Advertisement

In vivo, In vitro, and In silico Studies of the GI Tract

  • Syahrizal Muttakin
  • Thomas E. Moxon
  • Ourania GousetiEmail author
Chapter

Abstract

This chapter is divided into three sections, each presenting a different type of methodologies that are commonly used to study the link between food digestion and health. The first section focuses on in vivo methods, which are those that involve a living organism. The main types of epidemiological study design are presented, including observational and intervention studies. The relatively new field of nutritional epidemiology is further introduced, while animal studies are also briefly considered. The second section concerns in vitro experiments, which simulate digestive processes outside the body. The principles and practicalities of different static and dynamic in vitro models encountered in the literature are presented. Further, in silico approaches to digestion studies are discussed in the third section, with emphasis on developing understanding of digestive processes using numerical and computer techniques, with the aim to produce predictive models.

Keywords

Food digestion In vivo Epidemiology Animal studies In vitro Static Dynamic In silico 

References

  1. Aguilera, J. M. (2005). Why food microstructure? Journal of Food Engineering, 67, 3–11.CrossRefGoogle Scholar
  2. Al-Gousous, J., & Langguth, P. (2015). Oral solid dosage form disintegration testing—The forgotten test. Journal of Pharmaceutical Sciences, 104, 2664–2675.PubMedCrossRefPubMedCentralGoogle Scholar
  3. An, J. S., Bae, I. Y., Han, S.-I., Lee, S.-J., & Lee, H. G. (2016). In vitro potential of phenolic phytochemicals from black rice on starch digestibility and rheological behaviors. Journal of Cereal Science, 70, 214–220.CrossRefGoogle Scholar
  4. Bach Knudsen, K. E., Lærke, H. N., Steenfeldt, S., Hedemann, M. S., & Jørgensen, H. (2006). In vivo methods to study the digestion of starch in pigs and poultry. Animal Feed Science and Technology, 130, 114–135.CrossRefGoogle Scholar
  5. Ban, C., Jo, M., Lim, S., & Choi, Y. L. (2018). Control of the gastrointestinal digestion of solid lipid nanoparticles using PEGylated emulsifiers. Food Chemistry, 239, 442–452.PubMedCrossRefPubMedCentralGoogle Scholar
  6. Barrett, K. E., Boitano, S., Barman, S. M., & Brooks, H. L. (2005). Gastrointestinal physiology. In K. E. Barrett (Ed.), Ganong’s review of medical physiology. New York: McGraw-Hill.Google Scholar
  7. Barroso, E., Cueva, C., Peláez, C., Martínez-Cuesta, M. C., & Requena, T. (2015). The computer-controlled multicompartmental dynamic model of the gastrointestinal system SIMGI. The impact of food bioactives on health: In vitro and ex vivo models. New York: Springer. https://doi.org/10.1007/978-3-319-16104-4_28CrossRefGoogle Scholar
  8. Bastianelli, D., Sauvant, D., & Rérat, A. (1996). Mathematical modeling of digestion and nutrient absorption in pigs. Journal of Animal Science, 74, 1873–1887.PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bellmann, S., Lelieveld, J., Gorissen, T., Minekus, M., & Havenaar, R. (2016). Development of an advanced in vitro model of the stomach and its evaluation versus human gastric physiology. Food Research International, 88, 191–198.CrossRefGoogle Scholar
  10. Benjamin, O., Silcock, P., Kieser, J. A., Waddell, J. N., Swain, M. V., & Everett, D. W. (2012). Development of a model mouth containing an artificial tongue to measure the release of volatile compounds. Innovative Food Science and Emerging Technologies, 15, 96–103.CrossRefGoogle Scholar
  11. Bidlack, W. R., Birt, D., Borzelleca, J., Clemens, R., Coutrelis, N., Coughlin, J. R., et al. (2009). Expert report: Making decisions about the risks of chemicals in foods with limited scientific information. Comprehensive Reviews in Food Science and Food Safety, 8, 269–303.CrossRefGoogle Scholar
  12. Blanquet, S., Marol-Bonnin, S., Beyssac, E., Pompon, D., Renaud, M., & Alric, M. (2001). The ‘biodrug’ concept: An innovative approach to therapy. Trends in Biotechnology, 19, 393–400.PubMedCrossRefPubMedCentralGoogle Scholar
  13. Boccia, S. (2015). Credibility of observational studies: Why public health researchers should care? European Journal of Public Health, 25, 554–555.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bohn, T., Carriere, F., Day, L., Deglaire, A., Egger, L., Freitas, D., et al. (2017). Correlation between in vitro and in vivo data on food digestion. What can we predict with static in vitro digestion models? Critical Reviews in Food Science and Nutrition, 1–23. https://doi.org/10.1080/10408398.2017.1315362PubMedCrossRefGoogle Scholar
