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Glycemic response, satiety, gastric secretions and emptying after bread consumption with water, tea or lemon juice: a randomized crossover intervention using MRI

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European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Numerous studies, including our previous work with lemon juice, have reported that low-pH meals reduce the glycemic response to starchy foods. However, the underlying mechanism is not yet understood. Tea, for its polyphenol content, has also been investigated. The main objective of this research was to concurrently study gastric emptying, appetite perceptions and glycemic responses to bread consumed with water, tea, or lemon juice.

Methods

In this randomized, crossover intervention, ten participants consumed equal portions of bread (100 g) with 250 mL of water, water-diluted lemon juice, or black tea at breakfast. Gastric volumes, blood glucose concentrations and appetite perceptions were alternately assessed over 180 min using magnetic resonance imaging, the finger-prick method and visual analogue scales, respectively.

Results

Compared to water, lemon juice led to a 1.5 fold increase of the volume of gastric contents, 30 min after the meal (454.0 ± 18.6 vs. 298.4 ± 19.5 mL, \(\overline{x}\)  ± SEM P < 0.00001). Gastric emptying was also 1.5 times faster (P < 0.01). Conversely, lemon juice elicited a lower glycemic response than water (blood glucose concentrations at t = 55 min were 35% lower, P = 0.039). Tea had no effect. Changes in appetite perceptions and gastric volumes correlated well, but with no significant differences between the meals.

Conclusions

Lemon juice lowered the glycemic response and increased both gastric secretions and emptying rate. The results are compatible with the hypothesis that the reduction of the glycemic response is mainly due to the interruption of starch hydrolysis via the acid-inhibition of salivary α-amylase.

Trial registration number

NCT03265392, August 29, 2017.

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Abbreviations

AUC :

Area Under the Curve

BMI:

Body Mass Index

HAS:

Human salivary α-amylase

VAS:

Visual Analogue Scale

References

  1. Boers HM, Alssema M, Mela DJ, Peters HP, Vonk RJ, Priebe MG (2019) The rate of glucose appearance is related to postprandial glucose and insulin responses in adults: a systematic review and meta-analysis of stable isotope studies. J Nutr 149(11):1896–1903

    PubMed  Google Scholar 

  2. Stylianopoulos CL (2012) Carbohydrates: Requirements and Dietary Importance. In: Caballero B, Allen LH, Prentice A (eds) Encyclopedia of human nutrition, vol 1, 2nd edn. Academic press, Cambridge, pp 316–321

    Google Scholar 

  3. Bornhorst GM, Singh RP (2012) Bolus formation and disintegration during digestion of food carbohydrates. Compr Rev Food Sci Food Saf 11(2):101–118

    CAS  Google Scholar 

  4. Gropper SS, Smith JL (2013) Digestion of polysaccharides. In: Advanced nutrition and human metabolism. 6th edn. Cengage Learning, United States of America, p 70

  5. Freitas D, Le Feunteun S (2018) Acid induced reduction of the glycaemic response to starch-rich foods: the salivary α-amylase inhibition hypothesis. Food Funct

  6. Fried M, Abramson S, Meyer J (1987) Passage of salivary amylase through the stomach in humans. Dig Dis Sci 32(10):1097–1103

    CAS  PubMed  Google Scholar 

  7. Salvatore T, Giugliano D (1996) Pharmacokinetic-pharmacodynamic relationships of Acarbose. Clin Pharmacokinet 30(2):94–106

    CAS  PubMed  Google Scholar 

  8. Davenport HW (1992) A history of gastric secretion and digestion: experimental studies to 1975. Oxford University Press, Oxford

    Google Scholar 

  9. Dressman JB, Berardi RR, Dermentzoglou LC, Russell TL, Schmaltz SP, Barnett JL, Jarvenpaa KM (1990) Upper gastrointestinal (GI) pH in young, healthy men and women. Pharm Res 7(7):756–761

    CAS  PubMed  Google Scholar 

  10. Gardner JD, Ciociola AA, Robinson M (2002) Measurement of meal-stimulated gastric acid secretion by in vivo gastric autotitration. J Appl Physiol 92(2):427–434

    CAS  PubMed  Google Scholar 

  11. Malagelada J-R, Go VLW, Summerskill WHJ (1979) Different gastric, pancreatic, and biliary responses to solid-liquid or homogenized meals. Dig Dis Sci 24(2):101–110

