Metabolomic signatures after bariatric surgery - a systematic review

Matilde Vaz, Sofia S Pereira, Mariana P Monteiro, Matilde Vaz, Sofia S Pereira, Mariana P Monteiro

Abstract

Metabolomics emerged as an important tool to gain insights on how the body responds to therapeutic interventions. Bariatric surgery is the most effective treatment for severe obesity and obesity-related co-morbidities. Our aim was to conduct a systematic review of the available data on metabolomics profiles that characterize patients submitted to different bariatric surgery procedures, which could be useful to predict clinical outcomes including weight loss and type 2 diabetes remission. For that, the Preferred Reporting Items for Systematic Reviews and Meta-Analyses - PRISMA guidelines were followed. Data from forty-seven original study reports addressing metabolomics profiles induced by bariatric surgery that met eligibility criteria were compiled and summarized. Amino acids, lipids, energy-related and gut microbiota-related were the metabolite classes most influenced by bariatric surgery. Among these, higher pre-operative levels of specific lipids including phospholipids, long-chain fatty acids and bile acids were associated with post-operative T2D remission. As conclusion, metabolite profiling could become a useful tool to predict long term response to different bariatric surgery procedures, allowing more personalized interventions and improved healthcare resources allocation.

Keywords: Bariatric surgery; Metabolomics; Type 2 diabetes remission; Weight loss.

Conflict of interest statement

The authors have nothing to disclose.

© 2021. The Author(s).

Figures

Fig. 1
Fig. 1
Flowchart of the search, eligibility criteria approaches and study inclusion for systematic review
Fig. 2
Fig. 2
Main metabolomic alterations induced by bariatric surgery, in patients with obesity. Abbreviations: 3-HB – 3-hydroxybutyrate; LCSFA – Long-Chain Saturated Fatty Acids; LPC – Lysophosphatidylcholine; MCSFA – Medium-Chain Saturated Fatty Acids; NEFA – Non-Esterified Fatty Acids; PE – Phosphatidylethanolamine; TCA – Tricarboxylic Acid
Fig. 3
Fig. 3
Metabolomic profiles of patients with successful weight loss/maintenance. Abbreviations: 5-HIAA – 5-hydroxyindoleacetic acid; 5-HTrp – 5-hydroxytryptophan; CDCA – Chenodeoxycholic Acid; CE – cholesterol esters; DG – diaglycerols; G- – glycine amidated; HCA – hyocholic acid, SG – Sleeve gastrectomy; RYGB – Roux-en-Y Gastric Bypass; TG – triacylglyceride
Fig. 4
Fig. 4
Metabolomic profiles of patients with T2D remission/improved insulin parameters. Abbreviations: BPD – Biliopancreatic diversion; DJB – Duodenal-jejunal bypass; HDL – High-density Lipoprotein; LCFA – long-chain free fatty acids; LDL – Low-density Lipoprotein; PE – Phosphatidylethanolamines; SG – Sleeve gastrectomy; RYGB – Roux-en-Y Gastric Bypass; TCA – Tricarboxylic Acid; VLDL – Very-low-density Lipoprotein

References

    1. Rangel-Huerta OD, Pastor-Villaescusa B, Gil A. Are we close to defining a metabolomic signature of human obesity? A systematic review of metabolomics studies. Metabolomics. 2019;15(6):93. doi: 10.1007/s11306-019-1553-y.
    1. Nyberg ST, Batty GD, Pentti J, Virtanen M, Alfredsson L, Fransson EI, Goldberg M, Heikkilä K, Jokela M, Knutsson A, Koskenvuo M, Lallukka T, Leineweber C, Lindbohm JV, Madsen IEH, Magnusson Hanson LL, Nordin M, Oksanen T, Pietiläinen O, Rahkonen O, Rugulies R, Shipley MJ, Stenholm S, Suominen S, Theorell T, Vahtera J, Westerholm PJM, Westerlund H, Zins M, Hamer M, Singh-Manoux A, Bell JA, Ferrie JE, Kivimäki M. Obesity and loss of disease-free years owing to major non-communicable diseases: a multicohort study. The Lancet Public Health. 2018;3(10):e490–e497. doi: 10.1016/S2468-2667(18)30139-7.
    1. Tulipani S, Griffin J, Palau-Rodriguez M, Mora-Cubillos X, Bernal-Lopez RM, Tinahones FJ, Corkey BE, Andres-Lacueva C. Metabolomics-guided insights on bariatric surgery versus behavioral interventions for weight loss. Obesity (Silver Spring) 2016;24(12):2451–2466. doi: 10.1002/oby.21686.
