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Impact of gastric emptying and small intestinal transit on blood glucose, intestinal hormones, glucose absorption in the morbidly obese

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Abstract

Objective:

This study evaluated gastric emptying (GE) and small intestinal (SI) transit in people with morbid obesity and their relationships to glycaemia, incretin hormones, and glucose absorption

Methods:

GE and caecal arrival time (CAT) of a mixed meal were assessed in 22 morbidly obese (50.2 ± 2.5 years; 13 F:9 M; BMI: 48.6 ± 1.8 kg/m2) and 10 lean (38.6 ± 8.4 years; 5 F:5 M; BMI: 23.9 ± 0.7 kg/m2) subjects, using scintigraphy. Blood glucose, plasma 3-O-methylglucose, insulin, glucagon, glucose-dependent insulinotropic polypeptide (GIP) and glucagon-like peptide-1 (GLP-1) were measured. Insulin sensitivity and resistance were also quantified

Results:

When compared with lean subjects, GE (t50: 60.7 ± 6.5 vs. 41.1 ± 7.3 min; P  = 0.04) and CAT (221.5 ± 9.8 vs. 148.0 ± 7.1 min; P =  0.001) of solids were prolonged in morbid obesity. Postprandial rises in GIP (P = 0.001), insulin (P  = 0.02), glucose (P = 0.03) and 3-O-methylglucose (P = 0.001) were less. Whereas GLP-1 increased at 45 mins post-prandially in lean subjects, there was no increase in the obese (P  = 0.04). Both fasting (P = 0.045) and postprandial (P = 0.012) plasma glucagon concentrations were higher in the obese

Conclusions:

GE and SI transit are slower in the morbidly obese, and associated with reductions in postprandial glucose absorption, and glycaemic excursions, as well as plasma GIP and GLP-1

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References

  1. Wright RA, Krinsky S, Fleeman C, Trujillo J, Teague E. Gastric emptying and obesity. Gastroenterology. 1983;84:747–51.

    Article  CAS  PubMed  Google Scholar 

  2. Tosetti C, et al. Gastric emptying of solids in morbid obesity. Int J Obes Relat Metab Disord. 1996;20:200–5.

    CAS  PubMed  Google Scholar 

  3. Sasaki H, et al. Hyperinsulinemia in obesity: lack of relation to gastric emptying of glucose solution or to plasma somatostatin levels. Metabolism. 1983;32:701–5.

    Article  CAS  PubMed  Google Scholar 

  4. Barkin JS, Reiner DK, Goldberg RI, Phillips RS, Janowitz WR. The effects of morbid obesity and the Garren-Edwards gastric bubble on solid phase gastric emptying. Am J Gastroenterol. 1988;83:1364–7.

    CAS  PubMed  Google Scholar 

  5. Verdich C, et al. Effect of obesity and major weight reduction on gastric emptying. Int J Obes Relat Metab Disord. 2000;24:899–905.

    Article  CAS  PubMed  Google Scholar 

  6. Collins PJ, Horowitz M, Cook DJ, Harding PE, Shearman DJ. Gastric emptying in normal subjects--a reproducible technique using a single scintillation camera and computer system. Gut. 1983;24:1117–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Horowitz M, Collins PJ, Harding PE, Shearman DJ. Gastric emptying after gastric bypass. Int J Obes. 1986;10:117–21.

    CAS  PubMed  Google Scholar 

  8. Maddox A, Horowitz M, Wishart J, Collins P. Gastric and oesophageal emptying in obesity. Scand J Gastroenterol. 1989;24:593–8.

    Article  CAS  PubMed  Google Scholar 

  9. Jackson SJ, et al. Delayed gastric emptying in the obese: an assessment using the non-invasive (13)C-octanoic acid breath test. Diabetes Obes Metab. 2004;6:264–70.

    Article  CAS  PubMed  Google Scholar 

  10. Wisen O, Hellstrom PM. Gastrointestinal motility in obesity. J Intern Med. 1995;237:411–8.

    Article  CAS  PubMed  Google Scholar 

  11. Wisen O, Johansson C. Gastrointestinal function in obesity: motility, secretion, and absorption following a liquid test meal. Metabolism. 1992;41:390–5.

    Article  CAS  PubMed  Google Scholar 

  12. Mushref MA, Srinivasan S. Effect of high fat-diet and obesity on gastrointestinal motility. Ann Transl Med. 2013;1:14.

    PubMed  PubMed Central  Google Scholar 

  13. le Roux CW, Bueter M. The physiology of altered eating behaviour after Roux-en-Y gastric bypass. Exp Physiol. 2014;99:1128–32.

    Article  PubMed  Google Scholar 

  14. le Roux CW, et al. Gut hormones as mediators of appetite and weight loss after Roux-en-Y gastric bypass. Ann Surg. 2007;246:780–5.