  15. Bongaerts, J. H. H., Rossetti, D., & Stokes, J. R. (2007). The lubricating properties of human whole saliva. Tribology Letters, 27, 277–287.CrossRefGoogle Scholar
  16. Bordoloi, A., Singh, J., & Kaur, L. (2012). In vitro digestibility of starch in cooked potatoes as affected by guar gum: Microstructural and rheological characteristics. Food Chemistry, 133, 1206–1213.CrossRefGoogle Scholar
  17. Bornhorst, G. M., Gouseti, O., Wickham, M. S. J., & Bakalis, S. (2016). Engineering digestion: Multiscale processes of food digestion. Journal of Food Science, 81, R534–R543.PubMedCrossRefGoogle Scholar
  18. Bornhorst, G. M., Roman, M. J., Dreschler, K. C., & Singh, R. P. (2013). Physical property changes in raw and roasted almonds during gastric digestion in vivo and in vitro. Food Biophysics, 9, 39–48.CrossRefGoogle Scholar
  19. Bornhorst, G. M., & Singh, R. P. (2013). Kinetics of in vitro bread bolus digestion with varying oral and gastric digestion parameters. Food Biophysics, 8, 50–59.CrossRefGoogle Scholar
  20. Brahma, S., Weier, S. A., & Rose, D. J. (2016). Effects of selected extrusion parameters on physicochemical properties and in vitro starch digestibility and β-glucan extractability of whole grain oats. Journal of Cereal Science, 70, 85–90.CrossRefGoogle Scholar
  21. Bratten, J., & Jones, M. P. (2009). Prolonged recording of duodenal acid exposure in patients with functional dyspepsia and controls using a radiotelemetry pH monitoring system. Journal of Clinical Gastroenterology, 43, 527–533.PubMedCrossRefPubMedCentralGoogle Scholar
  22. Brener, W., Hendrix, T. R., & McHugh, P. R. (1983). Regulation of the gastric emptying of glucose. Gastroenterology, 85, 76–82.PubMedPubMedCentralGoogle Scholar
  23. Brown, R., & Ogden, J. (2004). Children’s eating attitudes and behaviour: A study of the modelling and control theories of parental influence. Health Education Research, 19, 261–271.PubMedCrossRefPubMedCentralGoogle Scholar
  24. Calbet, J. A., & MacLean, D. A. (1997). Role of caloric content on gastric emptying in humans. The Journal of Physiology, 498, 553–559.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Carlson, M. D. A., & Morrison, R. S. (2009). Study design, precision, and validity in observational studies. Journal of Palliative Medicine, 12, 77–82.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Carneiro, I., & Howard, N. (2011). Introduction to epidemiology. Maidenhead: Open University Press.Google Scholar
  27. Carscaddon, L. Literature reviews: Types of clinical study designs. GSU Library Research Guides.Google Scholar
  28. Chen, J., Gaikwad, V., Holmes, M., Murray, B., Povey, M., Wang, Y., et al. (2011). Development of a simple model device for in vitro gastric digestion investigation. Food & Function, 2, 174–182.CrossRefGoogle Scholar
  29. Chen, L., Tian, Y., Zhang, Z., Tong, Q., Sun, B., Rashed, M. M. A., et al. (2017). Effect of pullulan on the digestible, crystalline and morphological characteristics of rice starch. Food Hydrocolloids, 63, 383–390.CrossRefGoogle Scholar
  30. Chen, L., Xu, Y., Fan, T., Liao, Z., Wu, P., Wu, X., et al. (2016). Gastric emptying and morphology of a ‘near real’ in vitro human stomach model (RD-IV-HSM). Journal of Food Engineering, 183(1–8).CrossRefGoogle Scholar
  31. Chessa, S., Huatan, H., Levina, M., Mehta, R. Y., Ferrizzi, D., Rajabi-Siahboomi, A. R., et al. (2014). Application of the dynamic gastric model to evaluate the effect of food on the drug release characteristics of a hydrophilic matrix formulation. International Journal of Pharmaceutics, 466, 359–367.PubMedCrossRefPubMedCentralGoogle Scholar
  32. Cozzini, P. (2015). From medicinal chemistry to food science: A transfer of in silico methods applications. New York: Nova.Google Scholar
  33. Dalla Man, C., Camilleri, M., & Cobelli, C. (2006). A system model of oral glucose absorption: Validation on gold standard data. IEEE Transactions on Biomedical Engineering, 53, 2472–2478.PubMedCrossRefPubMedCentralGoogle Scholar
  34. Dalla Man, C., Yarasheski, K. E., Caumo, A., Robertson, H., Toffolo, G., Polonsky, K. S., et al. (2005). Insulin sensitivity by oral glucose minimal models: Validation against clamp. American Journal of Physiology. Endocrinology and Metabolism, 289, E954–E959.PubMedCrossRefPubMedCentralGoogle Scholar
  35. Darragh, A. J., & Hodgkinson, S. M. (2000). Quantifying the digestibility of dietary protein. The Journal of Nutrition, 130, 1850S–1856S.PubMedCrossRefPubMedCentralGoogle Scholar
