Obesity Surgery

, Volume 27, Issue 3, pp 826–836 | Cite as

Mechanisms of Action of Surgical Interventions on Weight-Related Diseases: the Potential Role of Bile Acids

  • Mohsen Mazidi
  • Pedro Paulo P. de Caravatto
  • John R. Speakman
  • Ricardo V. Cohen
Review Article

Abstract

Surgical interventions for weight-related diseases (SWRD) may have substantial and sustainable effect on weight reduction, also leading to a higher remission rate of type 2 diabetes (T2D) mellitus than any other medical treatment or lifestyle intervention. The resolution of T2D after Roux-en-Y gastric bypass (RYGB) typically occurs too quickly to be accounted for by weight loss alone, suggesting that these operations have a direct impact on glucose homeostasis. The mechanisms underlying these beneficial effects however remain unclear. Recent research suggests that changes in the concentrations of plasma bile acids might contribute to these metabolic changes after surgery. In this review, we aimed to outline the potential role of bile acids in SWRD. We systematically reviewed MEDLINE, SCOPUS, and Web of Science for articles reporting the effect of SWRD on outcomes published between 1969 and 2016. We found that changes in circulating bile acids after surgery may play a major role through activation of the farnesoid X receptor A (FXRA), the fibroblast growth factor 19 (FGF19), and the G protein-coupled bile acid receptor (TGR5). Bile acid concentration increased significantly after RYGB. Some studies suggest that a transitory decrease occurs at 1 week post-surgery, followed by a gradual increase. Most studies have shown the increase to be proportionate by all bile acid subtypes. Bile acids can regulate glucose metabolism through the expression of TGR5 receptor in L cells, resulting in a release of glucagon-like peptide 1 (GLP-1). It may also induce the synthesis and secretion of FGF19 in ileal cells, thereby improving insulin sensitivity and regulating glucose metabolism. All the present SWRD are involved with changes in food stimulation to the stomach. This implies that discovering and developing the antagonists to TGR5 and FXRA may effectively control metabolic syndrome and the elucidation of the mechanisms underlying the physiological effects related to weight loss and T2D remission after surgery may help to identify new drug targets.

Keywords

Surgery of weight-related diseases RYGB Bile acids Mechanisms of action Metabolic surgery 

Supplementary material

11695_2017_2549_MOESM1_ESM.docx (14 kb)
ESM 1(DOCX 14 kb)

References

  1. 1.
    Chang SH, Stoll CR, Song J, et al. The effectiveness and risks of bariatric surgery: an updated systematic review and meta-analysis, 2003-2012. JAMA surgery. 2014;149(3):275–87.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Clifton PM. Bariatric surgery: results in obesity and effects on metabolic parameters. Curr Opin Lipidol. 2011;22(1):1–5.PubMedCrossRefGoogle Scholar
  3. 3.
    Eldar S, Heneghan HM, Brethauer SA, et al. Bariatric surgery for treatment of obesity. Int J Obes. 2005;35(Suppl 3):S16–21.Google Scholar
  4. 4.
    Fallahi-Shahabad S, Mazidi M, Tavasoli A, et al. Metabolic improvement of morbid obese patients following Roux-en-Y gastric bypass surgery: a prospective study in Mashhad. Iran Indian J Gastroenterol. 2016;35(3):195–200.PubMedCrossRefGoogle Scholar
  5. 5.
    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(7):1438–42.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Hajnal A, Kovacs P, Ahmed T, et al. Gastric bypass surgery alters behavioral and neural taste functions for sweet taste in obese rats. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2010;299(4):G967–G79.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Thanos PK, Subrize M, Delis F, et al. Gastric bypass increases ethanol and water consumption in diet-induced obese rats. Obes Surg. 2012;22(12):1884–92.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Roberts RE, Alaghband-Zadeh J, Le Roux CW. The role of bile acids in gut-hormone-induced weight loss after bariatric surgery: implications for appetite control and diabetes. Handbook of behavior, food and nutrition. Berlin: Springer; 2011. p. 1317–30.Google Scholar
  9. 9.
