Insulin secretion in healthy subjects and patients with Type 2 diabetes - role of the gastrointestinal tract

Best Practice and Research: Clinical Endocrinology and Metabolism

Volumn 23, Issue 4, 2009, Pages 413-424

  Ma, Jing ^a,b   Rayner, Christopher K ^a,b   Jones, Karen L ^a,b   Horowitz, Michael ^a,b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b NHMRC Centre of Clinical Research Excellence in Nutritional Physiology   (Australia)

Author keywords

gastric emptying; GIP; GLP 1; incretin hormones

Indexed keywords

ACARBOSE; CHOLECYSTOKININ; DIPEPTIDYL PEPTIDASE IV; DIPEPTIDYL PEPTIDASE IV INHIBITOR; EXENDIN 4; GASTRIC INHIBITORY POLYPEPTIDE; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 [7-36] AMIDE; GLUCAGON LIKE PEPTIDE 1 DERIVATIVE; GLUCOSE; GLUCOSE TRANSPORTER 2; GLUCOSE TRANSPORTER 5; INSULIN; LIRAGLUTIDE; METFORMIN; ORAL ANTIDIABETIC AGENT; PEPTIDE YY; PRAMLINTIDE; SITAGLIPTIN; SODIUM GLUCOSE COTRANSPORTER 1; SULFONYLUREA DERIVATIVE; VILDAGLIPTIN;

DIET SUPPLEMENTATION; DIETARY FIBER; DRUG EFFICACY; DRUG MECHANISM; ENZYMATIC DEGRADATION; GASTROINTESTINAL ABSORPTION; GASTROINTESTINAL TRACT FUNCTION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLYCEMIC CONTROL; HORMONE ACTION; HORMONE RESPONSE; HUMAN; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; INTESTINE FUNCTION; LOW CARBOHYDRATE DIET; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; POSTPRANDIAL STATE; PROTEIN DIET; PROTEIN EXPRESSION; REVIEW; STOMACH EMPTYING;

BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 2; DIETARY CARBOHYDRATES; GASTRIC EMPTYING; GASTROINTESTINAL TRACT; HUMANS; INCRETINS; INSULIN; INTESTINE, SMALL;

EID: 69849097361     PISSN: 1521690X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.beem.2009.03.009     Document Type: Review

References (98)

