Effect of Meal Texture on Postprandial Glucose Excursions and Gut Hormones After Roux-en-Y Gastric Bypass and Sleeve Gastrectomy

Nora Hedbäck, Morten Hindsø, Kirstine N Bojsen-Møller, Adelaide K Linddal, Nils B Jørgensen, Carsten Dirksen, Andreas Møller, Viggo B Kristiansen, Bolette Hartmann, Jens J Holst, Maria S Svane, Sten Madsbad, Nora Hedbäck, Morten Hindsø, Kirstine N Bojsen-Møller, Adelaide K Linddal, Nils B Jørgensen, Carsten Dirksen, Andreas Møller, Viggo B Kristiansen, Bolette Hartmann, Jens J Holst, Maria S Svane, Sten Madsbad

Abstract

Background and aims: The metabolic consequences after Roux-en-Y gastric bypass (RYGB) and sleeve gastrectomy (SG) are often studied using a liquid mixed meal. However, liquid meals may not be representative of the patients' everyday diet. We therefore examined postprandial glucose and gut hormone responses using mixed meals differing only with respect to meal texture.

Methods: Twelve RYGB-operated, 12 SG-operated, and 12 unoperated individuals (controls) were enrolled in the study. Participants were matched on age, sex, and body mass index. In randomized order, each participant underwent a liquid and a solid 4-h mixed meal test on separate days. The meals were isocaloric (309 kcal), and with identical macronutrient composition (47 E% carbohydrate, 18 E% protein, 32 E% fat, and 3 E% dietary fibers). The liquid meal was blended to create a smooth liquid texture while the other meal retained its solid components.

Results: Postprandial glucose concentrations (peak and incremental area under curve, iAUC) did not differ between the two meal textures in any group. In the control group, peak C-peptide was higher after the liquid meal compared with the solid meal (p = 0.04), whereas iAUCs of C-peptide were similar between the two meals in all groups. Peak of glucagon-like peptide-1 (GLP-1) was higher after the liquid meal compared with the solid meal in RYGB- and SG-operated individuals (RYGB p = 0.02; SG p < 0.01), but iAUC of GLP-1 did not differ between meal textures within any group. Peak of glucose-dependent insulin tropic polypeptide (GIP) was higher after the liquid meal in the SG and control groups (SG p = 0.02; controls p < 0.01), but iAUCs of GIP were equal between meals. There were no differences in total AUC of ghrelin between the liquid and solid meals within any of the groups.

Conclusion: A liquid and a solid meal with identical macronutrient composition result in similar postprandial glucose responses, both in operated and unoperated individuals. Small differences were observed for the postprandial peaks of C-peptide, GLP-1, and GIP concentrations. Overall, a liquid meal is suitable for evaluating glucose tolerance, β-cell function, and gut hormones responses, both after RYGB and SG and in unoperated individuals.

Clinical trial registration: [www.clinicaltrials.gov], identifier [NCT04082923].

Keywords: bariatric surgery; ghrelin; glucagon-like peptide-1; insulin secretion; liquid meal; solid meal.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2022 Hedbäck, Hindsø, Bojsen-Møller, Linddal, Jørgensen, Dirksen, Møller, Kristiansen, Hartmann, Holst, Svane and Madsbad.

Figures

FIGURE 1
FIGURE 1
Plasma concentrations of plasma glucose and C-peptide on two different study days with either a liquid or a solid meal. Plasma concentration of and paracetamol was studied after a liquid meal. (A–C) Plasma glucose (D–F) C-peptide (G–I) Paracetamol. Data are means ± SEM. Black (solid line): liquid; white (dotted line): solid.
FIGURE 2
FIGURE 2
Plasma concentrations of total GLP-1, total GIP, and total ghrelin on two different study days with either a liquid or a solid meal. (A–C) total GLP-1; (D–F) total GIP; (G–I) total ghrelin. Data are mean ± SEM. Black (solid line), liquid; white (dotted line), solid.

