Abstract
Background
The aim was to determine the effects of fat and protein preloads on pouch emptying (PE), caecal arrival time (CAT), glucose absorption, blood glucose (BSL), gut hormones, haemodynamics and gastrointestinal (GI) symptoms in subjects who had undergone Roux-en-Y gastric bypass (RYGB) >12 months previously.
Methods
Ten RYGB subjects were studied on three occasions, in randomised order, receiving 200-ml preloads of either water, fat (30 ml olive oil) or whey protein (55 g), 30 min before a mixed meal. PE, CAT, BSL, plasma 3-O-methyl-D-glucopyranose (3-OMG), insulin, glucose-dependent insulinotropic polypeptide (GIP), glucagon-like peptide 1 (GLP-1) and glucagon, blood pressure (BP), heart rate (HR) and GI symptoms were assessed over 270 min.
Results
Although fat and protein preloads did not alter PE of either solids or liquids, the CAT of solids, but not liquids, was longer than that after the water preload (fat 68 ± 5 min and protein 71 ± 6 min vs. water 46 ± 5 min; P = 0.02). BSL elevated promptly after the meal on all days (P < 0.001), but after protein, the magnitude and integrated increases in the first 75 min were less than fat and water preloads (area under the curve (AUC(0–75 min)), 18.7 ± 18.2 vs. 107.2 ± 30.4 and 76.1 ± 19.3 mmol/L/min; P < 0.05). Compared to water preload, the protein and fat preloads were associated with greater increases in plasma insulin, GLP-1 and glucagon concentrations, a reduction in BP, and greater increases in HR, fullness, bloating and nausea. Plasma 3-OMG levels were lower after the protein than after the water and fat preloads (P < 0.001).
Conclusions
Given its effects to attenuate post-prandial glycaemia, reduce intestinal glucose absorption and potentiate the “incretin response”, without inducing more adverse post-prandial GI symptom, protein preload may prove clinically useful in RYGB patients and warrant further evaluation, particularly in those with type 2 diabetes (T2DM) and/or dumping syndrome.
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References
Tice JA, Karliner L, Walsh J, et al. Gastric banding or bypass? A systematic review comparing the two most popular bariatric procedures. Am J Med. 2008;121(10):885–93.
Lin HC, Doty JE, Reedy TJ, et al. Inhibition of gastric emptying by glucose depends on length of intestine exposed to nutrient. Am J Physiol. 1989;256(2 Pt 1):G404–11.
Sun Y, Song G, Yin J, et al. Effects and mechanisms of electroacupuncture on glucagon-induced small intestinal hypomotility in dogs. Neurogastroenterol Motil: Off J Eur Gastrointest Motil Soc. 2010;22(11):1217–23. e318.
Trahair LG, Horowitz M, Hausken T, et al. Effects of exogenous glucagon like peptide 1 on the blood pressure, heart rate, mesenteric blood flow and glycemiac responses to intraduodenal glucose in healthy older subjects. J Clin Endocrinol Metab. 2014;99(12):E2628–34.
Chapman IM, Goble EA, Wittert GA, et al. Effects of small-intestinal fat and carbohydrate infusions on appetite and food intake in obese and nonobese men. Am J Clin Nutr. 1999;69(1):6–12.
Lin HC, Doty JE, Reedy TJ, et al. Inhibition of gastric emptying by sodium oleate depends on length of intestine exposed to nutrient. Am J Physiol. 1990;259(6 Pt 1):G1031–6.
Lin HC, Elashoff JD, Gu YG, et al. Nutrient feedback inhibition of gastric emptying plays a larger role than osmotically dependent duodenal resistance. Am J Physiol. 1993;265(4 Pt 1):G672–6.
Ma J, Stevens JE, Cukier K, et al. Effects of a protein preload on gastric emptying, glycemia, and gut hormones after a carbohydrate meal in diet-controlled type 2 diabetes. Diabetes Care. 2009;32(9):1600–2.