1. Del Prato S. In search of normoglycaemia in diabetes: controlling postprandial glucose. International Journal of Obesity and Related Metabolic Disorders 26 Suppl. 3 (2002) S9-S17
2. Ceriello A., Hanefeld M., Leiter L., et al. Postprandial glucose regulation and diabetic complications. Archives of Internal Medicine 164 (2004) 2090-2095
3. Nathan D.M., Cleary P.A., Backlund J.Y., et al. Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. The New England Journal of Medicine 353 (2005) 2643-2653
4. The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The New England Journal of Medicine 329 (1993) 977-986
5. UK Prospective Diabetes Study (UKPDS) Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352 (1998) 837-853
6. American Diabetes Association. Postprandial blood glucose. Diabetes Care 24 (2001) 775-778
7. Perley M.J., and Kipnis D.M. Plasma insulin responses to oral and intravenous glucose: studies in normal and diabetic sujbjects. The Journal of Clinical Investigation 46 (1967) 1954-1962
8. Horowitz M., and Nauck M.A. To be or not to be-an incretin or enterogastrone?. Gut 55 (2006) 148-150
9. Deacon C.F. What do we know about the secretion and degradation of incretin hormones?. Regulatory Peptides 128 (2005) 117-124
10. Drucker D.J. The biology of incretin hormones. Cell Metabolism 3 (2006) 153-165
11. Brener W., Hendrix T.R., and McHugh P.R. Regulation of the gastric emptying of glucose. Gastroenterology 85 (1983) 76-82
12. Schirra J., Houck P., Wank U., et al. Effects of glucagon-like peptide-1 (7-36)amide on antro-pyloro-duodenal motility in the interdigestive state and with duodenal lipid perfusion in humans. Gut 46 (2000) 622-631
13. Schirra J., Nicolaus M., Roggel R., et al. Endogenous glucagon-like peptide 1 controls endocrine pancreatic secretion and antro-pyloro-duodenal motility in humans. Gut 55 (2006) 243-251
14. MacIntosh C.G., Andrews J.M., Jones K.L., et al. Effects of age on concentrations of plasma cholecystokinin, glucagon-like peptide 1, and peptide YY and their relation to appetite and pyloric motility. The American Journal of Clinical Nutrition 69 (1999) 999-1006
15. Horowitz M., Edelbroek M.A., Wishart J.M., et al. Relationship between oral glucose tolerance and gastric emptying in normal healthy subjects. Diabetologia 36 (1993) 857-862
16. Jones K.L., Horowitz M., Carney B.I., et al. Gastric emptying in early noninsulin-dependent diabetes mellitus. Journal of Nuclear Medicine 37 (1996) 1643-1648
17. Gonlachanvit S., Hsu C.W., Boden G.H., et al. Effect of altering gastric emptying on postprandial plasma glucose concentrations following a physiologic meal in type-II diabetic patients. Digestive Diseases and Sciences 48 (2003) 488-497
18. Ishii M., Nakamura T., Kasai F., et al. Altered postprandial insulin requirement in IDDM patients with gastroparesis. Diabetes Care 17 (1994) 901-903
19. Olausson E.A., Alpsten M., Larsson A., et al. Small particle size of a solid meal increases gastric emptying and late postprandial glycaemic response in diabetic subjects with gastroparesis. Diabetes Research and Clinical Practice 80 (2008) 231-237
20. Pilichiewicz A.N., Chaikomin R., Brennan I.M., et al. Load-dependent effects of duodenal glucose on glycemia, gastrointestinal hormones, antropyloroduodenal motility, and energy intake in healthy men. American Journal of Physiology. Endocrinology and Metabolism 293 (2007) E743-E753
21. Bruce D.G., Chisholm D.J., Storlien L.H., et al. Physiological importance of deficiency in early prandial insulin secretion in non-insulin-dependent diabetes. Diabetes 37 (1988) 736-744
22. Gerich J.E. Pathogenesis and treatment of type 2 (noninsulin-dependent) diabetes mellitus (NIDDM). Hormone and Metabolic Research 28 (1996) 404-412
23. O'Donovan D.G., Doran S., Feinle-Bisset C., et al. Effect of variations in small intestinal glucose delivery on plasma glucose, insulin, and incretin hormones in healthy subjects and type 2 diabetes. The Journal of Clinical Endocrinology and Metabolism 89 (2004) 3431-3435