    Verdich C, Flint A, Gutzwiller JP, et al. A meta-analysis of the effect of glucagon-like peptide-1 (7-36) amide on ad libitum energy intake in humans. J Clin Endocrinol Metab. 2001;86(9):4382–9.PubMedGoogle Scholar
  10. 10.
    Mohsen Mazidi EK, Peyman rezaie, Ferns GA. Treatment with GLP1 receptor agonists reduce serum CRP concentrations in patients with type 2 diabetes mellitus: a systematic review and meta-analysis of randomized controlled trials. Journal of Diabetes and Its Complications. 2016.Google Scholar
  11. 11.
    Holst JJ, Deacon CF. Inhibition of the activity of dipeptidyl-peptidase IV as a treatment for type 2 diabetes. Diabetes. 1998;47(11):1663–70.PubMedCrossRefGoogle Scholar
  12. 12.
    Deacon CF, Holst JJ. Dipeptidyl peptidase IV inhibitors: a promising new therapeutic approach for the management of type 2 diabetes. Int J Biochem Cell Biol. 2006;38(5–6):831–44.PubMedCrossRefGoogle Scholar
  13. 13.
    Kindel TL, Yoder SM, Seeley RJ, et al. Duodenal-jejunal exclusion improves glucose tolerance in the diabetic, Goto-Kakizaki rat by a GLP-1 receptor-mediated mechanism. J Gastrointest Surg. 2009;13(10):1762–72.PubMedCrossRefGoogle Scholar
  14. 14.
    Patriti A, Aisa MC, Annetti C, et al. How the hindgut can cure type 2 diabetes. Ileal transposition improves glucose metabolism and beta-cell function in Goto-Kakizaki rats through an enhanced proglucagon gene expression and L-cell number. Surgery. 2007;142(1):74–85.PubMedCrossRefGoogle Scholar
  15. 15.
    Houten SM, Watanabe M, Auwerx J. Endocrine functions of bile acids. EMBO J. 2006;25(7):1419–25.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    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(5):741–9.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Pournaras DJ, Osborne A, Hawkins SC, et al. Remission of type 2 diabetes after gastric bypass and banding: mechanisms and 2 year outcomes. Ann Surg. 2010;252(6):966–71.PubMedCrossRefGoogle Scholar
  18. 18.
    le Roux CW, Welbourn R, Werling M, et al. Gut hormones as mediators of appetite and weight loss after Roux-en-Y gastric bypass. Ann Surg. 2007;246(5):780–5.PubMedCrossRefGoogle Scholar
  19. 19.
    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(3):339.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Neary NM, Small CJ, Druce MR, et al. Peptide YY3–36 and glucagon-like peptide-17–36 inhibit food intake additively. Endocrinology. 2005;146(12):5120–7.PubMedCrossRefGoogle Scholar
  21. 21.
    Chiang JY. Bile acids: regulation of synthesis. J Lipid Res. 2009;50(10):1955–66.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Ma H, Patti ME. Bile acids, obesity, and the metabolic syndrome. Best Pract Res Clin Gastroenterol. 2014;28(4):573–83.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Hofmann AF. The enterohepatic circulation of bile acids in mammals: form and functions. Frontiers in bioscience (Landmark edition). 2008;14:2584–98.Google Scholar
  24. 24.
    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(7):1859–64.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Kir S, Beddow SA, Samuel VT, et al. FGF19 as a postprandial, insulin-independent activator of hepatic protein and glycogen synthesis. Science (New York, NY). 2011;331(6024):1621–4.CrossRefGoogle Scholar
  26. 26.
    Lundåsen T, Gälman C, Angelin B, et al. Circulating intestinal fibroblast growth factor 19 has a pronounced diurnal variation and modulates hepatic bile acid synthesis in man. J Intern Med. 2006;260(6):530–6.PubMedCrossRefGoogle Scholar
  27. 27.
    Wu A-L, Coulter S, Liddle C, et al. FGF19 regulates cell proliferation, glucose and bile acid metabolism via FGFR4-dependent and independent pathways. PLoS One. 2011;6(3):e17868.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Seeley RJ, Chambers AP, Sandoval DA. The role of gut adaptation in the potent effects of multiple bariatric surgeries on obesity and diabetes. Cell Metab. 2015;21(3):369–78.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Taoka H, Yokoyama Y, Morimoto K, et al. Role of bile acids in the regulation of the metabolic pathways. World J Diabetes. 2016;7(13):260–70.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Vanwijngaerden YM, Wauters J, Langouche L, et al. Critical illness evokes elevated circulating bile acids related to altered hepatic transporter and nuclear receptor expression. Hepatology. 2011;54(5):1741–52.PubMedCrossRefGoogle Scholar
  31. 31.
