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Published in: Obesity Surgery 1/2019

01-01-2019 | Original Contributions

Comprehensive Assessment of the Effects of Sleeve Gastrectomy on Glucose, Lipid, and Amino Acid Metabolism in Asian Individuals with Morbid Obesity

Authors: Jie Yao, Jean-Paul Kovalik, Oi Fah Lai, Phong Ching Lee, Alvin Eng, Weng Hoong Chan, Kwang Wei Tham, Eugene Lim, Yong Mong Bee, Hong Chang Tan

Published in: Obesity Surgery | Issue 1/2019

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Abstract

Background

Obesity-induced insulin resistance leads to abnormalities in glucose, lipid, and amino acid metabolism. Our study examined the differences in insulin-mediated glucose, amino acid, and lipid metabolism between morbidly obese subjects with non-obese controls and the associated changes following sleeve gastrectomy (SG).

Methods

Non-obese controls and individuals with morbid obesity and scheduled for SG were recruited. Metabolic assessments were performed for all subjects at baseline and at 6 months after SG for eight subjects. The hyperinsulinemic-euglycemic clamp technique together with comprehensive metabolomic profiling was used to quantify insulin-mediated glucose, amino acid, and lipid metabolism.

Results

Eleven morbidly obese non-diabetic subjects scheduled for SG and nine non-obese controls were recruited. Compared to controls, obese subjects had significantly lower glucose uptake (4.4 ± 0.6 vs. 17.3 ± 2.4 mg/kg FFM/min per μU/mL·100) and higher concentration of branched-chain amino acids (BCAAs, 332.5 ± 26.8 vs. 235.3 ± 11.0 μM), non-esterified fatty acid (52.9 ± 9.9 vs. 25.6 ± 6.7 μM), and lipid-related acylcarnitines (intermediate chain 389.8 ± 32.5 vs. 285.9 ± 20.5; long chain 301.7 ± 22.1 vs. 236.0 ± 13.3 nM) during insulin clamp. Body weight significantly reduced at 6 months after bariatric surgery (92.5 ± 6.3 vs. 115.2 ± 6.9 kg), together with improvements in insulin-mediated glucose uptake, and suppression of BCAAs, non-esterified fatty acids, and lipid-related metabolites.