    1. Poirier P, Cornier MA, Mazzone T, Stiles S, Cummings S, Klein S, McCullough PA, Ren Fielding C, Franklin BA. Bariatric surgery and cardiovascular risk factors: a scientific statement from the American Heart Association. Circulation. 2011;123(15):1683–1701. doi: 10.1161/CIR.0b013e3182149099.
    1. Arterburn DE, Bogart A, Sherwood NE, Sidney S, Coleman KJ, Haneuse S, O'Connor PJ, Theis MK, Campos GM, McCulloch D, Selby J. A multisite study of long-term remission and relapse of type 2 diabetes mellitus following gastric bypass. Obes Surg. 2013;23(1):93–102. doi: 10.1007/s11695-012-0802-1.
    1. Courcoulas AP, King WC, Belle SH, Berk P, Flum DR, Garcia L, Gourash W, Horlick M, Mitchell JE, Pomp A, Pories WJ, Purnell JQ, Singh A, Spaniolas K, Thirlby R, Wolfe BM, Yanovski SZ. Seven-year weight trajectories and health outcomes in the longitudinal assessment of bariatric surgery (LABS) study. JAMA Surg. 2018;153(5):427–434. doi: 10.1001/jamasurg.2017.5025.
    1. 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):734–740. doi: 10.1097/01.sla.0000217592.04061.d5.
    1. Sun YV, Hu YJ. Integrative analysis of multi-omics data for discovery and functional studies of complex human diseases. Adv Genet. 2016;93:147–190. doi: 10.1016/bs.adgen.2015.11.004.
    1. Olivier M, Asmis R, Hawkins GA, Howard TD, Cox LA. The need for multi-omics biomarker signatures in precision medicine. Int J Mol Sci. 2019;20(19):4781. doi: 10.3390/ijms20194781.
    1. Jacob M, Lopata AL, Dasouki M, Abdel Rahman AM. Metabolomics toward personalized medicine. Mass Spectrom Rev. 2019;38(3):221–238. doi: 10.1002/mas.21548.
    1. Samczuk P, Ciborowski M, Kretowski A. Application of metabolomics to study effects of bariatric surgery. J Diabetes Res. 2018;2018:6270875. doi: 10.1155/2018/6270875.
    1. Luo JN, Sheu EG. Do serum metabolites predict weight regain following bariatric surgery? Dig Dis Sci. 2020;65(4):922–924. doi: 10.1007/s10620-019-05792-3.
    1. Peterli R, Steinert RE, Woelnerhanssen B, Peters T, Christoffel-Courtin C, Gass M, Kern B, von Fluee M, Beglinger C. Metabolic and hormonal changes after laparoscopic Roux-en-Y gastric bypass and sleeve gastrectomy: a randomized, prospective trial. Obes Surg. 2012;22(5):740–748. doi: 10.1007/s11695-012-0622-3.
    1. Floegel A, Stefan N, Yu Z, Mühlenbruch K, Drogan D, Joost HG, Fritsche A, Häring HU, de Angelis MH, Peters A, Roden M, Prehn C, Wang-Sattler R, Illig T, Schulze MB, Adamski J, Boeing H, Pischon T. Identification of serum metabolites associated with risk of type 2 diabetes using a targeted metabolomic approach. Diabetes. 2013;62(2):639–48. 10.2337/db12-0495.
    1. Malin SK, Kashyap SR. Effects of various gastrointestinal procedures on β-cell function in obesity and type 2 diabetes. Surg Obes Relat Dis. 2016;12(6):1213–1219. doi: 10.1016/j.soard.2016.02.035.
    1. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hróbjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S, McGuinness LA, Stewart LA, Thomas J, Tricco AC, Welch VA, Whiting P, Moher D. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. PLoS Med. 2021;18(3):e1003583. doi: 10.1371/journal.pmed.1003583.
    1. Luo P, Yu H, Zhao X, Bao Y, Hong CS, Zhang P, Tu Y, Yin P, Gao P, Wei L, Zhuang Z, Jia W, Xu G. Metabolomics study of Roux-en-Y gastric bypass surgery (RYGB) to treat type 2 diabetes patients based on ultraperformance liquid chromatography-mass spectrometry. J Proteome Res. 2016;15(4):1288–1299. doi: 10.1021/acs.jproteome.6b00022.
    1. Magkos F, Bradley D, Schweitzer GG, Finck BN, Eagon JC, Ilkayeva O, Newgard CB, Klein S. Effect of Roux-en-Y gastric bypass and laparoscopic adjustable gastric banding on branched-chain amino acid metabolism. Diabetes. 2013;62(8):2757–2761. doi: 10.2337/db13-0185.