    Zollner G, Wagner M, Moustafa T, et al. Coordinated induction of bile acid detoxification and alternative elimination in mice: role of FXR-regulated organic solute transporter-α/β in the adaptive response to bile acids. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2006;290(5):G923–G32.PubMedCrossRefGoogle Scholar
  32. 32.
    Yuan Z, Li K. The role of farnesoid X receptor in cholestasis. J Dig Dis. 2016;6 doi:10.1111/1751-2980.12378.
  33. 33.
    Hanniman EA, Lambert G, McCarthy TC, et al. Loss of functional farnesoid X receptor increases atherosclerotic lesions in apolipoprotein E-deficient mice. J Lipid Res. 2005;46(12):2595–604.PubMedCrossRefGoogle Scholar
  34. 34.
    Hartman HB, Gardell SJ, Petucci CJ, et al. Activation of farnesoid X receptor prevents atherosclerotic lesion formation in LDLR−/− and apoE−/− mice. J Lipid Res. 2009;50(6):1090–100.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Lambert G, Amar MJ, Guo G, et al. The farnesoid X-receptor is an essential regulator of cholesterol homeostasis. J Biol Chem. 2003;278(4):2563–70.PubMedCrossRefGoogle Scholar
  36. 36.
    Mencarelli A, Renga B, Distrutti E, et al. Antiatherosclerotic effect of farnesoid X receptor. Am J Phys Heart Circ Phys. 2009;296(2):H272–H81.Google Scholar
  37. 37.
    Zhang Y, Wang X, Vales C, et al. FXR deficiency causes reduced atherosclerosis in Ldlr−/− mice. Arterioscler Thromb Vasc Biol. 2006;26(10):2316–21.PubMedCrossRefGoogle Scholar
  38. 38.
    Watanabe M, Houten SM, Wang L, et al. Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c. J Clin Invest. 2004;113(10):1408–18.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Katsuma S, Hirasawa A, Tsujimoto G. Bile acids promote glucagon-like peptide-1 secretion through TGR5 in a murine enteroendocrine cell line STC-1. Biochem Biophys Res Commun. 2005;329(1):386–90.PubMedCrossRefGoogle Scholar
  40. 40.
    Thomas C, Gioiello A, Noriega L, et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 2009;10(3):167–77.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Sato H, Genet C, Strehle A, et al. Anti-hyperglycemic activity of a TGR5 agonist isolated from Olea europaea. Biochem Biophys Res Commun. 2007;362(4):793–8.PubMedCrossRefGoogle Scholar
  42. 42.
    Cipriani S, Mencarelli A, Palladino G, et al. FXR activation reverses insulin resistance and lipid abnormalities and protects against liver steatosis in Zucker (fa/fa) obese rats. J Lipid Res. 2010;51(4):771–84.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Ma K, Saha PK, Chan L, et al. Farnesoid X receptor is essential for normal glucose homeostasis. J Clin Invest. 2006;116(4):1102–9.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Zhang Y, Lee FY, Barrera G, et al. Activation of the nuclear receptor FXR improves hyperglycemia and hyperlipidemia in diabetic mice. Proc Natl Acad Sci U S A. 2006;103(4):1006–11.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    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(8):3613–9.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    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(1):214.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Dent P, Fang Y, Gupta S, et al. Conjugated bile acids promote ERK1/2 and AKT activation via a pertussis toxin–sensitive mechanism in murine and human hepatocytes. Hepatology. 2005;42(6):1291–9.PubMedCrossRefGoogle Scholar
  48. 48.
    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(2):456–63.PubMedCrossRefGoogle Scholar
  49. 49.
