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01-02-2018

Increased glycine-amidated hyocholic acid correlates to improved early weight loss after sleeve gastrectomy

Authors: Tammy L. Kindel, Crystal Krause, Melissa C. Helm, Corrigan L. McBride, Dmitry Oleynikov, Rhishikesh Thakare, Jawaher Alamoudi, Vishal Kothari, Yazen Alnouti, Rohit Kohli

Published in: Surgical Endoscopy | Issue 2/2018

Abstract

Background

Bile acids (BAs) are post-prandial hormones that play an important role in glucose and lipid homeostasis as well as energy expenditure. Total and glycine-amidated BAs increase after sleeve gastrectomy (SG) and correlate to improved metabolic disease. No specific bile acid subtype has been shown conclusively to mediate the weight loss effect. Therefore, the objective of this study was to prospectively evaluate the comprehensive changes in meal-stimulated BAs after SG and determine if a specific change in the BA profile correlates to the early weight loss response.

Methods

Patients were prospectively enrolled at the University of Nebraska Medical Center who were undergoing a SG for treatment of morbid obesity. Primary and secondary plasma bile acids and their amidated (glycine, G-, or taurine, T-) subtypes were measured at fasting, 30 and 60 min after a liquid meal performed pre-op, and at 6 and 12 weeks post-op. Area under the curve (AUC) was calculated for the hour meal test for each bile acid subtype. BAs that were significantly increased post-op were correlated to body mass index (BMI) loss.

Results

Total BA AUC was significantly increased at 6 (p < 0.01) and 12 weeks post-op (p < 0.01) compared to pre-operative values. The increase in total BA AUC was due to a statistically significant increase in G-BAs. Nine different BA AUC subtypes were significantly increased at both 6 and 12 weeks post-op. Increased total and G-chenodeoxycholic acid AUC was significantly correlated to the 6 week BMI loss (p = 0.03). Increased G-hyocholic acid was significantly correlated to increased weight loss at both 6 (p = 0.05) and 12 weeks (p = 0.006).

Conclusions

SG induced an early and persistent post-prandial surge in multiple bile acid subtypes. Increased G-hyocholic consistently correlated with greater early BMI loss. This study provides evidence for a role of BAs in the surgical weight loss response after SG.

Peterli R, Wolnerhanssen BK, Vetter D, Nett P, Gass M, Borbely Y, Peters T, Schiesser M, Schultes B, Beglinger C, Drewe J, Bueter M (2017) Laparoscopic sleeve gastrectomy versus Roux-Y-gastric bypass for morbid obesity-3-year outcomes of the prospective randomized Swiss Multicenter Bypass or Sleeve Study (SM-BOSS). Ann Surg 265:466–473CrossRefPubMed

Evers SS, Sandoval DA, Seeley RJ (2017) The physiology and molecular underpinnings of the effects of bariatric surgery on obesity and diabetes. Annu Rev Physiol 79:313–334CrossRefPubMed

Fouladi F, Mitchell JE, Wonderlich JA, Steffen KJ (2016) The contributing role of bile acids to metabolic improvements after obesity and metabolic surgery. Obes Surg 26:2492–2502CrossRefPubMed

Escalona A, Munoz R, Irribarra V, Solari S, Allende F, Francisco Miquel J (2016) Bile acids synthesis decreases after laparoscopic sleeve gastrectomy. Surg Obes Relat Dis 12:763–769CrossRefPubMed

Zhou H, Hylemon PB (2014) Bile acids are nutrient signaling hormones. Steroids 86:62–68CrossRefPubMed

Makishima M, Okamoto AY, Repa JJ, Tu H, Learned RM, Luk A, Hull MV, Lustig KD, Mangelsdorf DJ, Shan B (1999) Identification of a nuclear receptor for bile acids. Science 284:1362–1365CrossRefPubMed

de Aguiar Vallim TQ, Tarling EJ, Edwards PA (2013) Pleiotropic roles of bile acids in metabolism. Cell Metab 17:657–669CrossRefPubMedPubMedCentral

Watanabe M, Houten SM, Mataki C, Christoffolete MA, Kim BW, Sato H, Messaddeq N, Harney JW, Ezaki O, Kodama T, Schoonjans K, Bianco AC, Auwerx J (2006) Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439(7075):484–489CrossRefPubMed

Kumar DP, Rajagopal S, Mahavadi S, Mirshahi F, Grider JR, Murthy KS, Sanyal AJ (2012) Activation of transmembrane bile acid receptor TGR5 stimulates insulin secretion in pancreatic β cells. Biochem Biophys Res Commun 427:600–605CrossRefPubMedPubMedCentral

10.