    CAS  PubMed  Google Scholar 

  12. Freitas D, Le Feunteun S (2019) Oro-gastro-intestinal digestion of starch in white bread, wheat-based and gluten-free pasta: unveiling the contribution of human salivary α-amylase. Food Chem 274:566–573

    CAS  PubMed  Google Scholar 

  13. Bergeim O (1926) Intestinal chemistry: iii. Salivary digestion in the human stomach and intestines. Arch Intern Med 37(1):110–117

    Google Scholar 

  14. Martens BM, Bruininx EM, Gerrits WJ, Schols HA (2020) The importance of amylase action in the porcine stomach to starch digestion kinetics. Anim Feed Sci Technol 267:114546

    CAS  Google Scholar 

  15. Freitas D, Le Feunteun S (2019) Inhibitory effect of black tea, lemon juice, and other beverages on salivary and pancreatic amylases: What impact on bread starch digestion? A dynamic in vitro study. Food Chem 297:124885

    CAS  PubMed  Google Scholar 

  16. Kerimi A, Nyambe-Silavwe H, Gauer JS, Tomás-Barberán FA, Williamson G (2017) Pomegranate juice, but not an extract, confers a lower glycemic response on a high–glycemic index food: randomized, crossover, controlled trials in healthy subjects. Am J Clin Nutr 106(6):1384–1393

    CAS  PubMed  Google Scholar 

  17. Brighenti F, Castellani G, Benini L, Casiraghi M, Leopardi E, Crovetti R, Testolin G (1995) Effect of neutralized and native vinegar on blood glucose and acetate responses to a mixed meal in healthy subjects. Eur J Clin Nutr 49(4):242–247

    CAS  PubMed  Google Scholar 

  18. Johnston CS, Buller AJ (2005) Vinegar and peanut products as complementary foods to reduce postprandial glycemia. J Am Diet Assoc 105(12):1939–1942

    CAS  PubMed  Google Scholar 

  19. Johnston CS, Steplewska I, Long CA, Harris LN, Ryals RH (2010) Examination of the antiglycemic properties of vinegar in healthy adults. Ann Nutr Metab 56(1):74–79

    CAS  PubMed  Google Scholar 

  20. Leeman M, Ostman E, Bjorck I (2005) Vinegar dressing and cold storage of potatoes lowers postprandial glycaemic and insulinaemic responses in healthy subjects. Eur J Clin Nutr 59(11):1266–1271

  21. Liljeberg H, Björck I (1998) Delayed gastric emptying rate may explain improved glycaemia in healthy subjects to a starchy meal with added vinegar. Eur J Clin Nutr 52(5):368

    CAS  PubMed  Google Scholar 

  22. Östman E, Granfeldt Y, Persson L, Björck I (2005) Vinegar supplementation lowers glucose and insulin responses and increases satiety after a bread meal in healthy subjects. Eur J Clin Nutr 59(9):983

    PubMed  Google Scholar 

  23. Johnston CS, Kim CM, Buller AJ (2004) Vinegar improves insulin sensitivity to a high-carbohydrate meal in subjects with insulin resistance or type 2 diabetes. Diabetes Care 27(1):281–282

    PubMed  Google Scholar 

  24. Liatis S, Grammatikou S, Poulia K-A, Perrea D, Makrilakis K, Diakoumopoulou E, Katsilambros N (2010) Vinegar reduces postprandial hyperglycaemia in patients with type II diabetes when added to a high, but not to a low, glycaemic index meal. Eur J Clin Nutr 64(7):727

    CAS  PubMed  Google Scholar 

  25. Mitrou P, Raptis AE, Lambadiari V, Boutati E, Petsiou E, Spanoudi F, Papakonstantinou E, Maratou E, Economopoulos T, Dimitriadis G (2010) Vinegar decreases postprandial hyperglycemia in patients with type 1 diabetes. Diabetes Care 33(2):e27–e27

    PubMed  Google Scholar 

  26. Sugiyama M, Tang A, Wakaki Y, Koyama W (2003) Glycemic index of single and mixed meal foods among common Japanese foods with white rice as a reference food. Eur J Clin Nutr 57(6):743

    CAS  PubMed  Google Scholar 

  27. Bo S, Seletto M, Choc A, Ponzo V, Lezo A, Demagistris A, Evangelista A, Ciccone G, Bertolino M, Cassader M (2017) The acute impact of the intake of four types of bread on satiety and blood concentrations of glucose, insulin, free fatty acids, triglyceride and acylated ghrelin. A randomized controlled cross-over trial. Food Res Int 92:40–47