24. Chaikomin R., Doran S., Jones K.L., et al. Initially more rapid small intestinal glucose delivery increases plasma insulin, GIP, and GLP-1 but does not improve overall glycemia in healthy subjects. American Journal of Physiology. Endocrinology and Metabolism 289 (2005) E504-E507
25. Duchman S.M., Ryan A.J., Schedl H.P., et al. Upper limit for intestinal absorption of a dilute glucose solution in men at rest. Medicine and Science in Sports and Exercise 29 (1997) 482-488
26. Rayner C.K., Schwartz M.P., van Dam P.S., et al. Small intestinal glucose absorption and duodenal motility in type 1 diabetes mellitus. The American Journal of Gastroenterology 97 (2002) 3123-3130
27. Schwartz M.P., Samsom M., Renooij W., et al. Small bowel motility affects glucose absorption in a healthy man. Diabetes Care 25 (2002) 1857-1861
28. Nguyen H.N., Silny J., Wuller S., et al. Chyme transport patterns in human duodenum, determined by multiple intraluminal impedancometry. The American Journal of Physiology 268 (1995) G700-G708
29. Imam H., Sanmiguel C., Larive B., et al. Study of intestinal flow by combined videofluoroscopy, manometry, and multiple intraluminal impedance. The American Journal of Physiology. Gastrointestinal and Liver Physiology 286 (2004) G263-G270
30. Chaikomin R., Wu K.L., Doran S., et al. Concurrent duodenal manometric and impedance recording to evaluate the effects of hyoscine on motility and flow events, glucose absorption, and incretin release. The American Journal of Physiology. Gastrointestinal and Liver Physiology 292 (2007) G1099-G1104
31. Camilleri M., and Malagelada J.R. Abnormal intestinal motility in diabetics with the gastroparesis syndrome. European Journal of Clinical Investigation 14 (1984) 420-427
32. Samsom M., and Verhagen M.A. Intestinal function. In: Horowitz M., and Samsom M. (Eds). Gastrointestinal Function in Diabetes Mellitus (2004), John Wiley & Sons Ltd, Chichester 177-217
33. Fujita Y., Kojima H., Hidaka H., et al. Increased intestinal glucose absorption and postprandial hyperglycaemia at the early step of glucose intolerance in Otsuka Long-Evans Tokushima fatty rats. Diabetologia 41 (1998) 1459-1466
34. Cheeseman C.I., and Maenz D.D. Rapid regulation of D-glucose transport in basolateral membrane of rat jejunum. The American Journal of Physiology 256 (1989) G878-G883
35. Csaky T.Z., and Fischer E. Induction of an intestinal epithelial sugar transport system by high blood sugar. Experientia 33 (1977) 223-224
36. Csaky T.Z., and Fischer E. Intestinal sugar transport in experimental diabetes. Diabetes 30 (1981) 568-574
37. Fischer E., and Lauterbach F. Effect of hyperglycaemia on sugar transport in the isolated mucosa of guinea-pig small intestine. The Journal of Physiology 355 (1984) 567-586
38. Costrini N.V., Ganeshappa K.P., Wu W., et al. Effect of insulin, glucose, and controlled diabetes mellitus on human jejunal function. The American Journal of Physiology 233 (1977) E181-E187
39. Gulliford M.C., Bicknell E.J., Pover G.G., et al. Intestinal glucose and amino acid absorption in healthy volunteers and non-insulin-dependent diabetic subjects. The American Journal of Clinical Nutrition 49 (1989) 1247-1251
40. Dyer J., Wood I.S., Palejwala A., et al. Expression of monosaccharide transporters in intestine of diabetic humans. American Journal of Physiology. Gastrointestinal and Liver Physiology 282 (2002) G241-G248
41. Schirra J., Katschinski M., Weidmann C., et al. Gastric emptying and release of incretin hormones after glucose ingestion in humans. The Journal of Clinical Investigation 97 (1996) 92-103
42. Kuo P., Chaikomin R., Pilichiewicz A., et al. Transient, early release of glucagon-like peptide-1 during low rates of intraduodenal glucose delivery. Regulatory Peptides 146 (2008) 1-3
43. Rocca A.S., and Brubaker P.L. Role of the vagus nerve in mediating proximal nutrient-induced glucagon-like peptide-1 secretion. Endocrinology 140 (1999) 1687-1694
