Early increases in bile acids post Roux-en-Y gastric bypass are driven by insulin-sensitizing, secondary bile acids

Journal of Clinical Endocrinology and Metabolism

Volumn 100, Issue 9, 2015, Pages E1225-E1233

  Albaugh, Vance L ^a   Flynn, Charles Robb ^a   Cai, Steven ^b   Xiao, Yi ^c   Tamboli, Robyn A ^a   Abumrad, Naji N ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; GLYCINE; INSULIN; TAURINE; URSODEOXYCHOLIC ACID; GLUCOSE BLOOD LEVEL;

ADULT; ARTICLE; BILE ACID BLOOD LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; HORMONE DETERMINATION; HUMAN; INSULIN SENSITIVITY; OBESITY; OBSERVATIONAL STUDY; POSTOPERATIVE PERIOD; PREOPERATIVE PERIOD; PRIORITY JOURNAL; ROUX Y ANASTOMOSIS; STOMACH BYPASS; WEIGHT REDUCTION; ADOLESCENT; BLOOD; BODY MASS; DIET RESTRICTION; FEMALE; FOLLOW UP; GLUCOSE BLOOD LEVEL; INSULIN RESISTANCE; MALE; MIDDLE AGED; OBESITY, MORBID; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; TREATMENT OUTCOME; YOUNG ADULT;

ADOLESCENT; ADULT; BILE ACIDS AND SALTS; BLOOD GLUCOSE; BODY MASS INDEX; FASTING; FEMALE; FOLLOW-UP STUDIES; GASTRIC BYPASS; HUMANS; INSULIN; INSULIN RESISTANCE; MALE; MIDDLE AGED; OBESITY, MORBID; TREATMENT OUTCOME; WEIGHT LOSS; YOUNG ADULT;

EID: 84941654446     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2015-2467     Document Type: Article

References (43)

