Metabolic Mechanisms in Obesity and Type 2 Diabetes: Insights from Bariatric/Metabolic Surgery

Obesity Facts

Volumn 8, Issue 6, 2015, Pages 350-363

  Cətoi, Adriana Florinela ^a   Pârvu, Alina ^a   Mureşan, Adriana ^a   Busetto, Luca ^b  

^a IULIU HATIEGANU UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

Hyperinsulinemia; Incretins; Insulin resistance; Metabolic surgery; Obesity; Surgical food restriction; Type 2 diabetes

Indexed keywords

ALANINE; ANTIDIABETIC AGENT; BILE ACID; CHOLECYSTOKININ; FATTY ACID; GHRELIN; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; INCRETIN; INSULIN; LACTIC ACID; LIPOPROTEIN LIPASE; TRIACYLGLYCEROL;

BARIATRIC SURGERY; BILIOPANCREATIC BYPASS; DIET RESTRICTION; DISEASE COURSE; ENERGY EXPENDITURE; FATTY LIVER; FOOD INTAKE; GASTRECTOMY; GASTRIC BANDING; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HUMAN; HYPERGLYCEMIA; HYPERINSULINEMIA; INSULIN RELEASE; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TREATMENT; INTESTINE FLORA; LIVER WEIGHT; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OVERNUTRITION; PATHOGENESIS; PRIORITY JOURNAL; REMISSION; REVIEW; ROUX Y ANASTOMOSIS; SLEEVE GASTRECTOMY; WEIGHT REDUCTION; COMPLICATION; DIABETES MELLITUS, TYPE 2; GASTROINTESTINAL TRACT; HYPERINSULINISM; METABOLISM; MICROBIOLOGY;

BARIATRIC SURGERY; DIABETES MELLITUS, TYPE 2; GASTROINTESTINAL TRACT; HUMANS; HYPERINSULINISM; INSULIN; INSULIN RESISTANCE; OBESITY;

EID: 84947815284     PISSN: 16624025     EISSN: 16624033     Source Type: Journal    
DOI: 10.1159/000441259     Document Type: Review

References (100)

1. Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, Schoelles K: Bariatric surgery: a systematic review and meta-analysis. JAMA 2004; 292: 1724-1737.
2. Farag YMK, Gaballa MR: Diabesity: an overview of a rising epidemic. Nephrol Dial Transplant 2011; 26: 28-35.
3. Copəescu C: Metabolic surgery. Acta Endocrinol (Buc), 2013;IX:273-278.
4. Rubino F: From bariatric to metabolic surgery: definition of a new discipline and implications for clinical practice. Curr Atheroscler Rep 2013; 15: 369.
5. Buchwald H, Varco RL: Metabolic Surgery. New York, Grune and Stratton, 1978.
6. Rubino F, Schauer PR, Kaplan LM, Cummings DE: Metabolic surgery to treat type 2 diabetes: clinical outcomes and mechanisms of action. Annu Rev Med 2010; 61: 393-411.
7. Buchwald H, Estok R, Fahrbach K, et al: Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med 2009; 122: 248-256.
8. Dixon JB, O'Brien PE, Playfair J, et al: Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial. JAMA 2008; 299: 316-323.
9. Schauer PR, Kashyap SR, Wolski K, et al: Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med 2012; 26: 366: 1567-1576.
10. Mingrone G, Panunzi S, De Gaetano A, et al: Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med 2012; 26: 366: 1577-1585.
11. Ikramuddin S, Korner J, Lee WJ, et al: Roux-en-Y gastric bypass vs intensive medical management for the control of type 2 diabetes, hypertension, and hyperlipidemia. The Diabetes Surgery Study randomized clinical trial. JAMA 2013; 309: 2240-2249.
12. Müller-Stich BP, Senft JD, Warshkow R, et al: Surgical versus medical treatment of type 2 diabetes mellitus in nonseverely obese patients: a systematic review and meta-analysis. Ann Surg 2015; 261: 421-429.
13. Knop F, Taylor R: Mechanism of metabolic advantages after bariatric surgery. Diabetes Care 2013; 36(suppl 2):S287-291.
14. Lazar MA: How obesity causes diabetes: not a tall tale. Science 2005; 307: 373-375.
15. Taylor R: Type 2 diabetes: etiology and reversibility. Diabetes Care 2013; 36: 1047-1055.
16. Taylor R: Pathogenesis of type 2 diabetes: tracing the reverse route from cure to cause. Diabetologia 2008; 51: 1781-1789.
17. Pories WJ, Dohm GL: Diabetes: have we got it all wrong? Hyperinsulinism as the culprit: surgery provides the evidence. Diabetes Care 2012; 35: 2438-2442.
18. Turner RC, Cull CA, Frighi V, Holman RR; UK Prospective Diabetes Study (UKPDS) Group: Glycemic control with diet, sulfonylurea, metformin, or insulin in patients with type 2 diabetes mellitus: progressive requirement for multiple therapies (UKPDS 49). JAMA 1999; 281: 2005-2012.
19. Petersen KF, Dufour S, Savage DB, et al: The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc Natl Acad Sci U S A 2007; 104: 12587-12594.
20. Taylor R: Insulin resistance and type 2 diabetes. Diabetes 2012; 61: 778-779.
21. Unger RH, Eisentraut AM: Entero-insular axis. Arch Intern Med 1969; 123: 261-266.
22. Creutzfeldt W: The incretin concept today. Diabetologia 1979; 16: 75-85.
23. Patriti A, Facchiano E, Sanna A, Gullà N, Donini A: The enteroinsular axis and the recovery from type 2 diabetes after bariatric surgery. Obes Surg 2004; 14: 840-848.
24. Frezza E: Are we closer to finding the treatment for type 2 diabetes mellitus in morbid obesity? Are the incretins the key to success? Obes Surg 2004; 14: 999-1005.
25. Gumbs AA, Modlin IM, Ballantyne GH: Changes in insulin resistance following bariatric surgery: role of caloric restriction and weight loss. Obes Surg 2005; 15: 462-473.
26. Ashrafian H, le Roux CW: Metabolic surgery and gut hormones - a review of bariatric entero-humoral modulation. Physiol Behav 2009; 97: 620-631.
27. Perfetti R, Zhou J, Doyle ME, Egan JM: Glucagon-like peptide-I induces cell proliferation and pancreatic-duodenum homeobox-1 expression and increases endocrine cell mass in the pancreas of old, glucose-intolerant rats. Endocrinology 2000; 141: 4600-4605.
28. Drucker DJ: Glucagon-like peptides: regulators of cell proliferation, differentiation, and apoptosis. Mol Endo-crinol 2003; 17: 161-171.