    1. Mutch DM, Fuhrmann JC, Rein D, Wiemer JC, Bouillot JL, Poitou C, Clément K. Metabolite profiling identifies candidate markers reflecting the clinical adaptations associated with Roux-en-Y gastric bypass surgery. PLoS One. 2009;4(11):e7905. doi: 10.1371/journal.pone.0007905.
    1. Narath SH, Mautner SI, Svehlikova E, Schultes B, Pieber TR, Sinner FM, Gander E, Libiseller G, Schimek MG, Sourij H, Magnes C. An untargeted metabolomics approach to characterize short-term and long-term metabolic changes after bariatric surgery. PLoS One. 2016;11(9):e0161425. doi: 10.1371/journal.pone.0161425.
    1. Palau-Rodriguez M, Tulipani S, Marco-Ramell A, Miñarro A, Jáuregui O, Sanchez-Pla A, Ramos-Molina B, Tinahones FJ, Andres-Lacueva C. Metabotypes of response to bariatric surgery independent of the magnitude of weight loss. PLoS One. 2018;13(6):e0198214. doi: 10.1371/journal.pone.0198214.
    1. Wijayatunga NN, Sams VG, Dawson JA, Mancini ML, Mancini GJ, Moustaid-Moussa N. Roux-en-Y gastric bypass surgery alters serum metabolites and fatty acids in patients with morbid obesity. Diabetes Metab Res Rev. 2018;34(8):e3045. doi: 10.1002/dmrr.3045.
    1. Yao J, Kovalik JP, Lai OF, Lee PC, Eng A, Chan WH, Tham KW, Lim E, Bee YM, Tan HC. Comprehensive assessment of the effects of sleeve gastrectomy on glucose, lipid, and amino acid metabolism in Asian individuals with morbid obesity. Obes Surg. 2019;29(1):149–158. doi: 10.1007/s11695-018-3487-2.
    1. Yoshida N, Kitahama S, Yamashita T, Hirono Y, Tabata T, Saito Y, Shinohara R, Nakashima H, Emoto T, Hirota Y, Takahashi T, Ogawa W, Hirata KI. Metabolic alterations in plasma after laparoscopic sleeve gastrectomy. J Diabetes Investig. 2021;12(1):123–129. doi: 10.1111/jdi.13328.
    1. Arora T, Velagapudi V, Pournaras DJ, Welbourn R, le Roux CW, Orešič M, Bäckhed F. Roux-en-Y gastric bypass surgery induces early plasma metabolomic and lipidomic alterations in humans associated with diabetes remission. PLoS One. 2015;10(5):e0126401. doi: 10.1371/journal.pone.0126401.
    1. Dadson P, Rebelos E, Honka H, Juárez-Orozco LE, Kalliokoski KK, Iozzo P, Teuho J, Salminen P, Pihlajamäki J, Hannukainen JC, Nuutila P. Change in abdominal, but not femoral subcutaneous fat CT-radiodensity is associated with improved metabolic profile after bariatric surgery. Nutr Metab Cardiovasc Dis. 2020;30(12):2363–2371. doi: 10.1016/j.numecd.2020.07.010.
    1. Gralka E, Luchinat C, Tenori L, Ernst B, Thurnheer M, Schultes B. Metabolomic fingerprint of severe obesity is dynamically affected by bariatric surgery in a procedure-dependent manner. Am J Clin Nutr. 2015;102(6):1313–1322. doi: 10.3945/ajcn.115.110536.
    1. Khoo CM, Muehlbauer MJ, Stevens RD, Pamuklar Z, Chen J, Newgard CB, Torquati A. Postprandial metabolite profiles reveal differential nutrient handling after bariatric surgery compared with matched caloric restriction. Ann Surg. 2014;259(4):687–693. doi: 10.1097/SLA.0b013e318296633f.
    1. Kwon Y, Jang M, Lee Y, Ha J, Park S. Metabolomic analysis of the improvements in insulin secretion and resistance after sleeve gastrectomy: Implications of the novel biomarkers. Obes Surg. 2021;31(1):43–52. doi: 10.1007/s11695-020-04925-2.
    1. Laferrère B, Reilly D, Arias S, Swerdlow N, Gorroochurn P, Bawa B, Bose M, Teixeira J, Stevens RD, Wenner BR, Bain JR, Muehlbauer MJ, Haqq A, Lien L, Shah SH, Svetkey LP, Newgard CB. Differential metabolic impact of gastric bypass surgery versus dietary intervention in obese diabetic subjects despite identical weight loss. Sci Transl Med. 2011;3(80):80re82. 10.1126/scitranslmed.3002043.