    Parker H, Wallis K, Le Roux C, et al. Molecular mechanisms underlying bile acid-stimulated glucagon-like peptide-1 secretion. Br J Pharmacol. 2012;165(2):414–23.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Adrian TE, Gariballa S, Parekh K, et al. Rectal taurocholate increases L cell and insulin secretion, and decreases blood glucose and food intake in obese type 2 diabetic volunteers. Diabetologia. 2012;55(9):2343–7.PubMedCrossRefGoogle Scholar
  51. 51.
    Vassiliou EK, Gonzalez A, Garcia C, et al. Oleic acid and peanut oil high in oleic acid reverse the inhibitory effect of insulin production of the inflammatory cytokine TNF-alpha both in vitro and in vivo systems. Lipids Health Dis. 2009;8:25.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Watanabe M, Houten SM, Mataki C, et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature. 2006;439(7075):484–9.PubMedCrossRefGoogle Scholar
  53. 53.
    Ockenga J, Valentini L, Schuetz T, et al. Plasma bile acids are associated with energy expenditure and thyroid function in humans. The Journal of Clinical Endocrinology & Metabolism. 2011;97(2):535–42.CrossRefGoogle Scholar
  54. 54.
    Glicksman C, Pournaras D, Wright M, et al. Postprandial plasma bile acid responses in normal weight and obese subjects. Ann Clin Biochem. 2010;47(5):482–4.PubMedCrossRefGoogle Scholar
  55. 55.
    Ahmad N, Pfalzer A, Kaplan L. Roux-en-Y gastric bypass normalizes the blunted postprandial bile acid excursion associated with obesity. Int J Obes. 2013;37(12):1553–9.CrossRefGoogle Scholar
  56. 56.
    Sato H, Macchiarulo A, Thomas C, et al. Novel potent and selective bile acid derivatives as TGR5 agonists: biological screening, structure−activity relationships, and molecular modeling studies. J Med Chem. 2008;51(6):1831–41.PubMedCrossRefGoogle Scholar
  57. 57.
    Das SK, Roberts SB, McCrory MA, et al. Long-term changes in energy expenditure and body composition after massive weight loss induced by gastric bypass surgery. Am J Clin Nutr. 2003;78(1):22–30.PubMedGoogle Scholar
  58. 58.
    Faria SL, Faria OP, de Almeida CM, et al. Diet-induced thermogenesis and respiratory quotient after Roux-en-Y gastric bypass. Surg Obes Relat Dis. 2012;8(6):797–802.PubMedCrossRefGoogle Scholar
  59. 59.
    Thivel D, Brakonieki K, Duche P, et al. Surgical weight loss: impact on energy expenditure. Obes Surg. 2013;23(2):255–66.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Wilms B, Ernst B, Thurnheer M, et al. Increased thermic effect of food after gastric bypass surgery. Obesity reviews : an official journal of the International Association for the Study of Obesity. 2012;13(Suppl 2):125.Google Scholar
  61. 61.
    Mason EE, Ito C. Gastric bypass in obesity. Surg Clin North Am. 1967;47(6):1345–51.PubMedCrossRefGoogle Scholar
  62. 62.
    Pories WJ, Flickinger EG, Meelheim D, et al. The effectiveness of gastric bypass over gastric partition in morbid obesity: consequence of distal gastric and duodenal exclusion. Ann Surg. 1982;196(4):389–99.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Brolin RE, Kenler HA, Gorman JH, et al. Long-limb gastric bypass in the superobese. A prospective randomized study. Ann Surg. 1992;215(4):387–95.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Freeman JB, Kotlarewsky M, Phoenix C. Weight loss after extended gastric bypass. Obes Surg. 1997;7(4):337–44.PubMedCrossRefGoogle Scholar
  65. 65.
    Scopinaro N, Gianetta E, Adami GF, et al. Biliopancreatic diversion for obesity at eighteen years. Surgery. 1996;119(3):261–8.PubMedCrossRefGoogle Scholar
  66. 66.
    Pinheiro JS, Schiavon CA, Pereira PB, et al. Long-long limb Roux-en-Y gastric bypass is more efficacious in treatment of type 2 diabetes and lipid disorders in super-obese patients. Surg Obes Relat Dis. 2008;4(4):521–5.PubMedCrossRefGoogle Scholar
  67. 67.