29. Mingrone G: Role of the incretin system in the remission of type 2 diabetes following bariatric surgery. Nutr Metab Cardiovasc Dis 2008; 18: 574-579.
30. Baggio LL, Drucker DJ: Biology of incretins: GLP-1 and GIP. Gastroenterology 2007; 132: 2131-2157.
31. Roberge JN, Gronau KA, Brubaker PL: Gastrin-releasing peptide is a novel mediator of proximal nutrient-induced proglucagon-derived peptide secretion from the distal gut. Endocrinology 1996; 137: 2383-2388.
32. Lugari R, Dei Cas A, Ugolotti D, et al: Evidence for early impaired of glucagon-like peptide 1-induced insulin secretin in human type 2 (non insulin-dependent) diabetes. Horm Metab Res 2002; 34: 150-154.
33. Mannucci E, Ognibene A, Cremasco F, et al: Glucagon-like peptide (GLP)-1 and leptin concentrations in obese patients with type 2 diabetes mellitus. Diab Med 2000; 17: 713-719.
34. Vilsbøll T, Krarup T, Deacon CF, Madsbad S, Holst JJ: Reduced postprandial concentrations of intact biologically active glucagon-like peptide 1 in type 2 diabetic patients. Diabetes 2001; 50: 609-613.
35. Fetner R, McGinty J, Russell C, Pi-Sunyer FX, Laferrère B: Incretins, diabetes, and bariatric surgery: a review. Surg Obes Relat Dis 2005; 16: 589-597.
36. Preitner F, Ibberson M, Franklin I, et al: Glucoincretins control insulin secretion at multiple levels as revealed in mice lacking GLP-1 and GIP receptors. J Clin Invest 2004; 113: 635-645.
37. Pories WJ: Why does the gastric bypass control type 2 diabetes mellitus? Obes Surg 2002; 2: 303-313.
38. Pories WJ, Swanson MS, MacDonald KG, et al: Who would have thought it? An operation proves to be the most effective therapy for adult-onset diabetes mellitus. Ann Surg 1995; 222: 339-350.
39. Angrisani L, Santonicola A, Iovino P, et al: Bariatric surgery worldwide 2013. Obes Surg 2015; 25: 1822-1832.
40. Rubino F, Schauer PR, Kaplan LM, Cummings DE: Metabolic surgery to treat type 2 diabetes: clinical outcomes and mechanisms of action. Annu Rev Med 2010; 61: 393-411.
41. Gass M, Beglinger C, Peterli R. Metabolic surgery - principles and current concepts. Langenbecks Arch Surg 2011; 396: 949-972.
42. Copəescu C: Laparoscopic gastric plication at the greater curvature (for treatment of morbid obesity). Chirurgia (Bucur) 2011; 106: 91-97.
43. Bradnova O, Kyrou I, Hainer V, et al: Laparoscopic greater curvature plication in morbidly obese women with type 2 diabetes: effects on glucose homeostasis, postprandial triglyceridemia and selected gut hormones. Obes Surg 2014;24:718-726.
44. Isbell JM, Tamboli RA, Hansen EN, et al: The importance of caloric restriction in the early improvements in insulin sensitivity after Roux-en-Y gastric bypass surgery. Diabetes Care 2010; 33: 1438-1442.
45. Edholm D, Kullberg J, Haenni A, et al: Preoperative 4-week low-calorie diet reduces liver volume and intrahe-patic fat, and facilitates laparoscopic gastric bypass in morbidly obese. Obes Surg 2011; 21: 345-350.
46. Lewis MC, Phillips ML, Slavotinek JP, et al: Change in liver size and fat content after treatment with Optifast ® very low calorie diet. Obes Surg 2006; 16: 697-701.
47. Colles SL, Dixon JB, Marks P, Strauss BJ, O'Brien PE: Preoperative weight loss with a very-low-energy diet: quantitation of changes in liver and abdominal fat by serial imaging. Am J Clin Nutr 2006; 84: 304-311.
48. Lim EL, Hollingsworth KG, Aribisala BS, Chen MJ, Mathers JC, Taylor R: Reversal of type 2 diabetes: normalisation of beta cell function in association with decreased pancreas and liver triacylglycerol. Diabetologia 2011; 54:2506-2514.
49. Reed MA, Pories WJ, Chapman W, et al: Roux-en-Y gastric bypass corrects hyperinsulinemia implications for the remission of type 2 diabetes. J Clin Endocrinol Metab 2011; 96: 2525-2531.
50. Pories WJ, Albrecht RJ: Etiology of type II diabetes mellitus: role of the foregut. World J Surg 2001; 25: 527-531.
51. Rubino F, Gagner M: Potential of surgery for curing type 2 diabetes mellitus. Ann Surg 2002; 236: 554-559.