  36. Darragh, A. J., & Moughan, P. J. (1995). The three-week-old piglet as a model animal for studying protein digestion in human infants. Journal of Pediatric Gastroenterology and Nutrition, 21, 387–393.PubMedCrossRefPubMedCentralGoogle Scholar
  37. de Loubens, C., Panouillé, M., Saint-Eve, A., Déléris, I., Tréléa, I. C., & Souchon, I. (2011). Mechanistic model of in vitro salt release from model dairy gels based on standardized breakdown test simulating mastication. Journal of Food Engineering, 105, 161–168.CrossRefGoogle Scholar
  38. de Wijk, R. A., Janssen, A. M., & Prinz, J. F. (2011). Oral movements and the perception of semi-solid foods. Physiology and Behavior, 104, 423–428.PubMedCrossRefGoogle Scholar
  39. Deeks, J. J., Dinnes, J., D’Amico, R., Sowden, A. J., Sakarovitch, C., Song, F., et al. (2003). Evaluating non-randomised intervention studies. Health Technology Assessment, 7, iii–iix.PubMedCrossRefPubMedCentralGoogle Scholar
  40. Deferme, S., Annaert, P., & Augustijns, P. (2008). Vitro screening models to assess intestinal drug absorption and metabolism. In C. Ehrhardt & K. J. Kim (Eds.), Drug absorption studies (pp. 182–215). Boston, MA: Springer. https://doi.org/10.1007/978-0-387-74901-3_8CrossRefGoogle Scholar
  41. Deglaire, A., & Moughan, P. J. (2012). Animal models for determining amino acid digestibility in humans – A review. The British Journal of Nutrition, 108, S273–S281.PubMedCrossRefPubMedCentralGoogle Scholar
  42. Dhital, S., Dabit, L., Zhang, B., Flanagan, B., & Shrestha, A. K. (2015). In vitro digestibility and physicochemical properties of milled rice. Food Chemistry, 172, 757–765.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Di Muria, M., Lamberti, G., & Titomanlio, G. (2010). Physiologically based pharmacokinetics: A simple, all purpose model. Industrial and Engineering Chemistry Research, 49, 2969–2978.CrossRefGoogle Scholar
  44. Donaldson, B., Rush, E., Young, O., & Winger, R. (2014). Variation in gastric pH may determine kiwifruit’s effect on functional GI disorder: An in vitro study. Nutrients, 6, 1488–1500.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Dupont, D., & Mackie, A. R. (2015). Static and dynamic in vitro digestion models to study protein stability in the gastrointestinal tract. Drug Discovery Today: Disease Models, 17–18, 23–27.Google Scholar
  46. Egger, L., Ménard, O., Delgado-Andrade, C., Alvito, P., Assunção, R., Balance, S., et al. (2016). The harmonized INFOGEST in vitro digestion method: From knowledge to action. Food Research International, 88, 217–225.CrossRefGoogle Scholar
  47. Englyst, H. N., Kingman, S. M., & Cummings, J. H. (1992). Classification and measurement of nutritionally important starch fractions. European Journal of Clinical Nutrition, 46(Suppl 2), S33–S50.PubMedPubMedCentralGoogle Scholar
  48. Englyst, H. N., Kingman, S. M., Hudson, G. J., & Cummings, J. H. (1996). Measurement of resistant starch in vitro and in vivo. The British Journal of Nutrition, 75, 749.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Englyst, H. N., Veenstra, J., & Hudson, G. J. (2007). Measurement of rapidly available glucose (RAG) in plant foods: A potential in vitro predictor of the glycaemic response. The British Journal of Nutrition, 75, 327.CrossRefGoogle Scholar
  50. Englyst, K. N., Vinoy, S., Englyst, H. N., & Lang, V. (2003). Glycaemic index of cereal products explained by their content of rapidly and slowly available glucose. The British Journal of Nutrition, 89, 329.PubMedCrossRefPubMedCentralGoogle Scholar
  51. Farmer, A. D., Scott, S. M., & Hobson, A. R. (2013). Gastrointestinal motility revisited: The wireless motility capsule. United European Gastroenterology Journal, 1, 413–421.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Ferrua, M. J., & Singh, R. P. (2011). Understanding the fluid dynamics of gastric digestion using computational modeling. Procedia Food Science, 1, 1465–1472.CrossRefGoogle Scholar
  53. Gidley, M. J. (2013). Hydrocolloids in the digestive tract and related health implications. Current Opinion in Colloid and Interface Science, 18, 371–378.CrossRefGoogle Scholar
  54. Goñi, I., Garcia-Alonso, A., & Saura-Calixto, F. (1997). A starch hydrolysis procedure to estimate glycemic index. Nutrition Research, 17, 427–437.CrossRefGoogle Scholar
  55. Gouseti, O., Jaime-Fonseca, M. R., Fryer, P. J., Mills, C., Wickham, M. S. J., & Bakalis, S. (2014). Hydrocolloids in human digestion: Dynamic in-vitro assessment of the effect of food formulation on mass transfer. Food Hydrocolloids, 42, 378–385.CrossRefGoogle Scholar
  56. Granfeldt, Y., Bjorck, I., Drews, A., Tovar, J. (1992). An in vitro procedure based on chewing to predict metabolic response to starch in cereal and legume products. European Journal of Clinical Nutrition, 46, 649–660.Google Scholar