    CAS  PubMed  Google Scholar 

  28. Lappi J, Selinheimo E, Schwab U, Katina K, Lehtinen P, Mykkänen H, Kolehmainen M, Poutanen K (2010) Sourdough fermentation of wholemeal wheat bread increases solubility of arabinoxylan and protein and decreases postprandial glucose and insulin responses. J Cereal Sci 51(1):152–158

    CAS  Google Scholar 

  29. Liljeberg H, Björck I (1996) Delayed gastric emptying rate as a potential mechanism for lowered glycemia after eating sourdough bread: studies in humans and rats using test products with added organic acids or an organic salt. Am J Clin Nutr 64(6):886–893

    CAS  PubMed  Google Scholar 

  30. Liljeberg HG, Lönner CH, Björck IM (1995) Sourdough fermentation or addition of organic acids or corresponding salts to bread improves nutritional properties of starch in healthy humans. J Nutr 125(6):1503–1511

    CAS  PubMed  Google Scholar 

  31. Maioli M, Pes GM, Sanna M, Cherchi S, Dettori M, Manca E, Farris GA (2008) Sourdough-leavened bread improves postprandial glucose and insulin plasma levels in subjects with impaired glucose tolerance. Acta Diabetol 45(2):91–96

    CAS  PubMed  Google Scholar 

  32. Scazzina F, Del Rio D, Pellegrini N, Brighenti F (2009) Sourdough bread: Starch digestibility and postprandial glycemic response. J Cereal Sci 49(3):419–421

    CAS  Google Scholar 

  33. Freitas D, Boué F, Benallaoua M, Airinei G, Benamouzig R, Le Feunteun S (2021) Lemon juice, but not tea, reduces the glycemic response to bread in healthy volunteers: a randomized crossover trial. Eur J Nutr 60(1):113–122

    CAS  PubMed  Google Scholar 

  34. Gobbetti M, Rizzello CG, Di Cagno R, De Angelis M (2014) How the sourdough may affect the functional features of leavened baked goods. Food Microbiol 37:30–40

    CAS  PubMed  Google Scholar 

  35. Lim J, Henry CJ, Haldar S (2016) Vinegar as a functional ingredient to improve postprandial glycemic control—human intervention findings and molecular mechanisms. Mol Nutr Food Res 60(8):1837–1849

    CAS  PubMed  Google Scholar 

  36. Poutanen K, Flander L, Katina K (2009) Sourdough and cereal fermentation in a nutritional perspective. Food Microbiol 26(7):693–699

    CAS  PubMed  Google Scholar 

  37. Petsiou EI, Mitrou PI, Raptis SA, Dimitriadis GD (2014) Effect and mechanisms of action of vinegar on glucose metabolism, lipid profile, and body weight. Nutr Rev 72(10):651–661

    PubMed  Google Scholar 

  38. Pulido JME, Salazar MA (1999) Changes in insulin sensitivity, secretion and glucose effectiveness during menstrual cycle. Arch Med Res 30(1):19–22

    CAS  Google Scholar 

  39. Dye L, Blundell J (1997) Menstrual cycle and appetite control: implications for weight regulation. Hum Reprod 12(6):1142–1151

    CAS  PubMed  Google Scholar 

  40. Freitas D, Le Feunteun S, Panouillé M, Souchon I (2018) The important role of salivary α-amylase in the gastric digestion of wheat bread starch. Food Funct 9(1):200–208

    CAS  PubMed  Google Scholar 

  41. Treier R, Steingoetter A, Weishaupt D, Goetze O, Boesiger P, Fried M, Schwizer W (2006) Gastric motor function and emptying in the right decubitus and seated body position as assessed by magnetic resonance imaging. J Magn Reson Imaging 23(3):331–338

    PubMed  Google Scholar 

  42. Flint A, Raben A, Blundell J, Astrup A (2000) Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int J Obes 24(1):38

    CAS  Google Scholar 

  43. Kwiatek MA, Menne D, Steingoetter A, Goetze O, Forras-Kaufman Z, Kaufman E, Fruehauf H, Boesiger P, Fried M, Schwizer W (2009) Effect of meal volume and calorie load on postprandial gastric function and emptying: studies under physiological conditions by combined fiber-optic pressure measurement and MRI. Am J Physiol 297(5):G894–G901