Bowen J, Noakes M, Trenerry C, et al. Energy intake, ghrelin, and cholecystokinin after different carbohydrate and protein preloads in overweight men. J Clin Endocrinol Metab. 2006;91(4):1477–83.
Gentilcore D, Chaikomin R, Jones KL, et al. Effects of fat on gastric emptying of and the glycemic, insulin, and incretin responses to a carbohydrate meal in type 2 diabetes. J Clin Endocrinol Metab. 2006;91(6):2062–7.
Asmar M. New physiological effects of the incretin hormones GLP-1 and GIP. Dan Med Bull. 2011;58(2):B4248.
Chapman MJ, Fraser RJL, Matthews G, et al. Glucose absorption and gastric emptying in critical illness. Crit Care. 2009;13:R140.
Read NW, Cammack J, Edwards C, et al. Is the transit time of a meal through the small intestine related to the rate at which it leaves the stomach? Gut. 1982;23(10):824–8.
Brennan IM, Luscombe-Marsh ND, Seimon RV, et al. Effects of fat, protein, and carbohydrate and protein load on appetite, plasma cholecystokinin, peptide YY, and ghrelin, and energy intake in lean and obese men. Am J Physiol Gastrointest Liver Physiol. 2012;303(1):G129–40.
Nguyen NQ, Game P, Bessell J, et al. Outcomes of Roux-en-Y gastric bypass and laparoscopic adjustable gastric banding. World J Gastroenterol: WJG. 2013;19(36):6035–43.
Pilichiewicz AN, Little TJ, Brennan IM, et al. Effects of load, and duration, of duodenal lipid on antropyloroduodenal motility, plasma CCK and PYY, and energy intake in healthy men. Am J Physiol Regul, Integr Comp Physiol. 2006;290(3):R668–77.
Little TJ, Doran S, Meyer JH, et al. The release of GLP-1 and ghrelin, but not GIP and CCK, by glucose is dependent upon the length of small intestine exposed. Am J Physiol Endocrinol Metab. 2006;291(3):E647–55.
Pilichiewicz AN, Papadopoulos P, Brennan IM, et al. Load-dependent effects of duodenal lipid on antropyloroduodenal motility, plasma CCK and PYY, and energy intake in healthy men. Am J Physiol Regul, Integr Comp Physiol. 2007;293(6):R2170–8.
Gentilcore D, Doran S, Meyer JH, et al. Effects of intraduodenal glucose concentration on blood pressure and heart rate in healthy older subjects. Dig Dis Sci. 2006;51(4):652–6.
Nguyen NQ, Mangoni AA, Fraser RJ, et al. Prokinetic therapy with erythromycin has no significant impact on blood pressure and heart rate in critically ill patients. Br J Clin Pharmacol. 2007;63(4):498–500.
Mallory GN, Macgregor AM, Rand CS. The Influence of Dumping on Weight Loss After Gastric Restrictive Surgery for Morbid Obesity. Obes Surg. 1996;6(6):474–8.
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 (Silver Spring). 2014;22(9):2003–9.
Nguyen NQ, Debreceni TL, Burgstad CM, Wishart JM, Bellon M, Rayner CK, et al. Effects of Posture and Meal Volume on Gastric Emptying, Intestinal Transit, Oral Glucose Tolerance, Blood Pressure and Gastrointestinal Symptoms After Roux-en-Y Gastric Bypass. Obes Surg. 2014. doi:10.1007/s11695-014-1531-4.
Edholm T, Cejvan K, Abdel-Halim SM, et al. The incretin hormones GIP and GLP-1 in diabetic rats: effects on insulin secretion and small bowel motility. Neurogastroenterol Motil: Off J Eur Gastrointest Motil Soc. 2009;21(3):313–21.