  57. Grimes, D. A., & Schulz, K. F. (2002). An overview of clinical research: The lay of the land. Lancet, 359, 57–61.PubMedCrossRefPubMedCentralGoogle Scholar
  58. Hajat C. (2011) An Introduction to Epidemiology. In: Teare M. (ed), Genetic Epidemiology. Methods in Molecular Biology (Methods and Protocols), vol 713. Humana Press, Totowa, NJGoogle Scholar
  59. Hellström, P. M., Grybäck, P., & Jacobsson, H. (2006). The physiology of gastric emptying. Best Practice & Research. Clinical Anaesthesiology, 20, 397–407.CrossRefGoogle Scholar
  60. Hoffmann, K., Schulze, M. B., Schienkiewitz, A., Nöthlings, U., & Boeing, H. (2004). Application of a new statistical method to derive dietary patterns in nutritional epidemiology. American Journal of Epidemiology, 159, 935–944.PubMedCrossRefPubMedCentralGoogle Scholar
  61. Home Office, Department for Business Innovation & Skills, Department of Health, (2014). Working to reduce the use of animals in scientific research. Crown Copyright. https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/277942/bis-14-589-working-to-reduce-the-use-of_animals-in-research.pdf
  62. Hsu, R. J. C., Chen, H. J., Lu, S., & Chiang, W. (2015). Effects of cooking, retrogradation and drying on starch digestibility in instant rice making. Journal of Cereal Science, 65, 154–161.CrossRefGoogle Scholar
  63. Hu, F. B. (2002). Dietary pattern analysis: A new direction in nutritional epidemiology. Current Opinion Lipidology, 13(1), 3–9.CrossRefGoogle Scholar
  64. Hur, S. J., Lim, B. O., Decker, E. A., & McClements, D. J. (2011). In vitro human digestion models for food applications. Food Chemistry, 125, 1–12.CrossRefGoogle Scholar
  65. Jenkins, D. J., Wolever, T. M., Leeds, A. R., Gassull, M. A., Haisman, P., Dilawari, J., et al. (1978). Dietary fibres, fibre analogues, and glucose tolerance: Importance of viscosity. British Medical Journal, 1, 1392–1394.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Joseph, I. M. P., Zavros, Y., Merchant, J. L., & Kirschner, D. (2003). A model for integrative study of human gastric acid secretion. Journal of Applied Physiology, 94, 1602–1618.PubMedCrossRefPubMedCentralGoogle Scholar
  67. Jumars, P. A. (2000). Animal guts as nonideal chemical reactors: Partial mixing and axial variation in absorption kinetics. The American Naturalist, 155, 544–555.PubMedCrossRefPubMedCentralGoogle Scholar
  68. Kahan, B. C., Rehal, S., & Cro, S. (2015). Risk of selection bias in randomised trials. Trials, 16(405).Google Scholar
  69. Kong, F., & Singh, R. P. (2008a). Disintegration of solid foods in human stomach. Journal of Food Science, 73, R67–R80.PubMedCrossRefPubMedCentralGoogle Scholar
  70. Kong, F., & Singh, R. P. (2008b). A model stomach system to investigate disintegration kinetics of solid foods during gastric digestion. Journal of Food Science, 73, E202–E210.PubMedCrossRefPubMedCentralGoogle Scholar
  71. Kong, F., & Singh, R. P. (2009). Modes of disintegration of solid foods in simulated gastric environment. Food Biophysics, 4, 180–190.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Kozu, H., Kobayashi, I., Neves, M. A., Nakajima, M., Uemura, K., Sato, S., et al. (2010). Analysis of flow phenomena in gastric contents induced by human gastric peristalsis using CFD. Food Biophysics, 5, 330–336.CrossRefGoogle Scholar
  73. Krul, C., Luiten-Schuite, A., Baandagger, R., Verhagen, H., Mohn, G., Feron, V., et al. (2000). Application of a dynamic in vitro gastrointestinal tract model to study the availability of food mutagens, using heterocyclic aromatic amines as model compounds. Food and Chemical Toxicology, 38, 783–792.PubMedCrossRefPubMedCentralGoogle Scholar
  74. Last, J. M., & International Epidemiological Association. (2001). A dictionary of epidemiology. New York: Oxford University Press.Google Scholar
  75. Le Ferrec, E., Chesne, C., Artusson, P., Brayden, D., Fabre, G., & Gires, P. (2001). In vitro models of the intestinal barrier. ATLA, 29, 649–668.PubMedPubMedCentralGoogle Scholar
  76. Lea, A. S. (1890). A comparative study of artificial and natural digestions. The Journal of Physiology, 11, 226–263.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lefebvre, D. E., Venema, K., Gombau, L., Valerio Jr., L. G., Raju, J., Bondy, G. S., et al. (2015). Utility of models of the gastrointestinal tract for assessment of the digestion and absorption of engineered nanomaterials released from food matrices. Nanotoxicology, 9, 523–542.PubMedCrossRefPubMedCentralGoogle Scholar