    CAS  Google Scholar 

  44. Marciani L, Gowland PA, Spiller RC, Manoj P, Moore RJ, Young P, Fillery-Travis AJ (2001) Effect of meal viscosity and nutrients on satiety, intragastric dilution, and emptying assessed by MRI. Am J Physiol 280(6):G1227–G1233

    CAS  Google Scholar 

  45. Marciani L, Pritchard SE, Hellier-Woods C, Costigan C, Hoad C, Gowland PA, Spiller RC (2013) Delayed gastric emptying and reduced postprandial small bowel water content of equicaloric whole meal bread versus rice meals in healthy subjects: novel MRI insights. Eur J Clin Nutr 67(7):754

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Deane AM, Nguyen NQ, Stevens JE, Fraser RJ, Holloway RH, Besanko LK, Burgstad C, Jones KL, Chapman MJ, Rayner CK (2010) Endogenous glucagon-like peptide-1 slows gastric emptying in healthy subjects, attenuating postprandial glycemia. J Clin Endocrinol Metab 95(1):215–221

    CAS  PubMed  Google Scholar 

  47. Feinle C, Kunz P, Boesiger P, Fried M, Schwizer W (1999) Scintigraphic validation of a magnetic resonance imaging method to study gastric emptying of a solid meal in humans. Gut 44(1):106–111

    CAS  PubMed  PubMed Central  Google Scholar 

  48. RCoreTeam (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  49. Hunt J, Knox M (1962) The regulation of gastric emptying of meals containing citric acid and salts of citric acid. J Physiol 163(1):34–45

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Hunt J, Knox M (1969) The slowing of gastric emptying by nine acids. J Physiol 201(1):161–179

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Hunt J, Knox M (1972) The slowing of gastric emptying by four strong acids and three weak acids. J Physiol 222(1):187–208

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Watanabe S, Dawes C (1988) The effects of different foods and concentrations of citric acid on the flow rate of whole saliva in man. Arch Oral Biol 33(1):1–5

    CAS  PubMed  Google Scholar 

  53. Carreira L, Midori Castelo P, Simões C, Capela e Silva F, Viegas C, Lamy E (2020) Changes in salivary proteome in response to bread odour. Nutrients 12(4):1002

    CAS  PubMed Central  Google Scholar 

  54. Lamy E, Santos V, Barrambana S, Simões C, Carreira L, Infante P, Capela e Silva F (2021) Saliva protein composition relates with interindividual variations in bread sensory ratings. Starch-Stärke 73(1–2):2000052

    CAS  Google Scholar 

  55. Johnson LR (1973) Effect of gastric mucosal acidification on the action of pepsigogues. Am J Physiol 225(6):1411–1415

    CAS  PubMed  Google Scholar 

  56. Goetze O, Treier R, Fox M, Steingoetter A, Fried M, Boesiger P, Schwizer W (2009) The effect of gastric secretion on gastric physiology and emptying in the fasted and fed state assessed by magnetic resonance imaging. Neurogastroenterol Motil 21(7):725-e742

    CAS  PubMed  Google Scholar 

  57. Hunt J, Smith J, Jiang C (1985) Effect of meal volume and energy density on the gastric emptying of carbohydrates. Gastroenterology 89(6):1326–1330

    CAS  PubMed  Google Scholar 

  58. Calbet J, MacLean D (1997) Role of caloric content on gastric emptying in humans. J Physiol 498(2):553–559

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Siegel J, Urbain J, Adler L, Charkes N, Maurer A, Krevsky B, Knight L, Fisher R, Malmud L (1988) Biphasic nature of gastric emptying. Gut 29(1):85–89

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Grimm M, Koziolek M, Saleh M, Schneider F, Garbacz G, Kühn J-P, Weitschies W (2018) Gastric emptying and small bowel water content after administration of grapefruit juice compared to water and isocaloric solutions of glucose and fructose: a four-way crossover mri pilot study in healthy subjects. Mol Pharm 15(2):548–559

    CAS  PubMed  Google Scholar 

  61. Sievenpiper JL, Jenkins DJ, Josse RG, Vuksan V (2000) Dilution of the 75-g oral glucose tolerance test increases postprandial glycemia: implications for diagnostic criteria. CMAJ 162(7):993–996

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Blaak E, Antoine JM, Benton D, Björck I, Bozzetto L, Brouns F, Diamant M, Dye L, Hulshof T, Holst J (2012) Impact of postprandial glycaemia on health and prevention of disease. Obesity Rev 13(10):923–984