    1. Lips MA, Van Klinken JB, van Harmelen V, Dharuri HK, t Hoen PA, Laros JF, van Ommen GJ, Janssen IM, Van Ramshorst B, Van Wagensveld BA, Swank DJ, Van Dielen F, Dane A, Harms A, Vreeken R, Hankemeier T, Smit JW, Pijl H, Willems van Dijk K. Roux-en-Y gastric bypass surgery, but not calorie restriction, reduces plasma branched-chain amino acids in obese women independent of weight loss or the presence of type 2 diabetes. Diabetes Care. 2014;37(12):3150–6. 10.2337/dc14-0195.
    1. Lopes TI, Geloneze B, Pareja JC, Calixto AR, Ferreira MM, Marsaioli AJ. Blood metabolome changes before and after bariatric surgery: a (1)H NMR-based clinical investigation. OMICS. 2015;19(5):318–327. doi: 10.1089/omi.2015.0009.
    1. Tan HC, Khoo CM, Tan MZ, Kovalik JP, Ng AC, Eng AK, Lai OF, Ching JH, Tham KW, Pasupathy S. The effects of sleeve gastrectomy and gastric bypass on branched-chain amino acid metabolism 1 year after bariatric surgery. Obes Surg. 2016;26(8):1830–1835. doi: 10.1007/s11695-015-2023-x.
    1. Tan HC, Hsu JW, Kovalik JP, Eng A, Chan WH, Khoo CM, Tai ES, Chacko S, Jahoor F. Branched-chain amino acid oxidation is elevated in adults with morbid obesity and decreases significantly after sleeve gastrectomy. J Nutr. 2020;150(12):3180–3189. doi: 10.1093/jn/nxaa298.
    1. Cabré N, Luciano-Mateo F, Baiges-Gayà G, Fernández-Arroyo S, Rodríguez-Tomàs E, Hernández-Aguilera A, París M, Sabench F, Del Castillo D, López-Miranda J, Menéndez JA, Camps J, Joven J. Plasma metabolic alterations in patients with severe obesity and non-alcoholic steatohepatitis. Aliment Pharmacol Ther. 2020;51(3):374–387. doi: 10.1111/apt.15606.
    1. Hubal MJ, Nadler EP, Ferrante SC, Barberio MD, Suh JH, Wang J, Dohm GL, Pories WJ, Mietus-Snyder M, Freishtat RJ. Circulating adipocyte-derived exosomal microRNAs associated with decreased insulin resistance after gastric bypass. Obesity. 2017;25(1):102–110. doi: 10.1002/oby.21709.
    1. Samczuk P, Luba M, Godzien J, Mastrangelo A, Hady HR, Dadan J, Barbas C, Gorska M, Kretowski A, Ciborowski M. Gear mechanism of bariatric interventions revealed by untargeted metabolomics. J Pharm Biomed Anal. 2018;151:219–226. doi: 10.1016/j.jpba.2018.01.016.
    1. Mendonça Machado N, Torrinhas RS, Sala P, Ishida RK, Guarda I, Moura EGH, Sakai P, Santo MA, Linetzky WD. Type 2 diabetes metabolic improvement after Roux-en-Y gastric bypass may include a compensatory mechanism that balances fatty acid β and ω oxidation. JPEN J Parenter Enteral Nutr. 2020;44(8):1417–1427. doi: 10.1002/jpen.1960.
    1. Jüllig M, Yip S, Xu A, Smith G, Middleditch M, Booth M, Babor R, Beban G, Murphy R. Lower fetuin-A, retinol binding protein 4 and several metabolites after gastric bypass compared to sleeve gastrectomy in patients with type 2 diabetes. PLoS One. 2014;9(5):e96489. doi: 10.1371/journal.pone.0096489.
    1. Ocaña-Wilhelmi L, Cardona F, Garrido-Sanchez L, Fernandez-Garcia D, Tinahones FJ, Ramos-Molina B. Change in serum polyamine metabolome pattern after bariatric surgery in obese patients with metabolic syndrome. Surg Obes Relat Dis. 2020;16(2):306–311. doi: 10.1016/j.soard.2019.10.024.
    1. Sarosiek K, Pappan KL, Gandhi AV, Saxena S, Kang CY, McMahon H, Chipitsyna GI, Tichansky DS, Arafat HA. Conserved metabolic changes in nondiabetic and type 2 diabetic bariatric surgery patients: Global metabolomic pilot study. J Diabetes Res. 2016;2016:3467403. doi: 10.1155/2016/3467403.