  78. Lo Curto, A., Pitino, I., Mandalari, G., Dainty, J. R., Faulks, R. M., John Wickham, M. S., et al. (2011). Survival of probiotic lactobacilli in the upper gastrointestinal tract using an in vitro gastric model of digestion. Food Microbiology, 28, 1359–1366.PubMedCrossRefPubMedCentralGoogle Scholar
  79. Logan, J. D., Joern, A., & Wolesensky, W. (2002). Location, time, and temperature dependence of digestion in simple animal tracts. Journal of Theoretical Biology, 216, 5–18.PubMedCrossRefPubMedCentralGoogle Scholar
  80. Love, R. J., Lentle, R. G., Asvarujanon, P., Hemar, Y., & Stafford, K. J. (2012). An expanded finite element model of the intestinal mixing of digesta. Food Digestion, 4, 26–35.CrossRefGoogle Scholar
  81. Lvova, L., Denis, S., Barra, A., Mielle, P., Salles, C., Vergoignan, C., et al. (2012). Salt release monitoring with specific sensors in ‘in vitro’ oral and digestive environments from soft cheeses. Talanta, 97, 171–180.PubMedCrossRefPubMedCentralGoogle Scholar
  82. Mackie, A. R., Bajka, B. H., Rigby, N. M., Wilde, P. J., Alves-Pereira, F., Mosleth, E. F., et al. (2017). Oatmeal particle size alters glycemic index but not as a function of gastric emptying rate. American Journal of Physiology. Gastrointestinal and Liver Physiology, 313, G239–G246.PubMedCrossRefPubMedCentralGoogle Scholar
  83. Mackie, A., Rigby, N., Macierzanka, A. & Bajka, B. (2015). Approaches to static digestion models. In The impact of food bioactives on health (pp. 23–31). Cham: Springer International Publishing. https://doi.org/10.1007/978-3-319-16104-4_3Google Scholar
  84. Mainville, I., Arcand, Y., & Farnworth, E. R. (2005). A dynamic model that simulates the human upper gastrointestinal tract for the study of probiotics. International Journal of Food Microbiology, 99, 287–296.PubMedCrossRefPubMedCentralGoogle Scholar
  85. Maldonado-Valderrama, J., Terriza, J. A. H., Torcello-Gómez, A., & Cabrerizo-Vílchez, M. A. (2013). In vitro digestion of interfacial protein structures. Soft Matter, 9, 1043.CrossRefGoogle Scholar
  86. Marciani, L., Gowland, P. A., Spiller, R. C., Manoj, P., Moore, R. J., Young, P., et al. (2000). Gastric response to increased meal viscosity assessed by echo-planar magnetic resonance imaging in humans. The Journal of Nutrition, 130, 122–127.PubMedCrossRefPubMedCentralGoogle Scholar
  87. Marciani, L., Gowland, P. A., Spiller, R. C., Manoj, P., Moore, R. J., Young, P., et al. (2001). Effect of meal viscosity and nutrients on satiety, intragastric dilution, and emptying assessed by MRI. American Journal of Physiology. Gastrointestinal and Liver Physiology, 280, G1227–G1233.PubMedCrossRefPubMedCentralGoogle Scholar
  88. Marciani, L., Hall, N., Pritchard, S. E., Cox, E. F., Totman, J. J., Lad, M., et al. (2012). Preventing gastric sieving by blending a solid/water meal enhances satiation in healthy humans. The Journal of Nutrition, 142, 1253–1258.PubMedCrossRefPubMedCentralGoogle Scholar
  89. Marino, S., Ganguli, S., Joseph, I. M. P., & Kirschner, D. E. (2003). The importance of an inter-compartmental delay in a model for human gastric acid secretion. Bulletin of Mathematical Biology, 65, 963–990.PubMedCrossRefPubMedCentralGoogle Scholar
  90. Marteau, P., Minekus, M., Havenaar, R., & Huis in’t Veld, J. H. (1997). Survival of lactic acid bacteria in a dynamic model of the stomach and small intestine: Validation and the effects of bile. Journal of Dairy Science, 80, 1031–1037.PubMedCrossRefPubMedCentralGoogle Scholar
  91. Marze, S. (2017). Bioavailability of nutrients and micronutrients: Advances in modeling and in vitro approaches. Annual Review of Food Science and Technology, 8, 35–55.PubMedCrossRefPubMedCentralGoogle Scholar
  92. Mason, W. D., Winer, N., Kochak, G., Cohen, I., & Bell, R. (1979). Kinetics and absolute bioavailability of atenolol. Clinical Pharmacology and Therapeutics, 25.CrossRefGoogle Scholar
  93. McAllister, M. (2010). Dynamic dissolution: A step closer to predictive dissolution testing? Molecular Pharmaceutics, 7, 1374–1387.PubMedCrossRefPubMedCentralGoogle Scholar
  94. McClements, D. J. (2007). Understanding and controlling the microstructure of complex foods. Boca Raton, FL: CRC Press.CrossRefGoogle Scholar
  95. McClements, D. J., & Li, Y. (2010). Review of in vitro digestion models for rapid screening of emulsion-based systems. Food & Function, 1, 32–59.CrossRefGoogle Scholar
  96. McClements, D. J., Li, F., & Xiao, H. (2015). The nutraceutical bioavailability classification scheme: Classifying nutraceuticals according to factors limiting their oral bioavailability. Annual Review of Food Science and Technology, 6, 299–327.PubMedCrossRefPubMedCentralGoogle Scholar