44. Nauck M.A., Bartels E., Orskov C., et al. Additive insulinotropic effects of exogenous synthetic human gastric inhibitory polypeptide and glucagon-like peptide-1-(7-36) amide infused at near-physiological insulinotropic hormone and glucose concentrations. The Journal of Clinical Endocrinology and Metabolism 76 (1993) 912-917
45. Nauck M.A., Heimesaat M.M., Orskov C., et al. Preserved incretin activity of glucagon-like peptide 1 [7-36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. The Journal of Clinical Investigation 91 (1993) 301-307
46. Theodorakis M.J., Carlson O., Michopoulos S., et al. Human duodenal enteroendocrine cells: source of both incretin peptides, GLP-1 and GIP. American Journal of Physiology. Gastrointestinal and Liver Physiology 290 (2006) E550-E559
47. Little T.J., Doran S., Meyer J.H., 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. American Journal of Physiology. Gastrointestinal and Liver Physiology 291 (2006) E647-E655
48. Herrmann C., Goke R., Richter G., et al. Glucagon-like peptide-1 and glucose-dependent insulin-releasing polypeptide plasma levels in response to nutrients. Digestion 56 (1995) 117-126
49. Elliott R.M., Morgan L.M., Tredger J.A., et al. Glucagon-like peptide-1 (7-36)amide and glucose-dependent insulinotropic polypeptide secretion in response to nutrient ingestion in man: acute post-prandial and 24-h secretion patterns. The Journal of Endocrinology 138 (1993) 159-166
50. Bowen J., Noakes M., and Clifton P.M. Appetite regulatory hormone responses to various dietary proteins differ by body mass index status despite similar reductions in ad libitum energy intake. The Journal of Clinical Endocrinology and Metabolism 91 (2006) 2913-2919
51. Rayner C.K., Park H.S., Wishart J.M., et al. Effects of intraduodenal glucose and fructose on antropyloric motility and appetite in healthy humans. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 278 (2000) R360-R366
52. Horowitz M., Wishart J.M., Jones K.L., et al. Gastric emptying in diabetes: an overview. Diabetic Medicine 13 (1996) S16-S22
53. Frank J.W., Saslow S.B., Camilleri M., et al. Mechanism of accelerated gastric emptying of liquids and hyperglycemia in patients with type II diabetes mellitus. Gastroenterology 109 (1995) 755-765
54. Phillips W.T., Schwartz J.G., and McMahan C.A. Rapid gastric emptying of an oral glucose solution in type 2 diabetic patients. Journal of Nuclear Medicine 33 (1992) 1496-1500
55. Schwartz J.G., Green G.M., Guan D., et al. Rapid gastric emptying of a solid pancake meal in type II diabetic patients. Diabetes Care 19 (1996) 468-471
56. Jones K.L., Russo A., Berry M.K., et al. A longitudinal study of gastric emptying and upper gastrointestinal symptoms in patients with diabetes mellitus. The American Journal of Medicine 113 (2002) 449-455
57. Krarup T. Immunoreactive gastric inhibitory polypeptide. Endocrine Reviews 9 (1988) 122-134
58. Elahi D., McAloon-Dyke M., Fukagawa N.K., et al. The insulinotropic actions of glucose-dependent insulinotropic polypeptide (GIP) and glucagon-like peptide-1 (7-37) in normal and diabetic subjects. Regulatory Peptides 51 (1994) 63-74
59. Vilsboll T., Krarup T., Madsbad S., et al. Defective amplification of the late phase insulin response to glucose by GIP in obese type II diabetic patients. Diabetologia 45 (2002) 1111-1119
60. Lynn F.C., Pamir N., Ng E.H., et al. Defective glucose-dependent insulinotropic polypeptide receptor expression in diabetic fatty Zucker rats. Diabetes 50 (2001) 1004-1011
61. Meier J.J., Hucking K., Holst J.J., et al. Reduced insulinotropic effect of gastric inhibitory polypeptide in first-degree relatives of patients with type 2 diabetes. Diabetes 50 (2001) 2497-2504
62. Vilsboll T., Knop F.K., Krarup T., et al. The pathophysiology of diabetes involves a defective amplification of the late-phase insulin response to glucose by glucose-dependent insulinotropic polypeptide-regardless of etiology and phenotype. The Journal of Clinical Endocrinology and Metabolism 88 (2003) 4897-4903