    MacLean LD, Rhode BM, Nohr CW. Long- or short-limb gastric bypass? J Gastrointest Surg. 2001;5(5):525–30.PubMedCrossRefGoogle Scholar
  68. 68.
    Ciovica R, Takata M, Vittinghoff E, et al. The impact of roux limb length on weight loss after gastric bypass. Obes Surg. 2008;18(1):5–10.PubMedCrossRefGoogle Scholar
  69. 69.
    Feng JJ, Gagner M, Pomp A, et al. Effect of standard vs extended Roux limb length on weight loss outcomes after laparoscopic Roux-en-Y gastric bypass. Surg Endosc. 2003;17(7):1055–60.PubMedCrossRefGoogle Scholar
  70. 70.
    Christou NV, Look D, Maclean LD. Weight gain after short- and long-limb gastric bypass in patients followed for longer than 10 years. Ann Surg. 2006;244(5):734–40.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Sugerman HJKJ, DeMaria EJ. Conversion of proximal to distal bypass for failed gastric bypass for superobesity. J Gastrointest Surg. 1997;1:517–26.PubMedCrossRefGoogle Scholar
  72. 72.
    Brolin RECR. Adding malabsorption for weight loss failure after gastric bypass. SurgEndosc. 2007;21:1924–6.Google Scholar
  73. 73.
    Nelson WKFJ, Houghton SG, et al. The malabsorptive very, very long limb Roux-en-Y gastric bypass for super obesity: results in 257 patients. Surgery. 2006;140:517–23.PubMedCrossRefGoogle Scholar
  74. 74.
    McConnell DBORR, Deveney CW. Common channel length predicts outcomes of biliopancreatic diversion alone and with the duodenal switch surgery. Am J Surg. 2005;189:536–40.PubMedCrossRefGoogle Scholar
  75. 75.
    Brolin RELL, Kelner HA, et al. Malabsorptive gastric bypass in patients with superobesity. J Gastrointest Surgery. 2002;6:195–205.CrossRefGoogle Scholar
  76. 76.
    Ionut V, Burch M, Youdim A, et al. Gastrointestinal hormones and bariatric surgery-induced weight loss. Obesity. 2013;21(6):1093–103.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    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. 2009;17(9):1671–7.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    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. 2013;21(12):E660–E8.PubMedCrossRefGoogle Scholar
  79. 79.
    Scholtz S, Miras AD, Chhina N, et al. Obese patients after gastric bypass surgery have lower brain-hedonic responses to food than after gastric banding. Gut. 2014;63(6):891–902.PubMedCrossRefGoogle Scholar
  80. 80.
    Werling M, Vincent RP, Cross GF, et al. Enhanced fasting and post-prandial plasma bile acid responses after Roux-en-Y gastric bypass surgery. Scand J Gastroenterol. 2013;48(11):1257–64.PubMedCrossRefGoogle Scholar
  81. 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(4):E708–12.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Ashrafian H, Li JV, Spagou K, et al. Bariatric surgery modulates circulating and cardiac metabolites. J Proteome Res. 2014;13(2):570–80.PubMedCrossRefGoogle Scholar
  83. 83.
    Jansen PL, van Werven J, Aarts E, et al. Alterations of hormonally active fibroblast growth factors after Roux-en-Y gastric bypass surgery. Dig Dis. 2011;29(1):48–51.PubMedCrossRefGoogle Scholar
  84. 84.
    Simonen M, Dali-Youcef N, Kaminska D, et al. Conjugated bile acids associate with altered rates of glucose and lipid oxidation after Roux-en-Y gastric bypass. Obes Surg. 2012;22(9):1473–80.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Dirksen C, Jørgensen N, Bojsen-Møller K, et al. Gut hormones, early dumping and resting energy expenditure in patients with good and poor weight loss response after Roux-en-Y gastric bypass. Int J Obes. 2013;37(11):1452–9.CrossRefGoogle Scholar
  86. 86.
    Nakatani H, Kasama K, Oshiro T, et al. Serum bile acid along with plasma incretins and serum high-molecular weight adiponectin levels are increased after bariatric surgery. Metabolism. 2009;58(10):1400–7.PubMedCrossRefGoogle Scholar
  87. 87.