1. Kashyap SR, Bhatt DL, Wolski K, et al. Metabolic effects of bariatric surgery in patients with moderate obesity and type 2 diabetes: analysis of a randomized control trial comparing surgery with intensive medical treatment. Diabetes Care. 2013;36:2175-2182.
2. Schauer PR, Kashyap SR, Wolski K, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med. 2012;366:1567-1576.
3. Gloy VL, Briel M, Bhatt DL, et al. Bariatric surgery versus nonsurgical treatment for obesity: a systematic review and meta-analysis of randomised controlled trials. BMJ. 2013;347:f5934.
4. Puzziferri N, Roshek TB 3rd, Mayo HG, Gallagher R, Belle SH, Livingston EH. Long-term follow-up after bariatric surgery: a systematic review. JAMA. 2014;312:934-942.
5. Ahn SM, Pomp A, Rubino F. Metabolic surgery for type 2 diabetes. Ann NY Acad Sci. 2010;1212:E37-E45.
6. Matsubara T, Li F, Gonzalez FJ. FXR signaling in the enterohepatic system. Mol Cell Endocrinol. 2013;368:17-29.
7. 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 USA. 2006;103:1006-1011.
8. Watanabe M, Horai Y, Houten SM, et al. Lowering bile acid pool size with a synthetic farnesoid X receptor (FXR) agonist induces obesity and diabetes through reduced energy expenditure. J Biol Chem. 2011;286:26913-26920.
9. Watanabe M, Houten SM, Mataki C, et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature. 2006;439:484-489.
10. Trauner M, Claudel T, Fickert P, Moustafa T, Wagner M. Bile acids as regulators of hepatic lipid and glucose metabolism. Dig Dis. 2010;28:220-224.
11. Culnan DM, Albaugh V, Sun M, Lynch CJ, Lang CH, Cooney RN. Ileal interposition improves glucose tolerance and insulin sensitivity in the obese Zucker rat. Am J Physiol Gastrointest Liver Physiol. 2010;299:G751-G760.
12. Bhutta HY, Rajpal N, White W, et al. Effect of Roux-en-Y gastric bypass surgery on bile acid metabolism in normal and obese diabetic rats. PLoS One. 2015;10:e0122273.
13. Dunn JP, Abumrad NN, Breitman I, et al. Hepatic and peripheral insulin sensitivity and diabetes remission at 1 month after Rouxen-Y gastric bypass surgery in patients randomized to omentectomy. Diabetes Care. 2012;35:137-142.
14. Tamboli RA, Hajri T, Jiang A, et al. Reduction in inflammatory gene expression in skeletal muscle from Roux-en-Y gastric bypass patients randomized to omentectomy. PLoS One. 2011;6:e28577.
15. Fabbrini E, Tamboli RA, Magkos F, et al. Surgical removal of omental fat does not improve insulin sensitivity and cardiovascular risk factors in obese adults. Gastroenterology. 2010;139:448-455.
16. Tataranni PA, Ravussin E. Use of dual-energy x-ray absorptiometry in obese individuals. Am J Clin Nutr. 1995;62:730-734.
17. Rodrigues CM, Setchell KD. Performance characteristics of reversed-phase bonded silica cartridges for serum bile acid extraction. Biomed Chromatogr. 1996;10:1-5.
18. Hagio M, Matsumoto M, Fukushima M, Hara H, Ishizuka S. Improved analysis of bile acids in tissues and intestinal contents of rats using LC/ESI-MS. J Lipid Res. 2009;50:173-180.
19. 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.
20. Kohli R, Bradley D, Setchell KD, Eagon JC, Abumrad N, Klein S. 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.
21. 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.
22. Jørgensen NB, Dirksen C, Bojsen-Møller KN, et al. Improvements in glucose metabolism early after gastric bypass surgery are not explained by increases in total bile acids and fibroblast growth factor 19 concentrations. J Clin Endocrinol Metab. 2015;100:E396-E406.
23. Nakatani H, Kasama K, Oshiro T, Watanabe M, Hirose H, Itoh H. Serum bile acid along with plasma incretins and serum high-molecular weight adiponectin levels are increased after bariatric surgery. Metabolism. 2009;58:1400-1407.
24. 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.
25. 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;22:1473-1480.
26. Haeusler RA, Astiarraga B, Camastra S, Accili D, Ferrannini E. Human insulin resistance is associated with increased plasma levels of 12-hydroxylated bile acids. Diabetes. 2013;62:4184-4191.
27. Gerhard GS, StyerAM,WoodGC, et al.Arole for fibroblast growth factor 19 and bile acids in diabetes remission after Roux-en-Y gastric bypass. Diabetes Care. 2013;36:1859-1864.
28. Werling M, Vincent RP, Cross GF, et al. Enhanced fasting and postprandial plasma bile acid responses after Roux-en-Y gastric bypass surgery. Scand J Gastroenterol. 2013;48:1257-1264.
29. 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.
30. Mueller M, Thorell A, Claudel T, et al. Ursodeoxycholic acid exerts farnesoid X receptor-antagonistic effects on bile acid and lipid metabolism in morbid obesity. J Hepatol. 2015;62:1398-1404.
31. Gonzalez FJ, Jiang C, BissonWH,Patterson AD. Inhibition of farnesoid X receptor signaling shows beneficial effects in human obesity. J Hepatol. 2015;62:1234-1236.
32. Ryan KK, Tremaroli V, Clemmensen C, et al. FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature. 2014; 509:183-188.
33. Dutia R, Embrey M, O'Brien S, et al. Temporal changes in bile acid levels and 12-hydroxylation after Roux-en-Y gastric bypass surgery in type 2 diabetes. Int J Obes (Lond). 2015;39:806-813.
34. Kars M, Yang L, Gregor MF, et al. Tauroursodeoxycholic acid may improve liver and muscle but not adipose tissue insulin sensitivity in obese men and women. Diabetes. 2010;59:1899-1905.
35. Sayin SI, Wahlström A, Felin J, et al. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-muricholic acid, a naturally occurring FXR antagonist. Cell Metab. 2013;17:225-235.
36. WangYD, ChenWD,YuD, FormanBM,HuangW.The G-proteincoupled bile acid receptor, Gpbar1 (TGR5), negatively regulates hepatic inflammatory response through antagonizing nuclear factor β light-chain enhancer of activated B cells (NF-κB) in mice. Hepatology. 2011;54:1421-1432.
37. Kuipers F, Bloks VW, Groen AK. Beyond intestinal soap-bile acids in metabolic control. Nat Rev Endocrinol. 2014;10:488-498.
38. Jones ML, Tomaro-Duchesneau C, Prakash S. The gut microbiome, probiotics, bile acids axis, and human health. Trends Microbiol. 2014;22:306-308.
39. Liou AP, Paziuk M, Luevano JM Jr, Machineni S, Turnbaugh PJ, Kaplan LM. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med. 2013;5: 178ra41.
40. Li F, Jiang C, Krausz KW, et al. Microbiome remodelling leads to inhibition of intestinal farnesoidXreceptor signalling and decreased obesity. Nat Commun. 2013;4:2384.
41. Ridlon JM, Kang DJ, Hylemon PB. Bile salt biotransformations by human intestinal bacteria. J Lipid Res. 2006;47:241-259.
42. Flynn CR, Albaugh VL, Cai S, et al. Bile diversion to the distal small intestine has comparable metabolic benefits to bariatric surgery. Nat Commun. 2015;6:7715.
43. Myronovych A, Kirby M, Ryan KK, et al. Vertical sleeve gastrectomy reduces hepatic steatosis while increasing serum bile acids in a weight-loss-independent manner. Obesity (Silver Spring). 2014; 22:390-400.