52. Rubino F, Forgione A, Cummings DE, et al: The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes. Ann Surg 2006; 244: 741-749.
53. Rubino F, Marescaux J: Effect of duodenal-jejunal exclusion in a nonobese animal model of type 2 diabetes: a new perspective for an old disease. Ann Surg 2004; 239: 1-11.
54. Rubino F, Zizzari P, Tomasetto C, et al: The role of the small bowel in the regulation of circulating ghrelin levels and food intake in the obese Zucker rat. Endocrinology 2005; 146: 1745-1751.
55. Pacheco D, de Luis DA, Romero A, et al: The effects of duodenal-jejunal exclusion on hormonal regulation of glucose metabolism in Goto-Kakizaki rats. Am J Surg 2007; 194: 221-224.
56. Cohen RV, Schiavon CA, Pinheiro JS, Correa J Luiz, Rubino F: Duodenal-jejunal bypass for the treatment of type 2 diabetes in patients with BMI 22-34: a report of two cases. Surg Obes Relat Dis 2007; 3: 195-197.
57. Dixon JB: Obesity and diabetes: the impact of bariatric surgery on type-2 diabetes. World J Surg 2009; 33: 2014-2021.
58. Thaler JP, Cummings DE: Minireview: hormonal and metabolic mechanisms of diabetes remission after gastrointestinal surgery. Endocrinology 2009; 150: 2518-2525.
59. Laferrère B, Heshka S, Wang K, 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: 1709-1716.
60. Usinger L, Hansen KB, Kristiansen VB, Larsen S, Holst JJ, Knop FK: Gastric emptying of orally administered glucose solutions and incretin hormone responses are unaffected by laparoscopic adjustable gastric banding. Obes Surg 2011; 21: 625-632.
61. Korner J, Bessler M, Inabnet W, Taveras C, Holst JJ: Exaggerated glucagon-like peptide-1 and blunted glucose-dependent insulinotropic peptide secretion are associated with Roux-en-Y gastric bypass but not adjustable gastric banding. Surg Obes Relat Dis 2007; 3: 597-601.
62. Ye J, Hao Z, Mumphrey MB, et al: GLP-1 receptor signaling is not required for reduced body weight after RYGB in rodents. Am J Physiol Regul Integr Comp Physiol 2014;306:R352-362.
63. Peterli R, Steinert RE, Woelnerhanssen B, et al: Metabolic and hormonal changes after laparoscopic Roux-en-Y gastric bypass and sleeve gastrectomy: a randomized, prospective trial. Obes Surg 2012; 22: 740-748.
64. Dixon JB, Lambert EA, Lambert GW: Neuroendocrine adaptations to bariatric surgery. Mol Cell Endocrinol 2015; doi: 10.1016/j.mce.2015.05.033.
65. Ma H, Patti ME: Bile acids, obesity, and the metabolic syndrome. Best Pract Res Clin Gastroenterol 2014; 28: 573-583.
66. Sweeney TE, Morton JM: Metabolic surgery: action via hormonal milieu changes, changes in bile acids or gut microbiota? A summary of the literature. Best Pract Res Clin Gastroenterol 2014; 28: 727-740.
67. Argyropoulos G: Bariatric surgery: prevalence, predictors, and mechanisms of diabetes remission. Curr Diab Rep 2015; 15: 15.
68. Thomas C, Pellicciari R, Pruzanski M, Auwerx J, Schoonjans K: Targeting bile-acid signalling for metabolic diseases. Nat Rev Drug Discov 2008; 7: 678-693.
69. Han SI, Studer E, Gupta S, et al: Bile acids enhance the activity of the insulin receptor and glycogen synthase in primary rodent hepatocytes. Hepatology 2004; 39: 456-463.
70. Pournaras DJ, Glicksman C, Vincent RP, et al: The role of bile after Roux-en-Y gastric bypass in promoting weight loss and improving glycaemic control. Endocrinology 2012; 153: 3613-3619.
71. Chiang JY: Bile acids: regulation of synthesis. J Lipid Res 2009;50:1955-1966.
72. Lee FY, Lee H, Hubbert ML, Edwards PA, Zhang Y: FXR, a multipurpose nuclear receptor. Trends Biochem Sci 2006; 31: 572-580.
73. Pols TW, Noriega LG, Nomura M, Auwerx J, Schoonjans K: The bile acid membrane receptor TGR5 as an emerging target in metabolism and inflammation. J Hepatol 2011; 54: 1263-1272.
74. Shaham O, Wei R, Wang TJ, et al: Metabolic profiling of the human response to a glucose challenge reveals distinct axes of insulin sensitivity. Mol Syst Biol 2008; 4: 214.
75. Haeusler RA, Astiarraga B, Camastra S, Accili D, Ferrannini E: Human insulin resistance is associated with increased plasma levels of 12α-hydroxylated bile acids. Diabetes 2013; 62: 4184-4191.