63. Toft-Nielsen M.B., Damholt M.B., Madsbad S., et al. Determinants of the impaired secretion of glucagon-like peptide-1 in type 2 diabetic patients. The Journal of Clinical Endocrinology and Metabolism 86 (2001) 3717-3723
64. Chandalia M., Garg A., Lutjohann D., et al. Beneficial effects of high dietary fiber intake in patients with type 2 diabetes mellitus. The New England Journal of Medicine 342 (2000) 1392-1398
65. Russo A., Stevens J.E., Wilson T., et al. Guar attenuates fall in postprandial blood pressure and slows gastric emptying of oral glucose in type 2 diabetes. Digestive Diseases and Sciences 48 (2003) 1221-1229
66. Cunningham K.M., and Read N.W. The effect of incorporating fat into different components of a meal on gastric emptying and postprandial blood glucose and insulin responses. The British Journal of Nutrition 61 (1989) 285-290
67. Feinle C., O'Donovan D., Doran S., et al. Effects of fat digestion on appetite, APD motility, and gut hormones in response to duodenal fat infusion in humans. American Journal of Physiology. Gastrointestinal and Liver Physiology 284 (2003) G798-G807
68. O'Donovan D., Horowitz M., Russo A., et al. Effects of lipase inhibition on gastric emptying of, and on the glycaemic, insulin and cardiovascular responses to, a high-fat/carbohydrate meal in type 2 diabetes. Diabetologia 47 (2004) 2208-2214
69. Gentilcore D., Chaikomin R., Jones K.L., et al. Effects of fat on gastric emptying of, and the glycemic, insulin and incretin responses to, a carbohydrate meal in type 2 diabetes. The Journal of Clinical Endocrinology and Metabolism 91 6 (2006) 2062-2067
70. Thompson R.G., Pearson L., and Kolterman O.G. Effects of 4 weeks' administration of pramlintide, a human amylin analogue, on glycaemia control in patients with IDDM: effects on plasma glucose profiles and serum fructosamine concentrations. Diabetologia 40 (1997) 1278-1285
71. Thompson R.G., Pearson L., Schoenfeld S.L., et al. Pramlintide, a synthetic analog of human amylin, improves the metabolic profile of patients with type 2 diabetes using insulin. The Pramlintide in type 2 diabetes group. Diabetes Care 21 (1998) 987-993
72. Singh-Franco D., Robles G., and Gazze D. Pramlintide acetate injection for the treatment of type 1 and type 2 diabetes mellitus. Clinical Therapeutics 29 (2007) 535-562
73. Aronne L., Fujioka K., Aroda V., et al. Progressive reduction in body weight after treatment with the amylin analog pramlintide in obese subjects: a phase 2, randomized, placebo-controlled, dose-escalation study. The Journal of Clinical Endocrinology and Metabolism 92 (2007) 2977-2983
74. Nauck M.A., Niedereichholz U., Ettler R., et al. Glucagon-like peptide 1 inhibition of gastric emptying outweighs its insulinotropic effects in healthy humans. The American Journal of Physiology 273 (1997) E981-E988
75. Little T.J., Pilichiewicz A.N., Russo A., et al. Effects of intravenous glucagon-like peptide-1 on gastric emptying and intragastric distribution in healthy subjects: relationships with postprandial glycemic and insulinemic responses. The Journal of Clinical Endocrinology and Metabolism 91 (2006) 1916-1923
76. Cervera A., Wajcberg E., Sriwijitkamol A., et al. Mechanism of action of exenatide to reduce postprandial hyperglycemia in type 2 diabetes. American Journal of Physiology. Endocrinology and Metabolism 294 (2008) E846-E852
77. Bischoff H. Pharmacology of alpha-glucosidase inhibition. European Journal of Clinical Investigation 24 Suppl. 3 (1994) 3-10
78. Qualmann C., Nauck M.A., Holst J.J., et al. Glucagon-like peptide 1 (7-36 amide) secretion in response to luminal sucrose from the upper and lower gut. A study using alpha-glucosidase inhibition (acarbose). Scandinavian Journal of Gastroenterology 30 (1995) 892-896