    CAS  Google Scholar 

  63. Wolever TM, Leung J, Vuksan V, Jenkins AL (2009) Day-to-day variation in glycemic response elicited by white bread is not related to variation in satiety in humans. Appetite 52(3):654–658

    CAS  PubMed  Google Scholar 

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Acknowledgements

First of all, we thank the participants for their involvement. We thank Anders Sjödin and Thea Toft Hansen (University of Copenhagen) for their help during the preparation of this study. We thank Claire Gaudichon (INRA), Furio Brighenti (University of Parma), Luca Marciani (University of Nottingham) and Valérie Micard (Montpellier Supagro) for helpful discussions. We thank Amira Halabi and Ousmane Suwareh for their help using R software for statistical analysis. We thank our colleagues from the GMPA research unit (now UMR SayFood), Isabelle Souchon and Anne Saint-Eve, team leaders, for their constant valuable support and technical help, and Pascal Bonnarme, head of GMPA during this study. We thank Vincent Lebon, head of the Service Hospitalier François Joliot (SHFJ) for allowing us to conduct the MRI exams in its facilities. We also recall that this study was developed on the ground of former tests run at SHFJ also, jointly by all authors from GMPA and SHFJ-IR4M laboratories. Finally we also thank all of those who contributed to the successful completion of this part of the study, in particular the MRI technicians Laure Miche, Brigitte Mansalier, Béatrice Lhuillery et Laurence Tavassoli who performed the MRI exams.

Funding

Daniela Freitas acknowledges funding from an IDEX Paris-Saclay doctoral grant. This research did not receive any other specific grant from funding agencies in the public, commercial or not-for-profit sectors.

Author information

Author notes

  1. Daniela Freitas

    Present address: Teagasc Food Research Centre, Moorepark, Fermoy, Ireland

  2. François Boué

    Present address: Laboratoire Léon Brillouin UMR 12, CNRS - CEA Université Paris-Saclay, 91191, Gif-sur-Yvette Cedex, France

  3. Evelyne Lutton

    Present address: MIA, INRAE, ISC-PIF, 75013, Paris, France

  4. Steven Le Feunteun

    Present address: STLO, INRAE, Institut Agro, 35042, Rennes, France

Authors and Affiliations

  1. Université Paris-Saclay, INRAE, AgroParisTech, UMR SayFood, 78850, Thiverval-Grignon, France

    Daniela Freitas, Evelyne Lutton & Steven Le Feunteun

  2. CEFRED (Centre d’exploration Fonctionnelle et de Rééducation Digestive), Hôpital Avicenne, Service de gastro-entérologie, Bobigny Cedex, France

    François Boué, Mourad Benallaoua, Gheorghe Airinei & Robert Benamouzig

  3. Université Paris‐Saclay, CEA, CNRS, Inserm, BioMaps, Orsay, France

    Laurène Jourdain, Rose-Marie Dubuisson, Xavier Maître & Luc Darrasse

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Contributions

DF participated in the conceptualization of the study, conducted the research, analyzed and interpreted the data and wrote the manuscript. FB was involved in the conceptualization of the study, supervision of the study and interpretation. MB was involved in the conceptualization of the study. GA was involved in the conceptualization of the study. RB was the principal investigator and primary clinical advisor, and was involved in the conceptualization of the study. EL was involved in the conceptualization of the study and in the analytical procedures for the MRI scans. LJ assisted in the preparation of the MRI protocol and in the acquisition of MRI data. R-MD assisted in the preparation of the MRI protocol and in the acquisition of MRI data. XM was involved in the conceptualization of the study, established the MRI examination protocol and the analytical procedures for the MRI scans. LD was involved in the conceptualization of the study and supervision of the study. SLF was involved in the conceptualization of the study, supervision, data analysis and interpretation. All authors reviewed the manuscript and approved the final version.

Corresponding author

Correspondence to Steven Le Feunteun.

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Ethical approval by the ethics committee Lyon Sud-Est IV (Lyon, France), approval code: A 17–347.

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Freitas, D., Boué, F., Benallaoua, M. et al. Glycemic response, satiety, gastric secretions and emptying after bread consumption with water, tea or lemon juice: a randomized crossover intervention using MRI. Eur J Nutr 61, 1621–1636 (2022). https://doi.org/10.1007/s00394-021-02762-2

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