76. Ahmad NN, Pfalzer A, Kaplan LM: Roux-en-Y gastric bypass normalizes the blunted postprandial bile acid excursion associated with obesity. Int J Obes (Lond) 2013; 37: 1553-1559.
77. Gerhard GS, Styer AM, Wood GC, et al: A role for fibroblast growth factor 19 and bile acids in diabetes remission after Roux-en-Y gastric bypass. Diabetes Care 2013; 36: 1859-1864.
78. Penney NC, Kinross JM, Newton RC, Purkayastha S: The role of bile acids in reducing the metabolic complications of obesity after bariatric surgery: A systematic review. Int J Obes 2015; doi: 10.1038/ijo.2015.115.
79. Steinert RE, Peterli R, Keller S, et al: Bile acids and gut peptide secretion after bariatric surgery: a 1-year prospective randomized pilot trial. Obesity (Silver Spring) 2013; 21:E660-E668.
80. Patti ME, Houten SM, Bianco AC, et al: Serum bile acids are higher in humans with prior gastric bypass: potential contribution to improved glucose and lipid metabolism. Obesity (Silver Spring) 2009; 17: 1671-1677.
81. Kohli R, Bradley D, Setchell KD, et al: Weight loss induced by Roux-en-Y gastric bypass but not laparoscopic adjustable gastric banding increases circulating bile acids. J Clin Endocrinol Metab 2013; 98:E708-E712.
82. Laferrere B: Gut feelings about diabetes. Endocrinol Nutr. 2012; 59: 254-260.
83. Kerr CA, Grice DM, Tran CD, et al: Early life events influence whole-of-life metabolic health via gut microflora and gut permeability. Crit Rev Microbiol 2015; 41: 326-240.
84. Luckey TD: Introduction to the ecology of the intestinal flora. Am J Clin Nutr 1970; 23: 1430-1432.
85. Sweeney TE, Morton JM: The human gut microbiome: a review of the effect of obesity and surgically induced weight loss. JAMA Surg 2013; 148: 563-569.
86. Kootte RS, Vrieze A, Holleman F, et al: The therapeutic potential of manipulating gut microbiota in obesity and type 2 diabetes mellitus. Diabetes Obes Metab 2012; 14: 112-120.
87. Tremaroli V, Backhed F: Functional interactions between the gut microbiota and host metabolism. Nature 2012;489:242-249.
88. Cox, AJ, West NP, Cripps AW: Obesity, inflammation, and the gut microbiota. Lancet Diabetes Endocrinol 2015; 3: 207-215.
89. Ley RE, Turnbaugh PJ, Klein S, Gordon JI: Microbial ecology: human gut microbes associated with obesity. Nature 2006; 444: 1022-1023.
90. Aron-Wisnewsky J, Doré J, Clement K: The importance of the gut microbiota after bariatric surgery. Nat Rev Gastroenterol Hepatol 2012; 9: 590-598.
91. Liou AP, Paziuk M, Luevano JM Jr, et al: Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med 2013; 5: 178ra141.
92. Furet JP, Kong LC, Tap J, et al: Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 2010; 59: 3049-3057.
93. Zhang H, Di Baise JK, Zuccolo A, et al: Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A 2009; 106: 2365-2370.
94. Graessler J, Qin Y, Zhong H, et al: Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: correlation with inflammatory and metabolic parameters. Pharmacogenomics J 2013; 13: 514-522.
95. Osto M, Abegg K, Bueter M, et al: Roux-en-Y gastric bypass surgery in rats alters gut microbiota profile along the intestine. Physiol Behav 2013; 119: 92-96.
96. David LA, Maurice CF, Carmody RN, et al: Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014; 505: 559-563.
97. Vrieze A, Out C, Fuentes S, et al: Impact of oral vancomycin on gut microbiota, bile acid metabolism, and insulin sensitivity. J Hepatol 2014; 60: 824-831.
98. Ribaric G, Buchwald JN, McGlennon TW: Diabetes and weight in comparative studies of bariatric surgery vs conventional medical therapy: a systematic review and meta-analysis. Obes Surg 2014; 24: 437-455.
99. Terranova L, Busetto L, Vestri A, Zappa MA: Bariatric surgery: cost-effectiveness and budget impact. Obes Surg 2012; 22: 646-653.
100. Sane T, Pekkarinen T, Jaser N, Juuti A, Virtanen L, Leivonen M: The effect of gastric sleeve and bypass surgery on the use and costs of medications for type 2 diabetes. Duodecim 2013; 129: 1590-1597.