79. Ranganath L., Norris F., Morgan L., et al. Delayed gastric emptying occurs following acarbose administration and is a further mechanism for its anti-hyperglycaemic effect. Diabetic Medicine 15 (1998) 120-124
80. Hucking K., Kostic Z., Pox C., et al. Alpha-Glucosidase inhibition (acarbose) fails to enhance secretion of glucagon-like peptide 1 (7-36 amide) and to delay gastric emptying in type 2 diabetic patients. Diabetic Medicine 22 (2005) 470-476
81. Mourot J., Thouvenot P., Couet C., et al. Relationship between the rate of gastric emptying and glucose and insulin responses to starchy foods in young healthy adults. The American Journal of Clinical Nutrition 48 (1988) 1035-1040
82. Ou S., Kwok K., Li Y., et al. In vitro study of possible role of dietary fiber in lowering postprandial serum glucose. Journal of Agricultural and Food Chemistry 49 (2001) 1026-1029
83. Bjorck I., and Elmstahl H.L. The glycaemic index: importance of dietary fibre and other food properties. The Proceedings of the Nutrition Society 62 (2003) 201-206
84. Drucker D.J. The role of gut hormones in glucose homeostasis. The Journal of Clinical Investigation 117 (2007) 24-32
85. Fineman M.S., Bicsak T.A., Shen L.Z., et al. Effect on glycemic control of exenatide (synthetic exendin-4) additive to existing metformin and/or sulfonylurea treatment in patients with type 2 diabetes. Diabetes Care 26 (2003) 2370-2377
86. Ahren B. DPP-4 inhibitors. Best Practice & Research. Clinical Endocrinology & Metabolism 21 (2007) 517-533
87. Charbonnel B., Karasik A., Liu J., et al. Efficacy and safety of the dipeptidyl peptidase-4 inhibitor sitagliptin added to ongoing metformin therapy in patients with type 2 diabetes inadequately controlled with metformin alone. Diabetes Care 29 (2006) 2638-2643
88. Woerle H.J., Lindenberger T., Linke R., et al. A single dose of vildagliptin decelerates gastric emptying in patients with type 2 diabetes (Abstract). 67th Scientific Sessions of the American Diabetes Association (2007) 500-P
89. Vella A., Bock G., Giesler P.D., et al. Effects of dipeptidyl peptidase-4 inhibition on gastrointestinal function, meal appearance, and glucose metabolism in type 2 diabetes. Diabetes 56 (2007) 1475-1480
90. Gutierrez M., Akhavan M., Jovanovic L., et al. Utility of a short-term 25% carbohydrate diet on improving glycemic control in type 2 diabetes mellitus. Journal of the American College of Nutrition 17 (1998) 595-600
91. Stern L., Iqbal N., Seshadri P., et al. The effects of low-carbohydrate versus conventional weight loss diets in severely obese adults: one-year follow-up of a randomized trial. Annals of Internal Medicine 140 (2004) 778-785
92. Wolever T.M. Relationship between dietary fiber content and composition in foods and the glycemic index. The American Journal of Clinical Nutrition 51 (1990) 72-75
93. Gannon M.C., Nuttall F.Q., Saeed A., et al. An increase in dietary protein improves the blood glucose response in persons with type 2 diabetes. The American Journal of Clinical Nutrition 78 (2003) 734-741
94. Gannon M.C., Nuttall F.Q., Neil B.J., et al. The insulin and glucose responses to meals of glucose plus various proteins in type II diabetic subjects. Metabolism 37 (1988) 1081-1088
95. Karamanlis A., Chaikomin R., Doran S., et al. Effects of protein on glycemic and incretin responses and gastric emptying after oral glucose in healthy subjects. The American Journal of Clinical Nutrition 86 (2007) 1364-1368
96. Gunnarsson P.T., Winzell M.S., Deacon C.F., et al. Glucose-induced incretin hormone release and inactivation are differently modulated by oral fat and protein in mice. Endocrinology 147 (2006) 3173-3180
97. Ma J., Stevens J.E., Maddox A.F., et al. Effect of a protein preload on gastric emptying and glycaemia in type 2 diabetes (Abstract). Gastroenterology 134 (2008) A247-A248
98. Chaikomin R., Rayner C.K., Jones K.L., et al. Upper gastrointestinal function and glycemic control in diabetes mellitus. World Journal of Gastroenterology 12 (2006) 5611-5621