Trabelsi MS, Daoudi M, Prawitt J, Ducastel S, Touche V, Sayin SI, Perino A, Brighton CA, Sebti Y, Kluza J, Briand O, Dehondt H, Vallez E, Dorchies E, Baud G, Spinelli V, Hennuyer N, Caron S, Bantubungi K, Caiazzo R, Reimann F, Marchetti P, Lefebvre P, Bäckhed F, Gribble FM, Schoonjans K, Pattou F, Tailleux A, Staels B, Lestavel S (2015) Farnesoid X receptor inhibits glucagon-like peptide-1 production by enteroendocrine L cells. Nat Commun 6:7629CrossRefPubMedPubMedCentral

11.

Kohli R, Bradley D, Setchell KD, Eagon JC, Abumrad N, Klein S (2013) Weight loss induced by Roux-en-Y gastric bypass but not laparoscopic adjustable gastric banding increases circulating bile acids. J Clin Endocrinol Metab 98:E708–E712CrossRefPubMedPubMedCentral

12.

De Giorgi S, Campos V, Egli L, Toepel U, Carrel G, Cariou B, Rainteau D, Schneiter P, Tappy L, Giusti V (2015) Long-term effects of Roux-en-Y gastric bypass on postprandial plasma lipid and bile acid kinetics in female non diabetic subjects: a cross-sectional pilot study. Clin Nutr 34:911–917CrossRefPubMed

13.

Werling M, Vincent RP, Cross GF, Marschall HU, Fandriks L, Lonroth H, Taylor DR, Alaghband-Zadeh J, Olbers T, Le Roux CW (2013) Enhanced fasting and post-prandial plasma bile acid responses after Roux-en-Y gastric bypass surgery. Scand J Gastroenterol 48:1257–1264CrossRefPubMed

14.

Jahansouz C, Xu H, Hertzel AV, Serrot FJ, Kvalheim N, Cole A, Abraham A, Luthra G, Ewing K, Leslie DB, Bernlohr DA, Ikramuddin S (2016) Bile acids increase independently from hypocaloric restriction after bariatric surgery. Ann Surg 264:1022–1028CrossRefPubMed

15.

Belgaumkar AP, Vincent RP, Carswell KA, Hughes RD, Alaghband-Zadeh J, Mitry RR, le Roux CW, Patel AG (2016) Changes in bile acid profile after laparoscopic sleeve gastrectomy are associated with improvements in metabolic profile and fatty liver disease. Obes Surg 26:1195–1202CrossRefPubMed

16.

Steinert RE, Peterli R, Keller S, Meyer-Gerspach AC, Drewe J, Peters T, Beglinger C (2013) Bile acids and gut peptide secretion after bariatric surgery: a 1-year prospective randomized pilot trial. Obesity 21:E660–E668CrossRefPubMed

17.

Khan FH, Shaw L, Zhang W, Salazar Gonzalez RM, Mowery S, Oehrle M, Zhao X, Jenkins T, Setchell KD, Inge TH, Kohli R (2016) Fibroblast growth factor 21 correlates with weight loss after vertical sleeve gastrectomy in adolescents. Obesity 24:2377–2383CrossRefPubMed

18.

Myronovych A, Kirby M, Ryan KK, Zhang W, Jha P, Setchell KD, Dexheimer PJ, Aronow B, Seeley RJ, Kohli R (2014) Vertical sleeve gastrectomy reduces hepatic steatosis while increasing serum bile acids in a weight-loss-independent manner. Obesity 22:390–400CrossRefPubMed

19.

Ryan KK, Tremaroli V, Clemmensen C, Kovatcheva-Datchary P, Myronovych A, Karns R, Wilson-Perez HE, Sandoval DA, Kohli R, Backhed F, Seeley RJ (2014) FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature 509:183–188CrossRefPubMedPubMedCentral

20.