References

    1. Peterli R, Wölnerhanssen BK, Peters T, Vetter D, Kröll D, Borbély Y, et al. Effect of laparoscopic sleeve gastrectomy vs laparoscopic Roux-en-Y gastric bypass on weight loss in patients with morbid obesity: the SM-BOSS randomized clinical trial. JAMA. (2018) 319:255–65. 10.1001/jama.2017.20897
    1. Sjöström L. Review of the key results from the Swedish Obese Subjects (SOS) trial - a prospective controlled intervention study of bariatric surgery. J Internal Med. (2013) 273:219–34. 10.1111/joim.12012
    1. Felsenreich DM, Bichler C, Langer FB, Gachabayov M, Prager G. Sleeve gastrectomy: surgical technique, outcomes, and complications. Surg Technol Int. (2020) 36:63–9.
    1. Gribble FM, Reimann F. Function and mechanisms of enteroendocrine cells and gut hormones in metabolism. Nat Rev Endocrinol. (2019) 15:226–37. 10.1038/s41574-019-0168-8
    1. Dirksen C, Damgaard M, Bojsen-Møller KN, Jorgensen NB, Kielgast U, Jacobsen SH, et al. Fast pouch emptying, delayed small intestinal transit, and exaggerated gut hormone responses after Roux-en-Y gastric bypass. Neurogastroenterol Motil. (2013) 25:346–e255. 10.1111/nmo.12087
    1. Svane MS, Bojsen-Møller KN, Martinussen C, Dirksen C, Madsen JL, Reitelseder S, et al. Postprandial nutrient handling and gastrointestinal hormone secretion after Roux-en-Y gastric bypass vs sleeve gastrectomy. Gastroenterology. (2019) 156:1627–41.e1. 10.1053/j.gastro.2019.01.262
    1. Nguyen NQ, Debreceni TL, Bambrick JE, Bellon M, Wishart J, Standfield S, et al. Rapid gastric and intestinal transit is a major determinant of changes in blood glucose, intestinal hormones, glucose absorption and postprandial symptoms after gastric bypass. Obesity. (2014) 22:2003–9. 10.1002/oby.20791
    1. Laferrère B, Heshka S, Wang K, Khan Y, McGinty J, Teixeira J, et al. Incretin levels and effect are markedly enhanced 1 month after Roux-en-Y gastric bypass surgery in obese patients with type 2 diabetes. Diabetes Care. (2007) 30:1709–16. 10.2337/dc06-1549
    1. Hindsø M, Svane MS, Hedbäck N, Holst JJ, Madsbad S, Bojsen-Møller KN. The role of GLP-1 in postprandial glucose metabolism after bariatric surgery: a narrative review of human GLP-1 receptor antagonist studies. Surg Obes Related Dis. (2021) 17:1383–91. 10.1016/j.soard.2021.01.041
    1. Svane MS, Bojsen-Møller KN, Nielsen S, Jørgensen NB, Dirksen C, Bendtsen F, et al. Effects of endogenous GLP-1 and GIP on glucose tolerance after Roux-en-Y gastric bypass surgery. Am J Physiol Endocrinol Metab. (2016) 310:E505–14. 10.1152/ajpendo.00471.2015
    1. Tan M, Lamendola C, Luong R, McLaughlin T, Craig C. Safety, efficacy and pharmacokinetics of repeat subcutaneous dosing of avexitide (exendin 9-39) for treatment of post-bariatric hypoglycaemia. Diabetes Obes Metab. (2020) 22:1406–16. 10.1111/dom.14048
    1. Arakawa R, Febres G, Cheng B, Krikhely A, Bessler M, Korner J. Prospective study of gut hormone and metabolic changes after laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass. PLoS One. (2020) 15:e0236133. 10.1371/journal.pone.0236133
    1. Peterli R, Steinert RE, Woelnerhanssen B, Peters T, Christoffel-Courtin C, Gass M, et al. Metabolic and hormonal changes after laparoscopic Roux-en-Y gastric bypass and sleeve gastrectomy: a randomized, prospective trial. Obes Surg. (2012) 22:740–8. 10.1007/s11695-012-0622-3