    Article  PubMed  Google Scholar 

  15. Nguyen NQ, et al. Accelerated intestinal glucose absorption in morbidly obese humans: relationship to glucose transporters, incretin hormones, and glycemia. J Clin Endocrinol Metab. 2015;100:968–76.

    Article  CAS  PubMed  Google Scholar 

  16. Goy YM, Toumi Z, Date RS. Surgical cure for type 2 diabetes by foregut or hindgut operations: a myth or reality? A systematic review. Surg Endosc. 2017;31:25–37.

    Article  Google Scholar 

  17. Mingrone G, Castagneto-Gissey L. Mechanisms of early improvement/resolution of type 2 diabetes after bariatric surgery. Diabetes Metab. 2009;35:518–23.

    Article  CAS  PubMed  Google Scholar 

  18. Spector D, Shikora S. Neuro-modulation and bariatric surgery for type 2 diabetes mellitus. Int J Clin Pract Suppl. 2010;166:53–8.

    Article  Google Scholar 

  19. Kwon Y, et al. The foregut theory as a possible mechanism of action for the remission of type 2 diabetes in low body mass index patients undergoing subtotal gastrectomy for gastric cancer. Surg Obes Relat Dis. 2014;10:235–42.

    Article  PubMed  Google Scholar 

  20. O’Doherty M, Day A. Glycated haemoglobin and diagnosis of diabetes mellitus: now well established but beware the pitfalls. Ann Clin Biochem. 2016;53:309–11.

    Article  PubMed  Google Scholar 

  21. Nguyen NQ, et al. Upregulation of intestinal glucose transporters after Roux-en-Y gastric bypass to prevent carbohydrate malabsorption. Obes (Silver Spring). 2014;22:2164–71.

    Article  CAS  Google Scholar 

  22. Seimon RV, et al. Gastric emptying, mouth-to-cecum transit, and glycemic, insulin, incretin, and energy intake responses to a mixed-nutrient liquid in lean, overweight, and obese males. Am J Physiol Endocrinol Metab. 2013;304:E294–300.

    Article  CAS  PubMed  Google Scholar 

  23. Nguyen NQ, 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. 2016;26:77–84.

    Article  PubMed  Google Scholar 

  24. Nguyen NQ, 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. 2015;25:1392–400.

    Article  PubMed  Google Scholar 

  25. Dalla Man C, Caumo A, Cobelli C. The oral glucose minimal model: estimation of insulin sensitivity from a meal test. IEEE Trans Biomed Eng. 2002;49:419–29.

    Article  PubMed  Google Scholar 

  26. Dalla Man C, et al. Modeling hepatic insulin sensitivity during a meal: validation against the euglycemic hyperinsulinemic clamp. Am J Physiol Endocrinol Metab. 2013;304:E819–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Wolnerhanssen BK, et al. Gut hormone secretion, gastric emptying, and glycemic responses to erythritol and xylitol in lean and obese subjects. Am J Physiol Endocrinol Metab. 2016;310:E1053–61.

    Article  PubMed  Google Scholar 

  28. Andreazzi AE, et al. Impaired sympathoadrenal axis function contributes to enhanced insulin secretion in prediabetic obese rats. Exp Diabetes Res. 2011;2011:947917.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kruszynska YT, Olefsky JM, Frias JP. Effect of obesity on susceptibility to fatty acid-induced peripheral tissue insulin resistance. Metabolism. 2003;52:233–8.

    Article  CAS  PubMed  Google Scholar 

  30. le Roux CW, et al. Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann Surg. 2006;243:108–14.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Faerch K, et al. GLP-1 response to oral glucose is reduced in prediabetes, screen-detected type 2 diabetes, and obesity and influenced by sex: the ADDITION-PRO Study. Diabetes. 2015;64:2513–25.

    Article  CAS  PubMed  Google Scholar 

  32. Cecil JE, Francis J, Read NW. Comparison of the effects of a high-fat and high-carbohydrate soup delivered orally and intragastrically on gastric emptying, appetite, and eating behaviour. Physiol Behav. 1999;67:299–306.

    Article  CAS  PubMed  Google Scholar 

  33. Wijlens AG, Erkner A, Mars M, de Graaf C. Longer oral exposure with modified sham feeding does not slow down gastric emptying of low- and high-energy-dense gastric loads in healthy young men. J Nutr. 2015;145:365–71.

    Article  CAS  PubMed  Google Scholar 

  34. Corvilain B, et al. Effect of short-term starvation on gastric emptying in humans: relationship to oral glucose tolerance. Am J Physiol. 1995;269:G512–7.

    CAS  PubMed  Google Scholar 

  35. Kentish SJ, Ratcliff K, Li H, Wittert GA, Page AJ. High fat diet induced changes in gastric vagal afferent response to adiponectin. Physiol Behav. 2015;152:354–62.