    Haluzikova D, Lacinova Z, Kavalkova P, et al. Laparoscopic sleeve gastrectomy differentially affects serum concentrations of FGF-19 and FGF-21 in morbidly obese subjects. Obesity (Silver Spring). 2013 Jul;21(7):1335–42.CrossRefGoogle Scholar
  88. 88.
    Korner J, Inabnet W, Febres G, et al. Prospective study of gut hormone and metabolic changes after adjustable gastric banding and Roux-en-Y gastric bypass. Int J Obes. 2009;33(7):786–95.CrossRefGoogle Scholar
  89. 89.
    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(7):1709–16.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Morínigo R, Moizé V, Musri M, et al. Glucagon-like peptide-1, peptide YY, hunger, and satiety after gastric bypass surgery in morbidly obese subjects. The Journal of Clinical Endocrinology & Metabolism. 2006;91(5):1735–40.CrossRefGoogle Scholar
  91. 91.
    Vidal J, Nicolau J, Romero F, et al. Long-term effects of Roux-en-Y gastric bypass surgery on plasma glucagon-like peptide-1 and islet function in morbidly obese subjects. The Journal of Clinical Endocrinology & Metabolism. 2009;94(3):884–91.CrossRefGoogle Scholar
  92. 92.
    Nestoridi E, Kvas S, Kucharczyk J, et al. Resting energy expenditure and energetic cost of feeding are augmented after Roux-en-Y gastric bypass in obese mice. Endocrinology. 2012;153(5):2234–44.PubMedCrossRefGoogle Scholar
  93. 93.
    Plum L, Ahmed L, Febres G, et al. Comparison of glucostatic parameters after hypocaloric diet or bariatric surgery and equivalent weight loss. Obesity. 2011;19(11):2149–57.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Stylopoulos N, Zhang XB, Brownell A-L, et al. W1854 Roux-en-Y gastric bypass activates brown adipose tissue and increases energy expenditure in obese mice. Gastroenterology. 2010;138(5):S-754.Google Scholar
  95. 95.
    Nakatani H, Kasama K, Oshiro T, et al. Serum bile acid along with plasma incretins and serum high–molecular weight adiponectin levels are increased after bariatric surgery. Metab Clin Exp. 2009;58(10):1400–7.PubMedCrossRefGoogle Scholar
  96. 96.
    Liaset B, Hao Q, Jørgensen H, et al. Nutritional regulation of bile acid metabolism is associated with improved pathological characteristics of the metabolic syndrome. J Biol Chem. 2011;286(32):28382–95.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Mencarelli A, Renga B, D’Amore C, et al. Dissociation of intestinal and hepatic activities of FXR and LXRα supports metabolic effects of terminal ileum interposition in rodents. Diabetes. 2013;62(10):3384–93.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Pournaras D, le Roux C. Are bile acids the new gut hormones? Lessons from weight loss surgery models. Endocrinology. 2013;154(7):2255–6.PubMedCrossRefGoogle Scholar
  99. 99.
    Kohli R, Setchell KD, Kirby M, et al. A surgical model in male obese rats uncovers protective effects of bile acids post-bariatric surgery. Endocrinology. 2013;154(7):2341–51.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Dhurandhar NV, Schoeller D, Brown AW, et al. Energy balance measurement: when something is not better than nothing. Int J Obes. 2015 Jul;39(7):1109–13.CrossRefGoogle Scholar
  101. 101.
    Ryan KK, Tremaroli V, Clemmensen C, et al. FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature. 2014;509(7499):183–8.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Woelnerhanssen B, Peterli R, Steinert RE, et al. Effects of postbariatric surgery weight loss on adipokines and metabolic parameters: comparison of laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy—a prospective randomized trial. Surg Obes Relat Dis. 2011;7(5):561–8.PubMedCrossRefGoogle Scholar
  103. 103.
    Zhang Y, Edwards PA. FXR signaling in metabolic disease. FEBS Lett. 2008;582(1):10–8.PubMedCrossRefGoogle Scholar
  104. 104.
    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. The Journal of Clinical Endocrinology & Metabolism. 2013;98(4):E708–E12.CrossRefGoogle Scholar
  105. 105.