Bathena SP, Mukherjee S, Olivera M, Alnouti Y (2013) The profile of bile acids and their sulfate metabolites in human urine and serum. J Chromatogr B 942–943:53–62CrossRef

21.

Huang J, Bathena SP, Cxanaky IL, Alnouti Y (2011) Simultaneous characterization of bile acids and their sulfate metabolites in mouse liver, plasma, bile and urine using LC-MS/MS. J Pharm Biomed Anal 55:1111–1119CrossRefPubMed

22.

Haluzikova D, Lacinova Z, Kavalkova P, Drapalova J, Krizova J, Bartlova M, Mraz M, Petr T, Vitek L, Kasalicky M, Haluzik M (2013) Laparoscopic sleeve gastrectomy differentially affects serum concentrations of FGF-19 and FGF-21 in morbidly obese subjects. Obesity 21:1335–1342CrossRefPubMed

23.

Khan FH, Kohli R (2016) Bariatric surgery: the rise and fall of bile acids. Surg Obes Relat Dis 12:770–771CrossRefPubMed

24.

Heuman DM (1989) Quantitative estimation of the hydrophilic-hydrophobic balance of mixed bile salt solutions. J Lipid Res 30:719–730PubMed

25.

Radominska-Pyrek A, Zimniak P, Irshaid YM, Lester R, Tephly TR, St Pyrek J (1987) Glucuronidation of 6 alpa-hydroxy bile acids by human liver microsomes. J Clin Invest 80:234–241CrossRefPubMedPubMedCentral

26.

Kuipers F, Bloks VW, Groen AK (2014) Beyond intestinal soap–bile acids in metabolic control. Nat Rev Endocrinol 10:488–498CrossRefPubMed

27.

Bodin K, Lindbom U, Diczfalusy U (2005) Novel pathways of bile acid metabolism involving CYP3A4. Biochim Biophys Acta 1687:84–93CrossRefPubMed

28.

Kano M, Matsumoto M, Kamano T, Tsurumaru M (1999) ELISA determination of serum hyocholic acid concentrations in humans and their possible clinical significance. Hepatogastroenterology 46:983–984PubMed

29.

Chen J, Zhao KN, Chen C (2014) The role of CYP3A4 in the biotransformation of bile acids and therapeutic implication for cholestasis. Ann Transl Med 2:7PubMedPubMedCentral

30.

Stedman C, Robertson G, Coulter S, Liddle C (2004) Feed-forward regulation of bile acid detoxification by CYP3A4: studies in humanized transgenic mice. J Biol Chem 279:11336–11343CrossRefPubMed

31.

Araki Y, Andoh A, Bamba H, Yoshikawa K, Doi H, Komai Y, Higuchi A, Fujiyama Y (2003) The cytotoxicity of hydrophobic bile acids is ameliorated by more hydrophilic bile acids in intestinal cell lines IEC-6 and Caco-2. Oncol Rep 10:1931–1936PubMed

32.

Sato H, Macchiarulo A, Thomas C, Gioiello A, Une M, Hofmann AF, Saladin R, Schoonjans K, Pellicciari R, Auwerx J (2008) Novel potent and selective bile acid derivatives as TGR5 agonists: biological screening, structure-activity relationships, and molecular modeling studies. J Med Chem 51:1831–1841CrossRefPubMed

33.

Sayin SI, Wahlstrom A, Felin J, Jantti S, Marschall HU, Bamberg K, Angelin B, Hyotylainen T, Oresic M, Backhed F (2013) Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab 17:225–235CrossRefPubMed

Title: Increased glycine-amidated hyocholic acid correlates to improved early weight loss after sleeve gastrectomy
Authors: Tammy L. Kindel
Crystal Krause
Melissa C. Helm
Corrigan L. McBride
Dmitry Oleynikov
Rhishikesh Thakare
Jawaher Alamoudi
Vishal Kothari
Yazen Alnouti
Rohit Kohli
Publication date: 01-02-2018
Publisher: Springer US
Published in: Surgical Endoscopy / Issue 2/2018
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI: https://doi.org/10.1007/s00464-017-5747-y

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Increased glycine-amidated hyocholic acid correlates to improved early weight loss after sleeve gastrectomy

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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