    1. Oberbach A, Blüher M, Wirth H, Till H, Kovacs P, Kullnick Y, Schlichting N, Tomm JM, Rolle-Kampczyk U, Murugaiyan J, Binder H, Dietrich A, von Bergen M. Combined proteomic and metabolomic profiling of serum reveals association of the complement system with obesity and identifies novel markers of body fat mass changes. J Proteome Res. 2011;10(10):4769–4788. doi: 10.1021/pr2005555.
    1. Herzog K, Berggren J, Al Majdoub M, Balderas Arroyo C, Lindqvist A, Hedenbro J, Groop L, Wierup N, Spégel P. Metabolic effects of gastric bypass surgery: Is it all about calories? Diabetes. 2020;69(9):2027–2035. doi: 10.2337/db20-0131.
    1. Fiamoncini J, Fernandes Barbosa C, Arnoni Junior JR, Araújo Junior JC, Taglieri C, Szego T, Gelhaus B, Possolo de Souza H, Daniel H, Martins de Lima T. Roux-en-Y gastric bypass surgery induces distinct but frequently transient effects on acylcarnitine, bile acid and phospholipid levels. Metabolites. 2018;8(4). 10.3390/metabo8040083.
    1. Mika A, Kaczynski Z, Stepnowski P, Kaczor M, Proczko-Stepaniak M, Kaska L, Sledzinski T. Potential application of H-1 NMR for routine serum lipidome analysis - evaluation of effects of bariatric surgery. Sci Rep. 2017;7. 10.1038/s41598-017-15346-0.
    1. Ahlin S, Cefalù C, Bondia-Pons I, Capristo E, Marini L, Gastaldelli A, Mingrone G, Nolan JJ. Bile acid changes after metabolic surgery are linked to improvement in insulin sensitivity. Br J Surg. 2019;106(9):1178–1186. doi: 10.1002/bjs.11208.
    1. Ramos-Molina B, Castellano-Castillo D, Alcaide-Torres J, Pastor Ó, de Luna DR, Salas-Salvadó J, López-Moreno J, Fernández-García JC, Macías-González M, Cardona F, Tinahones FJ. Differential effects of restrictive and malabsorptive bariatric surgery procedures on the serum lipidome in obese subjects. J Clin Lipidol. 2018;12(6):1502–1512. doi: 10.1016/j.jacl.2018.07.006.
    1. Ahmad NN, Pfalzer A, Kaplan LM. Roux-en-Y gastric bypass normalizes the blunted postprandial bile acid excursion associated with obesity. Int J Obes. 2013;37(12):1553–1559. doi: 10.1038/ijo.2013.38.
    1. Kindel TL, Krause C, Helm MC, McBride CL, Oleynikov D, Thakare R, Alamoudi J, Kothari V, Alnouti Y, Kohli R. Increased glycine-amidated hyocholic acid correlates to improved early weight loss after sleeve gastrectomy. Surg Endosc Other Interv Tech. 2018;32(2):805–812. doi: 10.1007/s00464-017-5747-y.
    1. Kayser BD, Lhomme M, Dao MC, Ichou F, Bouillot JL, Prifti E, Kontush A, Chevallier JM, Aron-Wisnewsky J, Dugail I, Clément K. Serum lipidomics reveals early differential effects of gastric bypass compared with banding on phospholipids and sphingolipids independent of differences in weight loss. Int J Obes (Lond) 2017;41(6):917–925. doi: 10.1038/ijo.2017.63.
    1. Friedrich N, Budde K, Wolf T, Jungnickel A, Grotevendt A, Dressler M, Völzke H, Blüher M, Nauck M, Lohmann T, Wallaschofksi H. Short-term changes of the urine metabolome after bariatric surgery. OMICS. 2012;16(11):612–620. doi: 10.1089/omi.2012.0066.
    1. Pereira SS, Jarak I, Carvalho RA, Oliveira PF, Alves MG, Guimarães M, Almeida R, Pereira AM, Albrechtsen NJW, Holst JJ, Nora M, Monteiro MP. Different malabsorptive obesity surgery interventions result in distinct postprandial amino acid metabolomic signatures. Obes Surg. 2020;30(10):4019–4028. doi: 10.1007/s11695-020-04774-z.
    1. Jarak I, Pereira SS, Carvalho RA, Oliveira PF, Alves MG, Guimarães M, Albrechtsen NJW, Holst JJ, Nora M, Monteiro MP. Gastric bypass with different biliopancreatic limb lengths results in similar post-absorptive metabolomics profiles. Obes Surg. 2020;30(3):1068–1078. doi: 10.1007/s11695-019-04294-5.