    1. Fatima F, Hjelmesæth J, Birkeland KI, Gulseth HL, Hertel JK, Svanevik M, et al. Gastrointestinal hormones and β-Cell function after gastric bypass and sleeve gastrectomy: a randomized controlled trial (Oseberg). J Clin Endocrinol Metab. (2022) 107:e756–66. 10.1210/clinem/dgab643
    1. Pellegrini CA, Deveney CW, Patti MG, Lewin M, Way LW. Intestinal transit of food after total gastrectomy and Roux-Y esophagojejunostomy. Am J Surg. (1986) 151:117–25. 10.1016/0002-9610(86)90021-8
    1. Bennink R, Peeters M, Van Den Maegdenbergh V, Geypens B, Rutgeerts P, De Roo M, et al. Evaluation of small-bowel transit for solid and liquid test meal in healthy men and women. Eur J Nucl Med. (1999) 26:1560–6. 10.1007/s002590050495
    1. Grong E, Græslie H, Munkvold B, Arbo IB, Kulseng BE, Waldum HL, et al. Gastrin secretion after bariatric surgery—response to a protein-rich mixed meal following Roux-En-Y gastric bypass and sleeve gastrectomy: a pilot study in normoglycemic women. Obes Surg. (2016) 26:1448–56. 10.1007/s11695-015-1985-z
    1. Stano S, Alam F, Wu L, Dutia R, Ng S-N, Sala M, et al. Effect of meal size and texture on gastric pouch emptying and glucagon-like peptide 1 after gastric bypass surgery. Surg Obes Relat Dis Off J Am Soc Bariatr Surg. (2017) 13:1975–83. 10.1016/j.soard.2017.09.004
    1. Bunt JC, Blackstone R, Thearle MS, Vinales KL, Votruba S, Krakoff J. Changes in glycemia, insulin and gut hormone responses to a slowly ingested solid low-carbohydrate mixed meal after laparoscopic gastric bypass or band surgery. Int J Obes. (2017) 41:706–13. 10.1038/ijo.2017.22
    1. Christensen JJ, Arnesen EK, Andersen R, Eneroth H, Erkkola M, Høyer A, et al. The nordic nutrition recommendations 2022 – principles and methodologies. Food Nutr Res. (2020) 64: 1–15.
    1. Chan BY, Tsang HM, Ng CWY, Ling WHW, Leung DCW, Lee HHC, et al. Performance evaluation of five commercial assays for detection of acetaminophen. J Clin Lab Anal. (2019) 33:e22683. 10.1002/jcla.22683
    1. Orskov C, Rabenhoj L, Wettergren A, Kofod H, Holst JJ. Tissue and plasma concentrations of amidated and glycine-extended glucagon-like peptide I in humans. Diabetes. (1994) 43:535–9. 10.2337/diab.43.4.535
    1. Krarup T, Holst JJ. The heterogeneity of gastric inhibitory polypeptide in porcine and human gastrointestinal mucosa evaluated with five different antisera. Regul Pept. (1984) 9:35–46. 10.1016/0167-0115(84)90005-3
    1. Lindgren O, Carr RD, Deacon CF, Holst JJ, Pacini G, Mari A, et al. Incretin hormone and insulin responses to oral versus intravenous lipid administration in humans. J Clin Endocrinol Metab. (2011) 96:2519–24. 10.1210/jc.2011-0266
    1. Loo BM, Marniemi J, Jula A. Evaluation of multiplex immunoassays, used for determination of adiponectin, resistin, leptin, and ghrelin from human blood samples, in comparison to ELISA assays. Scand J Clin Lab Invest. (2011) 71:221–6. 10.3109/00365513.2011.554996
    1. Eiken A, Fuglsang S, Eiken M, Svane MS, Holst JJ, Bojsen-Moller KN, et al. After Roux-en-Y Gastric bypass, enterohepatic bile circulation is altered and bile acid retention increased while bile acid homeostasis remains normal after sleeve gastrectomy. Diabetes. (2018) 67.
    1. Hovorka R, Soons PA, Young MA. ISEC: a program to calculate insulin secretion. Comput Methods Programs Biomed. (1996) 50:253–64. 10.1016/0169-2607(96)01755-5