  97. McHugh, P. R. (1983). The control of gastric emptying. Journal of the Autonomic Nervous System, 9, 221–231.PubMedCrossRefPubMedCentralGoogle Scholar
  98. McHugh, P. R., & Moran, T. H. (1979). Calories and gastric emptying: A regulatory capacity with implications for feeding. The American Journal of Physiology, 236, R254–R260.PubMedPubMedCentralGoogle Scholar
  99. Ménard, O., Cattenoz, T., Guillemin, H., Souchon, I., Deglaire, A., Dupont, D., et al. (2014). Validation of a new in vitro dynamic system to simulate infant digestion. Food Chemistry, 145, 1039–1045.PubMedCrossRefPubMedCentralGoogle Scholar
  100. Mercuri, A., Lo Curto, A., Wickham, M. S. J., Craig, D. Q. M., & Barker, S. A. (2008). Dynamic gastric model (DGM): a novel in vitro apparatus to assess the impact of gastric digestion on the droplet size of self-emulsifying drug-delivery systems. Journal of Pharmacy and Pharmacology, 60, 4.CrossRefGoogle Scholar
  101. Meullenet, J.-F., & Gandhapuneni, R. K. (2006). Development of the BITE Master II and its application to the study of cheese hardness. Physiology and Behavior, 89, 39–43.PubMedCrossRefPubMedCentralGoogle Scholar
  102. Mielle, P., Tarrega, A., Sémon, E., Maratray, J., Gorria, P., Liodenot, J. J., et al. (2010). From human to artificial mouth, from basics to results. Sensors and Actuators B: Chemical, 146, 440–445.CrossRefGoogle Scholar
  103. Mills, C.E.N., Marsh, J.T., Johnson, P.E., Boyle, R.,Hoffmann-Sommerguber, K., Dupont, D., Bartra, J., Bakalis, S., McLaughlin, J., Shewry, P.R. (2013). Literature review: ‘in vitro digestibility tests for allergenicity assessment’. EFSA supporting publications, 10(12), EN-529.Google Scholar
  104. Mills, T., Spyropoulos, F., Norton, I. T., & Bakalis, S. (2011). Development of an in-vitro mouth model to quantify salt release from gels. Food Hydrocolloids, 25, 107–113.CrossRefGoogle Scholar
  105. Minekus, M., Alminger, M., Alvito, P., Ballance, S., Bohn, T., Bourlieu, C., et al. (2014). A standardised static in vitro digestion method suitable for food – An international consensus. Food and Function, 5, 1113–1124.PubMedCrossRefPubMedCentralGoogle Scholar
  106. Minekus, M., Marteau, P., Havenaar, R., & Huis in’t Veld, J. H. J. (1995). A multicompartmental dynamic computer-controlled model simulating the stomach and small intestine. ATLA, Alternatives to Laboratory Animals, 23, 197–209.Google Scholar
  107. Minekus, M., Smeets-Peeters, M., Bernalier, A., Marol-Bonnin, S., Havenaar, R., Marteau, P., et al. (1999). A computer-controlled system to simulate conditions of the large intestine with peristaltic mixing, water absorption and absorption of fermentation products. Applied Microbiology and Biotechnology, 53, 108–114.PubMedCrossRefPubMedCentralGoogle Scholar
  108. Misra, S. (2012). Randomized double blind placebo control studies, the ‘Gold Standard’ in intervention based studies. Indian Journal of Sexually Transmitted Diseases and AIDS, 33, 131.PubMedPubMedCentralCrossRefGoogle Scholar
  109. Moosavian, S. P., Haghighatdoost, F., Surkan, P. J., & Azadbakht, L. (2017). Salt and obesity: A systematic review and meta-analysis of observational studies. International Journal of Food Sciences and Nutrition, 68, 265–277.PubMedCrossRefPubMedCentralGoogle Scholar
  110. Morell, P., Hernando, I., & Fiszman, S. M. (2014). Understanding the relevance of in-mouth food processing. A review of in vitro techniques. Trends in Food Science and Technology, 35, 18–31.CrossRefGoogle Scholar
  111. Motilva, M.-J., Serra, A., & Rubió, L. (2015). Nutrikinetic studies of food bioactive compounds: From in vitro to in vivo approaches. International Journal of Food Sciences and Nutrition, 66, S41–S52.PubMedCrossRefPubMedCentralGoogle Scholar
  112. Moxon, T. E., Gouseti, O., & Bakalis, S. (2016). In silico modelling of mass transfer & absorption in the human gut. Journal of Food Engineering, 176, 110–120.PubMedPubMedCentralCrossRefGoogle Scholar
  113. Moxon, T. E., Nimmegeers, P., Telen, D., Fryer, P. J., Van Impe, J., Bakalisa, S., et al. (2017). Effect of chyme viscosity & nutrient feedback mechanism on gastric emptying. Chemical Engineering Science, 171, 318–330.PubMedPubMedCentralCrossRefGoogle Scholar
  114. Mun, S., & McClements, D. J. (2017). Influence of simulated in-mouth processing (size reduction and alpha-amylase addition) on lipid digestion and β-carotene bioaccessibility in starch-based filled hydrogels. LWT-Food Science and Technology, 80, 113–120.CrossRefGoogle Scholar