    1. Kwon Y, Jang M, Lee Y, Ha J, Park S. Amino acid metabolites and slow weight loss in the early postoperative period after sleeve gastrectomy. J Clin Med. 2020;9(8). 10.3390/jcm9082348.
    1. Abidi W, Nestoridi E, Feldman H, Stefater M, Clish C, Thompson CC, Stylopoulos N. Differential metabolomic signatures in patients with weight regain and sustained weight loss after gastric bypass surgery: a pilot study. Dig Dis Sci. 2020;65(4):1144–1154. doi: 10.1007/s10620-019-05714-3.
    1. Shantavasinkul PC, Muehlbauer MJ, Bain JR, Ilkayeva OR, Craig DM, Newgard CB, Svetkey LP, Shah SH, Torquati A. Improvement in insulin resistance after gastric bypass surgery is correlated with a decline in plasma 2-hydroxybutyric acid. Surg Obes Relat Dis. 2018;14(8):1126–1132. doi: 10.1016/j.soard.2018.03.033.
    1. Samczuk P, Hady HR, Adamska-Patruno E, Citko A, Dadan J, Barbas C, Kretowski A, Ciborowski M. In-and-out molecular changes linked to the type 2 diabetes remission after bariatric surgery: an influence of gut microbes on mitochondria metabolism. Int J Mol Sci. 2018;19(12). 10.3390/ijms19123744.
    1. Lopes TI, Geloneze B, Pareja JC, Calixto AR, Ferreira MM, Marsaioli AJ. Omics prospective monitoring of bariatric surgery: Roux-En-Y gastric bypass outcomes using mixed-meal tolerance test and time-resolved (1)H NMR-based metabolomics. OMICS. 2016;20(7):415–423. doi: 10.1089/omi.2016.0061.
    1. Yu H, Ni Y, Bao Y, Zhang P, Zhao A, Chen T, Xie G, Tu Y, Zhang L, Su M, Wei L, Jia W, Jia W. Chenodeoxycholic acid as a potential prognostic marker for Roux-en-Y gastric bypass in Chinese obese patients. J Clin Endocrinol Metab. 2015;100(11):4222–4230. doi: 10.1210/jc.2015-2884.
    1. Zhao L, Ni Y, Yu H, Zhang P, Zhao A, Bao Y, Liu J, Chen T, Xie G, Panee J, Chen W, Rajani C, Wei R, Su M, Jia W, Jia W. Serum stearic acid/palmitic acid ratio as a potential predictor of diabetes remission after Roux-en-Y gastric bypass in obesity. Faseb j. 2017;31(4):1449–1460. doi: 10.1096/fj.201600927R.
    1. Li QR, Wang ZM, Albrechtsen NJW, Wang DD, Su ZD, Gao XF, Wu QQ, Zhang HP, Zhu L, Li RX, Jacobsen S, Jorgensen NB, Dirksen C, Bojsen-Moller KN, Petersen JS, Madsbad S, Clausen TR, Diderichsen B, Chen LN, Holst JJ, Zeng R, Wu JR. Systems signatures reveal unique remission-path of type 2 diabetes following Roux-en-Y gastric bypass surgery. EBioMedicine. 2018;28:234–240. doi: 10.1016/j.ebiom.2018.01.018.
    1. Ha J, Jang M, Kwon Y, Park YS, Park DJ, Lee JH, Lee HJ, Ha TK, Kim YJ, Han SM, Han SU, Heo Y, Park S. Metabolomic profiles predict diabetes remission after bariatric surgery. J Clin Med. 2020;9(12). 10.3390/jcm9123897.
    1. Kwon HN, Lee YJ, Kang JH, Choi JH, An YJ, Kang S, Lee DH, Suh YJ, Heo Y, Park S. Prediction of glycated hemoglobin levels at 3 months after metabolic surgery based on the 7-day plasma metabolic profile. PLoS One. 2014;9(11):e109609. doi: 10.1371/journal.pone.0109609.
    1. Rauschert S, Uhl O, Koletzko B, Hellmuth C. Metabolomic biomarkers for obesity in humans: a short review. Ann Nutr Metab. 2014;64(3–4):314–324. doi: 10.1159/000365040.
    1. Newgard CB, An J, Bain JR, Muehlbauer MJ, Stevens RD, Lien LF, Haqq AM, Shah SH, Arlotto M, Slentz CA, Rochon J, Gallup D, Ilkayeva O, Wenner BR, Yancy WS, Jr, Eisenson H, Musante G, Surwit RS, Millington DS, Butler MD, Svetkey LP. A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab. 2009;9(4):311–326. doi: 10.1016/j.cmet.2009.02.002.