    Insull Jr W. Clinical utility of bile acid sequestrants in the treatment of dyslipidemia: a scientific review. South Med J. 2006;99(3):257–74.PubMedCrossRefGoogle Scholar
  106. 106.
    Beysen C, Murphy E, Deines K, et al. Effect of bile acid sequestrants on glucose metabolism, hepatic de novo lipogenesis, and cholesterol and bile acid kinetics in type 2 diabetes: a randomised controlled study. Diabetologia. 2012;55(2):432–42.PubMedCrossRefGoogle Scholar
  107. 107.
    Fonseca VA, Rosenstock J, Wang AC, et al. Colesevelam HCl improves glycemic control and reduces LDL cholesterol in patients with inadequately controlled type 2 diabetes on sulfonylurea-based therapy. Diabetes Care. 2008;31(8):1479–84.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Goldberg RB, Fonseca VA, Truitt KE, et al. Efficacy and safety of colesevelam in patients with type 2 diabetes mellitus and inadequate glycemic control receiving insulin-based therapy. Arch Intern Med. 2008;168(14):1531–40.PubMedCrossRefGoogle Scholar
  109. 109.
    Shang Q, Saumoy M, Holst JJ, et al. Colesevelam improves insulin resistance in a diet-induced obesity (F-DIO) rat model by increasing the release of GLP-1. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2010;298(3):G419–G24.PubMedCrossRefGoogle Scholar
  110. 110.
    Suzuki T, Oba K, Igari Y, et al. Colestimide lowers plasma glucose levels and increases plasma glucagon-like PEPTIDE-1 (7-36) levels in patients with type 2 diabetes mellitus complicated by hypercholesterolemia. Journal of Nippon Medical School. 2007;74(5):338–43.PubMedCrossRefGoogle Scholar
  111. 111.
    Watanabe M, Morimoto K, Houten SM, et al. Bile acid binding resin improves metabolic control through the induction of energy expenditure. PLoS One. 2012;7(8):e38286.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Harach T, Pols TW, Nomura M, et al. TGR5 potentiates GLP-1 secretion in response to anionic exchange resins. Scientific reports. 2012;2Google Scholar
  113. 113.
    Matsubara T, Li F, Gonzalez FJ. FXR signaling in the enterohepatic system. Mol Cell Endocrinol. 2013;368(1):17–29.PubMedCrossRefGoogle Scholar
  114. 114.
    Duboc H, Taché Y, Hofmann AF. The bile acid TGR5 membrane receptor: from basic research to clinical application. Dig Liver Dis. 2014;46(4):302–12.PubMedCrossRefGoogle Scholar
  115. 115.
    Stepanov V, Stankov K, Mikov M. The bile acid membrane receptor TGR5: a novel pharmacological target in metabolic, inflammatory and neoplastic disorders. Journal of Receptors and Signal Transduction. 2013;33(4):213–23.PubMedCrossRefGoogle Scholar
  116. 116.
    Staels B, Kuipers F. Bile acid sequestrants and the treatment of type 2 diabetes mellitus. Drugs. 2007;67(10):1383–92.PubMedCrossRefGoogle Scholar
  117. 117.
    Brufau G, Bahr MJ, Staels B, et al. Plasma bile acids are not associated with energy metabolism in humans. Nutrition & metabolism. 2010;7(1):1.CrossRefGoogle Scholar
  118. 118.
    Brufau G, Stellaard F, Prado K, et al. Improved glycemic control with colesevelam treatment in patients with type 2 diabetes is not directly associated with changes in bile acid metabolism. Hepatology. 2010;52(4):1455–64.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Mohsen Mazidi
    • 1
    • 2
  • Pedro Paulo P. de Caravatto
    • 3
  • John R. Speakman
    • 1
    • 4
  • Ricardo V. Cohen
    • 3
  1. 1.State Key Laboratory of Molecular Developmental BiologyInstitute of Genetics and Developmental Biology, Chinese Academy of SciencesChaoyangChina
  2. 2.University of the Chinese Academy of SciencesHuairouChina
  3. 3.The Center for Obesity and DiabetesOswaldo Cruz German HospitalSão PauloBrazil
  4. 4.Institute of Biological and Environmental ScienceUniversity of AberdeenAberdeenUK

Personalised recommendations