Ogawa E, Hosokawa M, Harada N, et al. The effect of gastric inhibitory polypeptide on intestinal glucose absorption and intestinal motility in mice. Biochem Biophys Res Commun. 2011;404(1):115–20.
Gunnerud UJ, Heinzle C, Holst JJ, Ostman EM, Bjorck IM. Effects of pre-meal drinks with protein and amino acids on glycemic and metabolic responses at a subsequent composite meal. PLoS One. 2012;7(9):e44731.
Akhavan T, Luhovyy BL, Brown PH, Cho CE, Anderson GH. Effect of premeal consumption of whey protein and its hydrolysate on food intake and postmeal glycemia and insulin responses in young adults. The American journal of clinical nutrition. 2010;91(4):966–75.
Vollmer K, Gardiwal H, Menge BA, et al. Hyperglycemia acutely lowers the postprandial excursions of glucagon-like Peptide-1 and gastric inhibitory polypeptide in humans. J Clin Endocrinol Metab. 2009;94(4):1379–85.
Laurenius A, Olbers T, Naslund I, et al. Dumping syndrome following gastric bypass: validation of the dumping symptom rating scale. Obes Surg. 2013;23(6):740–55.
Gentilcore D, Hausken T, Meyer JH, et al. Effects of intraduodenal glucose, fat, and protein on blood pressure, heart rate, and splanchnic blood flow in healthy older subjects. Am J Clin Nutr. 2008;87(1):156–61.
Mehagnoul-Schipper DJ, Lenders JW, Willemsen JJ, et al. Sympathoadrenal activation and the dumping syndrome after gastric surgery. Clin Auton Res. 2000;10(5):301–8.
Saito A. Acute adaptational disturbances due to the imbalance of the autonomic nervous system. Tohoku J Exp Med. 1971;103(1):71–92.
Yamamoto H, Mori T, Tsuchihashi H, et al. A possible role of GLP-1 in the pathophysiology of early dumping syndrome. Dig Dis Sci. 2005;50(12):2263–7.
Umeda LM, Silva EA, Carneiro G, et al. Early improvement in glycemic control after bariatric surgery and its relationships with insulin, GLP-1 and glucagon secretion in type 2 diabetic patients. Obes Surg. 2011;21(7):896–901.
Jorgensen NB, Jacobsen SH, Dirsken C, et al. Acute and long-term effects of RYGB on glucose metabolism in subjects with Type 2 diabetes and normal glucose tolerance. Am J Physiol Endocrinol Metab. 2012;303(1):E122–31.
Carswell KA, Vincent RP, Belgaumakar AP, et al. The effect of bariatric surgery on intestinal absorption and transit time. Obes Surg. 2014;24(5):796–805.
Staniforth DH. Comparison of orocaecal transit times assessed by the lactulose/hydrogen and the sulphasalazine/sulphapyridine methods. Gut. 1989;30(7):978–82.
Acknowledgments
Research Support from the National Health and Medical Research Council (NHMRC). Recipient of a New Investigator Project Grant 2010-2013
Conflict of interest
Authors Nam Q Nguyen, Tamara L Debreceni, Carly M Burgstad, Melissa Neo, Max Bellon , Judith M Wishart, Scott Standfield, Dylan Bartholomeusz, Chris K Rayner, Gary Wittert, Michael Horowitz declare that they have no conflict of interest.
Compliance with Ethical Standards
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Informed Consent
Informed consent was obtained from all individual participants included in the study.
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Nguyen, N.Q., Debreceni, T.L., Burgstad, C.M. et al. Effects of Fat and Protein Preloads on Pouch Emptying, Intestinal Transit, Glycaemia, Gut Hormones, Glucose Absorption, Blood Pressure and Gastrointestinal Symptoms After Roux-en-Y Gastric Bypass. OBES SURG 26, 77–84 (2016). https://doi.org/10.1007/s11695-015-1722-7
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DOI: https://doi.org/10.1007/s11695-015-1722-7