    1. She P, Van Horn C, Reid T, Hutson SM, Cooney RN, Lynch CJ. Obesity-related elevations in plasma leucine are associated with alterations in enzymes involved in branched-chain amino acid metabolism. Am J Physiol Endocrinol Metab. 2007;293(6):E1552–1563. doi: 10.1152/ajpendo.00134.2007.
    1. Guasch-Ferré M, Hruby A, Toledo E, Clish CB, Martínez-González MA, Salas-Salvadó J, Hu FB. Metabolomics in prediabetes and diabetes: a systematic review and meta-analysis. Diabetes Care. 2016;39(5):833–846. doi: 10.2337/dc15-2251.
    1. Felig P, Marliss E, Cahill GF., Jr Plasma amino acid levels and insulin secretion in obesity. N Engl J Med. 1969;281(15):811–816. doi: 10.1056/nejm196910092811503.
    1. Alves A, Bassot A, Bulteau A-L, Pirola L, Morio B. Glycine metabolism and its alterations in obesity and metabolic diseases. Nutrients. 2019;11(6):1356. doi: 10.3390/nu11061356.
    1. Wang-Sattler R, Yu Z, Herder C, Messias AC, Floegel A, He Y, Heim K, Campillos M, Holzapfel C, Thorand B, Grallert H, Xu T, Bader E, Huth C, Mittelstrass K, Döring A, Meisinger C, Gieger C, Prehn C, Roemisch-Margl W, Carstensen M, Xie L, Yamanaka-Okumura H, Xing G, Ceglarek U, Thiery J, Giani G, Lickert H, Lin X, Li Y, Boeing H, Joost HG, de Angelis MH, Rathmann W, Suhre K, Prokisch H, Peters A, Meitinger T, Roden M, Wichmann HE, Pischon T, Adamski J, Illig T. Novel biomarkers for pre-diabetes identified by metabolomics. Mol Syst Biol. 2012;8:615. doi: 10.1038/msb.2012.43.
    1. Rowland I, Gibson G, Heinken A, Scott K, Swann J, Thiele I, Tuohy K. Gut microbiota functions: Metabolism of nutrients and other food components. Eur J Nutr. 2018;57(1):1–24. doi: 10.1007/s00394-017-1445-8.
    1. Magne F, Gotteland M, Gauthier L, Zazueta A, Pesoa S, Navarrete P, Balamurugan R. The Firmicutes/Bacteroidetes ratio: a relevant marker of gut dysbiosis in obese patients? Nutrients. 2020;12(5). 10.3390/nu12051474.
    1. Smith EA, Macfarlane GT. Enumeration of human colonic bacteria producing phenolic and indolic compounds: Effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism. J Appl Bacteriol. 1996;81(3):288–302. doi: 10.1111/j.1365-2672.1996.tb04331.x.
    1. Zhang YJ, Li S, Gan RY, Zhou T, Xu DP, Li HB. Impacts of gut bacteria on human health and diseases. Int J Mol Sci. 2015;16(4):7493–7519. doi: 10.3390/ijms16047493.
    1. Murphy R, Tsai P, Jüllig M, Liu A, Plank L, Booth M. Differential changes in gut microbiota after gastric bypass and sleeve gastrectomy bariatric surgery vary according to diabetes remission. Obes Surg. 2017;27(4):917–925. doi: 10.1007/s11695-016-2399-2.
    1. Ohland CL, Jobin C. Microbial activities and intestinal homeostasis: a delicate balance between health and disease. Cell Mol Gastroenterol Hepatol. 2015;1(1):28–40. doi: 10.1016/j.jcmgh.2014.11.004.
    1. Pereira PR, Guimarães M, Morais T, Pereira SS, Nora M, Monteiro MP. Diabetic and elder patients experience superior cardiovascular benefits after gastric bypass induced weight loss. Front Endocrinol (Lausanne) 2018;9:718. doi: 10.3389/fendo.2018.00718.
    1. Ammar W, Basset HA, Al Faramawy A, Hegazy T, Sharaf Y. Bariatric surgery and cardiovascular outcome. Egypt Heart J. 2020;72(1):67. doi: 10.1186/s43044-020-00096-8.
    1. Trøseid M, Hov JR, Nestvold TK, Thoresen H, Berge RK, Svardal A, Lappegård KT. Major increase in microbiota-dependent proatherogenic metabolite TMAO one year after bariatric surgery. Metab Syndr Relat Disord. 2016;14(4):197–201. doi: 10.1089/met.2015.0120.
    1. He X, Slupsky CM. Metabolic fingerprint of dimethyl sulfone (DMSO2) in microbial-mammalian co-metabolism. J Proteome Res. 2014;13(12):5281–5292. doi: 10.1021/pr500629t.