  115. Ni, P. F., Ho, N. F. H., Fox, J. L., Leuenberger, H., & Higuchi, W. I. (1980). Theoretical model studies of intestinal drug absorption V. Non-steady-state fluid flow and absorption. International Journal of Pharmaceutics, 5, 33–47.CrossRefGoogle Scholar
  116. Panouillé, M., Saint-Eve, A., Déléris, I., Le Bleis, F., & Souchon, I. (2014). Oral processing and bolus properties drive the dynamics of salty and texture perceptions of bread. Food Research International, 62, 238–246.CrossRefGoogle Scholar
  117. Penry, D. L., & Jumars, P. A. (1986). Chemical reactor analysis and optimal digestion. Bioscience, 36, 310–315.CrossRefGoogle Scholar
  118. Penry, D. L., & Jumars, P. A. (1987). Modeling animal guts as chemical reactors. The American Naturalist, 129, 69.CrossRefGoogle Scholar
  119. Peyron, M.-A., & Woda, A. (2016). An update about artificial mastication. Current Opinion in Food Science, 9, 21–28.CrossRefGoogle Scholar
  120. Qin, D., Yang, X., Gao, S., Yao, J., & McClements, D. J. (2016). Influence of hydrocolloids (dietary fibers) on lipid digestion of protein-stabilized emulsions: Comparison of neutral, anionic, and cationic polysaccharides. Journal of Food Science, 81, C1636–C1645.PubMedCrossRefPubMedCentralGoogle Scholar
  121. Ronda, F., Rivero, P., Caballero, P. A., & Quilez, J. (2012). High insoluble fibre content increases in vitro starch digestibility in partially baked breads. International Journal of Food Sciences and Nutrition, 63, 971–977.PubMedCrossRefPubMedCentralGoogle Scholar
  122. Salles, C., Tarrega, A., Mielle, P., Maratray, J., Gorria, P., Liaboeuf, J., et al. (2007). Development of a chewing simulator for food breakdown and the analysis of in vitro flavor compound release in a mouth environment. Journal of Food Engineering, 82, 189–198.CrossRefGoogle Scholar
  123. Salvia-Trujillo, L., Qian, C., Martín-Belloso, O., & McClements, D. J. (2013). Influence of particle size on lipid digestion and β-carotene bioaccessibility in emulsions and nanoemulsions. Food Chemistry, 141, 1475–1480.CrossRefGoogle Scholar
  124. Sauter, M., Curcic, J., Menne, D., Goetze, O., Fried, M., Schwizer, W., et al. (2012). Measuring the interaction of meal and gastric secretion: A combined quantitative magnetic resonance imaging and pharmacokinetic modeling approach. Neurogastroenterology and Motility, 24, 632–e273.PubMedCrossRefPubMedCentralGoogle Scholar
  125. Schwizer, W., Steingötter, A., Fox, M., Zur, T., Thumshirn, M., Bösiger, P., et al. (2002). Non-invasive measurement of gastric accommodation in humans. Gut, 51(Suppl 1), i59–i62.PubMedPubMedCentralCrossRefGoogle Scholar
  126. Siegel, J. A., Urbain, J. L., Adler, L. P., Charkes, N. D., Maurer, A. H., Krevsky, B., et al. (1988). Biphasic nature of gastric emptying. Gut, 29, 85–89.PubMedPubMedCentralCrossRefGoogle Scholar
  127. Slavin, J. (2013). Fiber and prebiotics: Mechanisms and health benefits. Nutrients, 5, 1417–1435.PubMedPubMedCentralCrossRefGoogle Scholar
  128. Stamatopoulos, K., Batchelor, H. K., & Simmons, M. J. H. (2016). Dissolution profile of theophylline modified release tablets, using a biorelevant Dynamic Colon Model (DCM). European Journal of Pharmaceutics and Biopharmaceutics, 108, 9–17.PubMedCrossRefPubMedCentralGoogle Scholar
  129. Stoll, B. R., Batycky, R. P., Leipold, H. R., Milstein, S., & Edwards, D. A. (2000). A theory of molecular absorption from the small intestine. Chemical Engineering Science, 55, 473–489.CrossRefGoogle Scholar
  130. Sugano, K. (2009). Introduction to computational oral absorption simulation. Expert Opinion on Drug Metabolism and Toxicology, 5, 259–293.PubMedCrossRefPubMedCentralGoogle Scholar
  131. Sutton, G. (2003). Putrid gums and ‘Dead Men’s Cloaths’: James Lind aboard the Salisbury. Journal of the Royal Society of Medicine, 96, 605–608.PubMedPubMedCentralGoogle Scholar
  132. Taghipoor, M., Barles, G., Georgelin, C., Licois, J.-R., & Lescoat, P. (2014). Digestion modelling in the small intestine: Impact of dietary fibre. Mathematical Biosciences, 258, 101–112.PubMedCrossRefPubMedCentralGoogle Scholar
  133. Taghipoor, M., Lescoat, P., Licois, J. R., Georgelin, C., & Barles, G. (2012). Mathematical modeling of transport and degradation of feedstuffs in the small intestine. Journal of Theoretical Biology, 294, 114–121.PubMedCrossRefPubMedCentralGoogle Scholar
  134. Tamura, M., Okazaki, Y., Kumagai, C., & Ogawa, Y. (2017). The importance of an oral digestion step in evaluating simulated in vitro digestibility of starch from cooked rice grain. Food Research International, 94, 6–12.PubMedCrossRefPubMedCentralGoogle Scholar