Conclusions

Morbid obesity in Asian individuals was associated with impairment in the regulatory actions of insulin on glucose, amino acid, and lipid metabolism, and these obesity-induced regulatory dysfunctions improved significantly 6 months after SG.
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Literature
1.
go back to reference Heymsfield SB, Wadden TA. Mechanisms, pathophysiology, and management of obesity. N Engl J Med. 2017;376(3):254–66.CrossRef Heymsfield SB, Wadden TA. Mechanisms, pathophysiology, and management of obesity. N Engl J Med. 2017;376(3):254–66.CrossRef
2.
go back to reference Torgerson JS, Hauptman J, Boldrin MN, et al. XENical in the prevention of diabetes in obese subjects (XENDOS) study: a randomized study of orlistat as an adjunct to lifestyle changes for the prevention of type 2 diabetes in obese patients. Diabetes Care. 2004;27(1):155–61. Torgerson JS, Hauptman J, Boldrin MN, et al. XENical in the prevention of diabetes in obese subjects (XENDOS) study: a randomized study of orlistat as an adjunct to lifestyle changes for the prevention of type 2 diabetes in obese patients. Diabetes Care. 2004;27(1):155–61.
3.
go back to reference Cercato C, Roizenblatt VA, Leanca CC, et al. A randomized double-blind placebo-controlled study of the long-term efficacy and safety of diethylpropion in the treatment of obese subjects. Int J Obes (2005). 2009;33(8):857–65. Cercato C, Roizenblatt VA, Leanca CC, et al. A randomized double-blind placebo-controlled study of the long-term efficacy and safety of diethylpropion in the treatment of obese subjects. Int J Obes (2005). 2009;33(8):857–65.
4.
go back to reference Sjostrom L, Narbro K, Sjostrom CD, et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med. 2007;357(8):741–52. Sjostrom L, Narbro K, Sjostrom CD, et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med. 2007;357(8):741–52.
5.
go back to reference Grenier-Larouche T, Carreau AM, Carpentier AC. Early metabolic improvement after bariatric surgery: the first steps toward remission of type 2 diabetes. Can J Diabetes 2017;41(4):418–425. Epub 2017/03/21. eng. Grenier-Larouche T, Carreau AM, Carpentier AC. Early metabolic improvement after bariatric surgery: the first steps toward remission of type 2 diabetes. Can J Diabetes 2017;41(4):418–425. Epub 2017/03/21. eng.
6.
go back to reference Dimitriadis G, Mitrou P, Lambadiari V, et al. Insulin effects in muscle and adipose tissue. Diabetes Res Clin Pract. 2011;93(Suppl 1):S52–9. Dimitriadis G, Mitrou P, Lambadiari V, et al. Insulin effects in muscle and adipose tissue. Diabetes Res Clin Pract. 2011;93(Suppl 1):S52–9.
7.
go back to reference Caballero B, Wurtman RJ. Differential effects of insulin resistance on leucine and glucose kinetics in obesity. Metabolism: Clin Exp. 1991;40(1):51–8.CrossRef Caballero B, Wurtman RJ. Differential effects of insulin resistance on leucine and glucose kinetics in obesity. Metabolism: Clin Exp. 1991;40(1):51–8.CrossRef
8.
go back to reference Newgard CB, An J, Bain JR, et al. A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab. 2009;9(4):311–26. Newgard CB, An J, Bain JR, et al. A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab. 2009;9(4):311–26.
9.
go back to reference Mihalik SJ, Goodpaster BH, Kelley DE, et al. Increased levels of plasma acylcarnitines in obesity and type 2 diabetes and identification of a marker of glucolipotoxicity. Obesity (Silver Spring, Md). 2010 Sep;18(9):1695–700. Mihalik SJ, Goodpaster BH, Kelley DE, et al. Increased levels of plasma acylcarnitines in obesity and type 2 diabetes and identification of a marker of glucolipotoxicity. Obesity (Silver Spring, Md). 2010 Sep;18(9):1695–700.
10.
go back to reference Laferrere B, Reilly D, Arias S, et al. Differential metabolic impact of gastric bypass surgery versus dietary intervention in obese diabetic subjects despite identical weight loss. Sci Transl Med. 2011;3(80):80re2. Laferrere B, Reilly D, Arias S, et al. Differential metabolic impact of gastric bypass surgery versus dietary intervention in obese diabetic subjects despite identical weight loss. Sci Transl Med. 2011;3(80):80re2.
11.
go back to reference Khoo CM, Muehlbauer MJ, Stevens RD, et al. Postprandial metabolite profiles reveal differential nutrient handling after bariatric surgery compared with matched caloric restriction. Ann Surg. 2014 Apr;259(4):687–93. Khoo CM, Muehlbauer MJ, Stevens RD, et al. Postprandial metabolite profiles reveal differential nutrient handling after bariatric surgery compared with matched caloric restriction. Ann Surg. 2014 Apr;259(4):687–93.