    1. Patel DP, Krausz KW, Xie C, Beyoğlu D, Gonzalez FJ, Idle JR. Metabolic profiling by gas chromatography-mass spectrometry of energy metabolism in high-fat diet-fed obese mice. PLoS One. 2017;12(5):e0177953. doi: 10.1371/journal.pone.0177953.
    1. Goncalves D, Barataud A, De Vadder F, Vinera J, Zitoun C, Duchampt A, Mithieux G. Bile routing modification reproduces key features of gastric bypass in rat. Ann Surg. 2015;262(6):1006–1015. doi: 10.1097/sla.0000000000001121.
    1. Thomas C, Gioiello A, Noriega L, Strehle A, Oury J, Rizzo G, Macchiarulo A, Yamamoto H, Mataki C, Pruzanski M, Pellicciari R, Auwerx J, Schoonjans K. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 2009;10(3):167–177. doi: 10.1016/j.cmet.2009.08.001.
    1. Russell DW. Fifty years of advances in bile acid synthesis and metabolism. J Lipid Res. 2009;50Suppl(Suppl):S120–5. 10.1194/jlr.R800026-JLR200.
    1. 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. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature. 2006;439(7075):484–489. doi: 10.1038/nature04330.
    1. Nagao K, Yanagita T. Medium-chain fatty acids: functional lipids for the prevention and treatment of the metabolic syndrome. Pharmacol Res. 2010;61(3):208–212. doi: 10.1016/j.phrs.2009.11.007.
    1. Han JR, Deng B, Sun J, Chen CG, Corkey BE, Kirkland JL, Ma J, Guo W. Effects of dietary medium-chain triglyceride on weight loss and insulin sensitivity in a group of moderately overweight free-living type 2 diabetic Chinese subjects. Metabolism. 2007;56(7):985–991. doi: 10.1016/j.metabol.2007.03.005.
    1. Wein S, Wolffram S, Schrezenmeir J, Gasperiková D, Klimes I, Seböková E. Medium-chain fatty acids ameliorate insulin resistance caused by high-fat diets in rats. Diabetes Metab Res Rev. 2009;25(2):185–194. doi: 10.1002/dmrr.925.
    1. Poisson J-PG, Cunnane SC. Long-chain fatty acid metabolism in fasting and diabetes: relation between altered desaturase activity and fatty acid composition. J Nutr Biochem. 1991;2(2):60–70. 10.1016/0955-2863(91)90030-9.
    1. Lemaitre RN, Fretts AM, Sitlani CM, Biggs ML, Mukamal K, King IB, Song X, Djoussé L, Siscovick DS, McKnight B, Sotoodehnia N, Kizer JR, Mozaffarian D. Plasma phospholipid very-long-chain saturated fatty acids and incident diabetes in older adults: The cardiovascular health study. Am J Clin Nutr. 2015;101(5):1047–1054. doi: 10.3945/ajcn.114.101857.
    1. Liang H, Tantiwong P, Sriwijitkamol A, Shanmugasundaram K, Mohan S, Espinoza S, Defronzo RA, Dubé JJ, Musi N. Effect of a sustained reduction in plasma free fatty acid concentration on insulin signalling and inflammation in skeletal muscle from human subjects. J Physiol. 2013;591(11):2897–2909. doi: 10.1113/jphysiol.2012.247510.
    1. Rauschert S, Uhl O, Koletzko B, Kirchberg F, Mori TA, Huang R-C, Beilin LJ, Hellmuth C, Oddy WH. Lipidomics reveals associations of phospholipids with obesity and insulin resistance in young adults. J Clin Endocrinol Metab. 2016;101(3):871–879. doi: 10.1210/jc.2015-3525.
    1. Monzo-Beltran L, Vazquez-Tarragón A, Cerdà C, Garcia-Perez P, Iradi A, Sánchez C, Climent B, Tormos C, Vázquez-Prado A, Girbés J, Estáñ N, Blesa S, Cortés R, Chaves FJ, Sáez GT. One-year follow-up of clinical, metabolic and oxidative stress profile of morbid obese patients after laparoscopic sleeve gastrectomy. 8-oxo-dG as a clinical marker. Redox Biol. 2017;12:389–402. 10.1016/j.redox.2017.02.003.
    1. Iqbal J, Walsh MT, Hammad SM, Hussain MM. Sphingolipids and lipoproteins in health and metabolic disorders. Trends Endocrinol Metab. 2017;28(7):506–18. 10.1016/j.tem.2017.03.005.

Source: PubMed

3
Subscribe