  135. Tharakan, A., Norton, I. T., Fryer, P. J., & Bakalis, S. (2010). Mass transfer and nutrient absorption in a simulated model of small intestine. Journal of Food Science, 75, E339–E346.PubMedCrossRefPubMedCentralGoogle Scholar
  136. Thiese, M. S. (2014). Observational and interventional study design types; an overview. Biochemia Medica, 24, 199–210.PubMedPubMedCentralCrossRefGoogle Scholar
  137. Thomas, K., Aalbers, M., Bannon, G. A., Bartels, M., Dearman, R. J., Esdaile, D. J., et al. (2004). A multi-laboratory evaluation of a common in vitro pepsin digestion assay protocol used in assessing the safety of novel proteins. Regulatory Toxicology and Pharmacology, 39, 87–98.PubMedCrossRefPubMedCentralGoogle Scholar
  138. Thuenemann, E. C. (2015). Dynamic digestion models: general introduction. In: Verhoeckx, K., Cotter, P., López-Expósito, I., Kleiveland, C., Lea, T., Mackie, A., Requena, T., Swiatecka, D., Wichers, H. (eds), The impact of food bioactives on health, in-vitroand ex-vivomodels. Springer, USA.Google Scholar
  139. Timmreck, T. C. (2002). An introduction to epidemiology. Sudbury, MA: Jones and Bartlett Publishers.Google Scholar
  140. van Aken, G. A., Vingerhoeds, M. H., & de Hoog, E. H. A. (2007). Food colloids under oral conditions. Current Opinion in Colloid & Interface Science, 12, 251–262.CrossRefGoogle Scholar
  141. Van de Wiele, T., Van den Abbeele, P., Ossieur, W., Possemiers, S., & Marzorati, M. (2015). The simulator of the human intestinal microbial ecosystem (SHIME®). In K. Verhoeckx, P. Cotter, I. López-Expósito, C. Kleiveland, T. Lea, A. Mackie, et al. (Eds.), The impact of food bioactives on health (pp. 305–317). Cham: Springer International Publishing. https://doi.org/10.1007/978-3-319-16104-4_27CrossRefGoogle Scholar
  142. Van Hung, P., Lam, N., Thi, N., & Phi, L. (2016). Resistant starch improvement of rice starches under a combination of acid and heat-moisture treatments. Food Chemistry, 191, 67–73.PubMedCrossRefPubMedCentralGoogle Scholar
  143. Vardhanabhuti, B., Cox, P. W., Norton, I. T., & Foegeding, E. A. (2011). Lubricating properties of human whole saliva as affected by β-lactoglobulin. Food Hydrocolloids, 25, 1499–1506.CrossRefGoogle Scholar
  144. Vist, G. E., & Maughan, R. J. (1995). The effect of osmolality and carbohydrate content on the rate of gastric emptying of liquids in man. The Journal of Physiology, 486, 523–531.PubMedPubMedCentralCrossRefGoogle Scholar
  145. Wickham, M., Faulks, R., & Mills, C. (2009). In vitro digestion methods for assessing the effect of food structure on allergen breakdown. Molecular Nutrition & Food Research, 53, 952–958.CrossRefGoogle Scholar
  146. Willett, W. (1987). Nutritional epidemiology: Issues and challenges. International Journal of Epidemiology, 16, 312–317.PubMedCrossRefPubMedCentralGoogle Scholar
  147. Willett, W. (2013). Nutritional epidemiology. New York: Oxford University Press.Google Scholar
  148. Wilson, T., & Temple, N. J. (2001). Nutritional health: Strategies for disease prevention. Totowa, NJ: Humana Press.CrossRefGoogle Scholar
  149. Woolnough, J. W., Bird, A. R., Monro, J. A., & Brennan, C. S. (2010). The effect of a brief salivary α-amylase exposure during chewing on subsequent in vitro starch digestion curve profiles. International Journal of Molecular Sciences, 11, 2780–2790.PubMedPubMedCentralCrossRefGoogle Scholar
  150. Wright, N. D., Kong, F., Williams, B. S., & Fortner, L. (2016). A human duodenum model (HDM) to study transport and digestion of intestinal contents. Journal of Food Engineering, 171, 129–136.CrossRefGoogle Scholar
  151. Xu, W. L., Lewis, D., Bronlund, J. E., & Morgenstern, M. P. (2008). Mechanism, design and motion control of a linkage chewing device for food evaluation. Mechanism and Machine Theory, 43, 376–389.CrossRefGoogle Scholar
  152. Yu, L. X., & Amidon, G. L. (1999). A compartmental absorption and transit model for estimating oral drug absorption. International Journal of Pharmaceutics, 186, 119–125.PubMedCrossRefPubMedCentralGoogle Scholar
  153. Yu, L. X., Crison, J. R., & Amidon, G. L. (1996). Compartmental transit and dispersion model analysis of small intestinal transit flow in humans. International Journal of Pharmaceutics, 140, 111–118.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Syahrizal Muttakin
    • 1
    • 2
  • Thomas E. Moxon
    • 1
  • Ourania Gouseti
    • 3
    Email author
  1. 1.School of Chemical EngineeringUniversity of BirminghamBirminghamUK
  2. 2.Indonesian Agency for Agricultural Research and DevelopmentYogyakartaIndonesia
  3. 3.Department of Chemical and Environmental EngineeringUniversity of NottinghamNottinghamUK

Personalised recommendations