo N. High-yield purification of commercial lactulose syrup. Separ Purif Tech 2019; 224: 475-80.
[http://dx.doi.org/10.1016/j.seppur.2019.05.053]
[32]
Hooton D, Lentle R, Monro J, Wickham M, Simpson R. The secretion and action of brush border enzymes in the mammalian small intestine. Rev Physiol Biochem Pharmacol 2015; 168: 59-118.
[33]
Harlow E, Lane D. Preparing acetone powders CSH Protoc 2006; 2006(1)pii: pdb.prot4305..
[http://dx.doi.org/10.1101/pdb.prot4305] [PMID: 22485681]
[34]
Hernandez-Hernandez O, Olano A, Rastall RA, Moreno FJ. In vitro digestibility of dietary carbohydrates: Toward a standardized methodology beyond amylolytic and microbial enzymes. Front Nutr 2019; 6: 61.
[http://dx.doi.org/10.3389/fnut.2019.00061] [PMID: 31134206]
[35]
Pyner A, Nyambe-Silavwe H, Williamson G. Inhibition of human and rat sucrase and maltase activities to assess antiglycemic potential: Optimization of the assay using acarbose and polyphenols. J Agric Food Chem 2017; 65(39): 8643-51.
[http://dx.doi.org/10.1021/acs.jafc.7b03678] [PMID: 28914528]
[36]
Martínez-Maqueda D, Miralles B, Recio I. HT29 Cell Line Daniel. In: The impact of food bioactives on health: In vitro and ex vivo models . 2015; pp. 239-44.
[37]
Ozdal T, Sela DA, Xiao J, Boyacioglu D, Chen F, Capanoglu E. The reciprocal interactions between polyphenols and gut microbiota and effects on bioaccessibility. Nutr 2016; 8(2): 78.
[http://dx.doi.org/10.3390/nu8020078] [PMID: 26861391]
[38]
Cardona F, Andrés-Lacueva C, Tulipani S, Tinahones FJ, Queipo-Ortuño MI. Benefits of polyphenols on gut microbiota and implications in human health. J Nutr Biochem 2013; 24(8): 1415-22.
[http://dx.doi.org/10.1016/j.jnutbio.2013.05.001] [PMID: 23849454]
[39]
Costa JR, Amorim M, Vilas-Boas A, et al. Impact of in vitro gastrointestinal digestion on the chemical composition, bioactive properties, and cytotoxicity of Vitis vinifera L. cv. Syrah grape pomace extract. Food Funct 2019; 10(4): 1856-69.
[http://dx.doi.org/10.1039/C8FO02534G] [PMID: 30950465]
[40]
Gu Q, Duan G, Yu XYu. Bioconversion of flavonoid Glycosides from Hippophae rhamnoides leaves into flavonoid aglycones by Eurotium amstelodami. Microorganisms 2019; 7(5): 122.
[http://dx.doi.org/10.3390/microorganisms7050122] [PMID: 31060344]
[41]
Kalita D, Holm DG, LaBarbera DV, Petrash JM, Jayanty SS. Inhibition of α-glucosidase, α-amylase, and aldose reductase by potato polyphenolic compounds. PLoS One 2018; 13(1)e0191025
[http://dx.doi.org/10.1371/journal.pone.0191025] [PMID: 29370193]
[42]
Lavelli V, Sri Harsha PSC, Ferranti P, Scarafoni A, Iametti S. Grape skin phenolics as inhibitors of Mammalian α-glucosidase and α-amylase-effect of food matrix and processing on efficacy. Food Funct 2016; 7(3): 1655-63.
[http://dx.doi.org/10.1039/C6FO00073H] [PMID: 26943361]
[43]
Mosele JI, Macià A, Romero MP, Motilva MJ, Rubió L. Application of in vitro gastrointestinal digestion and colonic fermentation models to pomegranate products (juice, pulp and peel extract) to study the stability and catabolism of phenolic compounds. J Funct Foods 2015; 14: 529-40.
[http://dx.doi.org/10.1016/j.jff.2015.02.026]
[44]
Vollmer M, Esders S, Farquharson FM, et al. Mutual interaction of phenolic compounds and microbiota: Metabolism of complex phenolic apigenin-c- and kaempferol-o-derivatives by human fecal samples. J Agric Food Chem 2018; 66(2): 485-97.
[http://dx.doi.org/10.1021/acs.jafc.7b04842] [PMID: 29236499]
[45]
Németh K, Plumb GW, Berrin JG, et al. Deglycosylation by small intestinal epithelial cell β-glucosidases is a critical step in the absorption and metabolism of dietary flavonoid glycosides in humans. Eur J Nutr 2003; 42(1): 29-42.
[http://dx.doi.org/10.1007/s00394-003-0397-3] [PMID: 12594539]
[46]
Williamson G, Kay CD, Crozier A. The bioavailability, transport, and bioactivity of dietary flavonoids: A review from a historical perspective. Compr Rev Food Sci Food Saf 2018; 17(5): 1054-112.
[http://dx.doi.org/10.1111/1541-4337.12351]
[47]
Williamson G, Clifford MN. Role of the small intestine, colon and microbiota in determining the metabolic fate of polyphenols. Biochem Pharmacol 2017; 139: 24-39.
[http://dx.doi.org/10.1016/j.bcp.2017.03.012] [PMID: 28322745]
[48]
Villmones HC, Haug ES, Ulvestad E, et al. Species level description of the human ileal bacterial microbiota. Sci Rep 2018; 8(1): 4736.
[http://dx.doi.org/10.1038/s41598-018-23198-5] [PMID: 29549283]
[49]
Zoetendal EG, Raes J, van den Bogert B, et al. The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 2012; 6(7): 1415-26.
[http://dx.doi.org/10.1038/ismej.2011.212] [PMID: 22258098]


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Article Details

VOLUME: 25
ISSUE: 32
Year: 2019
Published on: 15 November, 2019
Page: [3478 - 3483]
Pages: 6
DOI: 10.2174/1381612825666191011094724
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