12.
go back to reference Sinclair P, Docherty N, le Roux CW. Metabolic effects of bariatric surgery. Clin Chem. 2018;64(1):72–81.CrossRefPubMed Sinclair P, Docherty N, le Roux CW. Metabolic effects of bariatric surgery. Clin Chem. 2018;64(1):72–81.CrossRefPubMed
13.
go back to reference Lomanto D, Lee WJ, Goel R, et al. Bariatric surgery in Asia in the last 5 years (2005-2009). Obes Surg. 2012;22(3):502–6. Lomanto D, Lee WJ, Goel R, et al. Bariatric surgery in Asia in the last 5 years (2005-2009). Obes Surg. 2012;22(3):502–6.
14.
go back to reference Toh BC, Chan WH, Eng AKH, et al. Five-year long-term clinical outcome after bariatric metabolic surgery: a multi-ethnic Asian population in Singapore. Diabetes Obes Metab. 2018;20 Toh BC, Chan WH, Eng AKH, et al. Five-year long-term clinical outcome after bariatric metabolic surgery: a multi-ethnic Asian population in Singapore. Diabetes Obes Metab. 2018;20
15.
go back to reference Chan JC, Malik V, Jia W, et al. Diabetes in Asia: epidemiology, risk factors, and pathophysiology. JAMA. 2009;301(20):2129–40. Chan JC, Malik V, Jia W, et al. Diabetes in Asia: epidemiology, risk factors, and pathophysiology. JAMA. 2009;301(20):2129–40.
16.
go back to reference Nanditha A, Ma RC, Ramachandran A, et al. Diabetes in Asia and the Pacific: implications for the global epidemic. Diabetes Care. 2016;39(3):472–85. Nanditha A, Ma RC, Ramachandran A, et al. Diabetes in Asia and the Pacific: implications for the global epidemic. Diabetes Care. 2016;39(3):472–85.
17.
go back to reference Tan HC, Khoo CM, Tan MZ, et al. The effects of sleeve gastrectomy and gastric bypass on branched-chain amino acid metabolism 1 year after bariatric surgery. Obes Surg. 2016;26(8):1830–5. Tan HC, Khoo CM, Tan MZ, et al. The effects of sleeve gastrectomy and gastric bypass on branched-chain amino acid metabolism 1 year after bariatric surgery. Obes Surg. 2016;26(8):1830–5.
18.
go back to reference Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985 Jul;28(7):412–9. Epub 1985/07/01. eng Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985 Jul;28(7):412–9. Epub 1985/07/01. eng
19.
go back to reference Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22(9):1462–70.CrossRef Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22(9):1462–70.CrossRef
20.
go back to reference DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Phys. 1979;237(3):E214–23. DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Phys. 1979;237(3):E214–23.
21.
go back to reference Kim SH. Measurement of insulin action: a tribute to Sir Harold Himsworth. Diabetic Medicine. 2011;28(12):1487–93.CrossRefPubMed Kim SH. Measurement of insulin action: a tribute to Sir Harold Himsworth. Diabetic Medicine. 2011;28(12):1487–93.CrossRefPubMed
22.
go back to reference Vencio S, Stival A, Halpern A, et al. Early mechanisms of glucose improvement following laparoscopic ileal interposition associated with a sleeve gastrectomy evaluated by the euglycemic hyperinsulinemic clamp in type 2 diabetic patients with BMI below 35. Dig Surg. 2011;28(4):293–8. Vencio S, Stival A, Halpern A, et al. Early mechanisms of glucose improvement following laparoscopic ileal interposition associated with a sleeve gastrectomy evaluated by the euglycemic hyperinsulinemic clamp in type 2 diabetic patients with BMI below 35. Dig Surg. 2011;28(4):293–8.
23.
go back to reference Immonen H, Hannukainen JC, Iozzo P, et al. Effect of bariatric surgery on liver glucose metabolism in morbidly obese diabetic and non-diabetic patients. J Hepatol. 2014 Feb;60(2):377–83. Immonen H, Hannukainen JC, Iozzo P, et al. Effect of bariatric surgery on liver glucose metabolism in morbidly obese diabetic and non-diabetic patients. J Hepatol. 2014 Feb;60(2):377–83.
24.
go back to reference Bradley D, Magkos F, Eagon JC, et al. Matched weight loss induced by sleeve gastrectomy or gastric bypass similarly improves metabolic function in obese subjects. Obesity (Silver Spring, Md). 2014;22(9):2026–31. Bradley D, Magkos F, Eagon JC, et al. Matched weight loss induced by sleeve gastrectomy or gastric bypass similarly improves metabolic function in obese subjects. Obesity (Silver Spring, Md). 2014;22(9):2026–31.
25.