    Article  CAS  PubMed  Google Scholar 

  36. Kentish SJ, Vincent AD, Kennaway DJ, Wittert GA, Page AJ. High-fat diet-induced obesity ablates gastric vagal afferent circadian rhythms. J Neurosci. 2016;36:3199–207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lavigne ME, Wiley ZD, Meyer JH, Martin P, MacGregor IL. Gastric emptying rates of solid food in relation to body size. Gastroenterology. 1978;74:1258–60.

    Article  CAS  PubMed  Google Scholar 

  38. Meyer-Gerspach AC, et al. Gastric and intestinal satiation in obese and normal weight healthy people. Physiol Behav. 2014;129:265–71.

    Article  CAS  PubMed  Google Scholar 

  39. van der Klaauw AA, et al. High protein intake stimulates postprandial GLP-1 and PYY release. Obes (Silver Spring). 2013;21:1602–7.

    Article  Google Scholar 

  40. Acosta A, et al. Quantitative gastrointestinal and psychological traits associated with obesity and response to weight-loss therapy. Gastroenterology. 2015;148:537–46.

    Article  PubMed  Google Scholar 

  41. Adam TC, Jocken J, Westerterp-Plantenga MS. Decreased glucagon-like peptide 1 release after weight loss in overweight/obese subjects. Obes Res. 2005;13:710–6.

    Article  CAS  PubMed  Google Scholar 

  42. Heden TD, et al. Liquid meal composition, postprandial satiety hormones, and perceived appetite and satiety in obese women during acute caloric restriction. Eur J Endocrinol. 2013;168:593–600.

    Article  CAS  PubMed  Google Scholar 

  43. Ranganath LR, et al. Attenuated GLP-1 secretion in obesity: cause or consequence? Gut. 1996;38:916–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Verdich C, et al. The role of postprandial releases of insulin and incretin hormones in meal-induced satiety--effect of obesity and weight reduction. Int J Obes Relat Metab Disord. 2001;25:1206–14.

    Article  CAS  PubMed  Google Scholar 

  45. Reaven GM, Chen YD, Golay A, Swislocki AL, Jaspan JB. Documentation of hyperglucagonemia throughout the day in nonobese and obese patients with noninsulin- dependent diabetes mellitus. J Clin Endocrinol Metab. 1987;64:106–10.

    Article  CAS  PubMed  Google Scholar 

  46. Kozawa J, et al. Early postprandial glucagon surge affects postprandial glucose levels in obese and non-obese patients with type 2 diabetes. Endocr J. 2013;60:813–8.

    Article  CAS  PubMed  Google Scholar 

  47. Henkel E, Menschikowski M, Koehler C, Leonhardt W, Hanefeld M. Impact of glucagon response on postprandial hyperglycemia in men with impaired glucose tolerance and type 2 diabetes mellitus. Metabolism. 2005;54:1168–73.

    Article  CAS  PubMed  Google Scholar 

  48. Ranganath LR, Beety JM, Morgan LM. Inhibition of insulin, glucose-dependent insulinotropic polypeptide (GIP) and glucagon-like peptide-1 (GLP-1) secretion by octreotide has no effect on post-heparin plasma lipoprotein lipase activity. Horm Metab Res. 1999;31:262–6.

    Article  CAS  PubMed  Google Scholar 

  49. Gu W, et al. Glucagon receptor antagonist-mediated improvements in glycemic control are dependent on functional pancreatic GLP-1 receptor. Am J Physiol Endocrinol Metab. 2010;299:E624–32.

    Article  CAS  PubMed  Google Scholar 

  50. Kazierad DJ, et al. Effects of multiple ascending doses of the glucagon receptor antagonist PF-06291874 in patients with type 2 diabetes mellitus. Diabetes Obes Metab. 2016;18:795–802.

    Article  CAS  PubMed  Google Scholar 

  51. Bennink R, et al. Comparison of total and compartmental gastric emptying and antral motility between healthy men and women. Eur J Nucl Med. 1998;25:1293–9.

    Article  CAS  PubMed  Google Scholar 

  52. Bennink R, 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.

    Article  CAS  PubMed  Google Scholar 

  53. Madsen JL, Graff J. Effects of ageing on gastrointestinal motor function. Age Ageing. 2004;33:154–9.

    Article  PubMed  Google Scholar 

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Correspondence to Nam Q Nguyen.

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Nguyen, N.Q., Debreceni, T.L., Burgess, J.E. et al. Impact of gastric emptying and small intestinal transit on blood glucose, intestinal hormones, glucose absorption in the morbidly obese. Int J Obes 42, 1556–1564 (2018). https://doi.org/10.1038/s41366-018-0012-6

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  • DOI: https://doi.org/10.1038/s41366-018-0012-6

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