    1. Kjems LL, Holst JJ, Vølund A, Madsbad S. The influence of GLP-1 on glucose-stimulated insulin secretion: effects on β-cell sensitivity in type 2 and nondiabetic subjects. Diabetes. (2003) 52:380–6. 10.2337/diabetes.52.2.380
    1. Shah M, Franklin B, Adams-Huet B, Mitchell J, Bouza B, Dart L, et al. Effect of meal composition on postprandial glucagon-like peptide-1, insulin, glucagon, C-peptide, and glucose responses in overweight/obese subjects. Eur J Nutr. (2017) 56:1053–62. 10.1007/s00394-016-1154-8
    1. Jensen CZ, Bojsen-Møller KN, Svane MS, Holst LM, Hermansen K, Hartmann B, et al. Responses of gut and pancreatic hormones, bile acids, and fibroblast growth factor-21 differ to glucose, protein, and fat ingestion after gastric bypass surgery. Am J Physiol Gastrointest Liver Physiol. (2020) 318:G661–72. 10.1152/ajpgi.00265.2019
    1. Lee CJ, Brown TT, Cheskin LJ, Choi P, Moran TH, Peterson L, et al. Effects of meal composition on postprandial incretin, glucose and insulin responses after surgical and medical weight loss. Obes Sci Pract. (2015) 1:104–9. 10.1002/osp4.17
    1. Martinussen C, Bojsen-Møller KN, Dirksen C, Svane MS, Kristiansen VB, Hartmann B, et al. Augmented GLP-1 secretion as seen after gastric bypass may be obtained by delaying carbohydrate digestion. J Clin Endocrinol Metab. (2019) 104:3233–44. 10.1210/jc.2018-02661
    1. Marathe CS, Feinle-Bisset C, Pilichiewicz A, Lange K, Jones KL, Rayner CK, et al. The duodenal glucose load impacts the oral disposition index in healthy subjects. Diabet Med. (2015) 32:1500–3. 10.1111/dme.12802
    1. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev. (2007) 87:1409–39.
    1. Rhee NA, Wahlgren CD, Pedersen J, Mortensen B, Langholz E, Wandall EP, et al. Effect of Roux-en-Y gastric bypass on the distribution and hormone expression of small-intestinal enteroendocrine cells in obese patients with type 2 diabetes. Diabetologia. (2015) 58:2254–8. 10.1007/s00125-015-3696-3
    1. Nergård BJ, Lindqvist A, Gislason HG, Groop L, Ekelund M, Wierup N, et al. Mucosal glucagon-like peptide-1 and glucose-dependent insulin tropic polypeptide cell numbers in the super-obese human foregut after gastric bypass. Surg Obes Relat Dis. (2015) 11:1237–46. 10.1016/j.soard.2015.03.021
    1. Jorsal T, Rhee NA, Pedersen J, Wahlgren CD, Mortensen B, Jepsen SL, et al. Enteroendocrine K and L cells in healthy and type 2 diabetic individuals. Diabetologia. (2018) 61:284–94. 10.1007/s00125-017-4450-9
    1. Salehi M, Gastaldelli A, D’Alessio DA. Altered islet function and insulin clearance cause hyperinsulinemia in gastric bypass patients with symptoms of postprandial hypoglycemia. J Clin Endocrinol Metab. (2014) 99:2008–17. 10.1210/jc.2013-2686
    1. Kandel D, Bojsen-Møller KN, Svane MS, Samkani A, Astrup A, Holst JJ, et al. Mechanisms of action of a carbohydrate-reduced, high-protein diet in reducing the risk of postprandial hypoglycemia after Roux-en-Y gastric bypass surgery. Am J Clin Nutr. (2019) 110:296–304. 10.1093/ajcn/nqy310
    1. Medhus AW, Lofthus CM, Bredesen J, Husebye E. Gastric emptying: the validity of the paracetamol absorption test adjusted for individual pharmacokinetics. Neurogastroenterol Motil. (2001) 13:179–85. 10.1046/j.1365-2982.2001.00249.x
    1. Bartholomé R, Salden B, Vrolijk MF, Troost FJ, Masclee A, Bast A, et al. Paracetamol as a post prandial marker for gastric emptying, a food-drug interaction on absorption. PLoS One. (2015) 10:e0136618. 10.1371/journal.pone.0136618

Source: PubMed

3
Se inscrever