go back to reference Casella G, Soricelli E, Castagneto-Gissey L, et al. Changes in insulin sensitivity and secretion after sleeve gastrectomy. Br J Surg. 2016;103(3):242–8. Casella G, Soricelli E, Castagneto-Gissey L, et al. Changes in insulin sensitivity and secretion after sleeve gastrectomy. Br J Surg. 2016;103(3):242–8.
26.
go back to reference Wang TJ, Larson MG, Vasan RS, et al. Metabolite profiles and the risk of developing diabetes. Nat Med. 2011;17(4):448–53. Wang TJ, Larson MG, Vasan RS, et al. Metabolite profiles and the risk of developing diabetes. Nat Med. 2011;17(4):448–53.
28.
go back to reference Lips MA, Van Klinken JB, van Harmelen V, et al. 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. Lips MA, Van Klinken JB, van Harmelen V, et al. 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.
29.
go back to reference Jensen MD, Haymond MW. Protein metabolism in obesity: effects of body fat distribution and hyperinsulinemia on leucine turnover. Am J Clin Nutr. 1991;53(1):172–6.CrossRefPubMed Jensen MD, Haymond MW. Protein metabolism in obesity: effects of body fat distribution and hyperinsulinemia on leucine turnover. Am J Clin Nutr. 1991;53(1):172–6.CrossRefPubMed
30.
go back to reference Luzi L, Castellino P, DeFronzo RA. Insulin and hyperaminoacidemia regulate by a different mechanism leucine turnover and oxidation in obesity. Am J Phys. 1996;270(2 Pt 1):E273–81. Luzi L, Castellino P, DeFronzo RA. Insulin and hyperaminoacidemia regulate by a different mechanism leucine turnover and oxidation in obesity. Am J Phys. 1996;270(2 Pt 1):E273–81.
31.
go back to reference Magkos F, Bradley D, Schweitzer GG, et al. Effect of Roux-en-Y gastric bypass and laparoscopic adjustable gastric banding on branched-chain amino acid metabolism. Diabetes. 2013;62(8):2757–61. Magkos F, Bradley D, Schweitzer GG, et al. Effect of Roux-en-Y gastric bypass and laparoscopic adjustable gastric banding on branched-chain amino acid metabolism. Diabetes. 2013;62(8):2757–61.
32.
go back to reference Glynn EL, Piner LW, Huffman KM, et al. Impact of combined resistance and aerobic exercise training on branched-chain amino acid turnover, glycine metabolism and insulin sensitivity in overweight humans. Diabetologia. 2015;58(10):2324–35. Glynn EL, Piner LW, Huffman KM, et al. Impact of combined resistance and aerobic exercise training on branched-chain amino acid turnover, glycine metabolism and insulin sensitivity in overweight humans. Diabetologia. 2015;58(10):2324–35.
33.
go back to reference Wang W, Wu Z, Dai Z, et al. Glycine metabolism in animals and humans: implications for nutrition and health. Amino Acids. 2013 Sep;45(3):463–77. Wang W, Wu Z, Dai Z, et al. Glycine metabolism in animals and humans: implications for nutrition and health. Amino Acids. 2013 Sep;45(3):463–77.
34.
go back to reference Chng CL, Lim AY, Tan HC, et al. Physiological and metabolic changes during the transition from hyperthyroidism to euthyroidism in Graves’ disease. Thyroid : Off J Am Thyroid Assoc. 2016;26(10):1422–30. Chng CL, Lim AY, Tan HC, et al. Physiological and metabolic changes during the transition from hyperthyroidism to euthyroidism in Graves’ disease. Thyroid : Off J Am Thyroid Assoc. 2016;26(10):1422–30.
35.
go back to reference Camastra S, Gastaldelli A, Mari A, et al. Early and longer term effects of gastric bypass surgery on tissue-specific insulin sensitivity and beta cell function in morbidly obese patients with and without type 2 diabetes. Diabetologia. 2011;54(8):2093–102. Camastra S, Gastaldelli A, Mari A, et al. Early and longer term effects of gastric bypass surgery on tissue-specific insulin sensitivity and beta cell function in morbidly obese patients with and without type 2 diabetes. Diabetologia. 2011;54(8):2093–102.
36.
go back to reference Kelley DE, Goodpaster B, Wing RR, et al. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Phys. 1999;277(6 Pt 1):E1130–41. Kelley DE, Goodpaster B, Wing RR, et al. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Phys. 1999;277(6 Pt 1):E1130–41.
Metadata
Title
Comprehensive Assessment of the Effects of Sleeve Gastrectomy on Glucose, Lipid, and Amino Acid Metabolism in Asian Individuals with Morbid Obesity
Authors
Jie Yao
Jean-Paul Kovalik
Oi Fah Lai
Phong Ching Lee
Alvin Eng
Weng Hoong Chan
Kwang Wei Tham
Eugene Lim
Yong Mong Bee
Hong Chang Tan
Publication date
01-01-2019
Publisher
Springer US
Published in
Obesity Surgery / Issue 1/2019
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-018-3487-2

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