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Published in: Langenbeck's Archives of Surgery 6/2017

01-09-2017 | ORIGINAL ARTICLE

Gastric bypass simultaneously improves adipose tissue function and insulin-dependent type 2 diabetes mellitus

Authors: Adrian T. Billeter, Spiros Vittas, Barbara Israel, Katharina M. Scheurlen, Asa Hidmark, Thomas H. Fleming, Stefan Kopf, Markus W. Büchler, Beat P. Müller-Stich

Published in: Langenbeck's Archives of Surgery | Issue 6/2017

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Abstract

Objective

The underlying causes of type 2 diabetes (T2DM) remain poorly understood. Adipose tissue dysfunction with high leptin, inflammation, and increased oxidative stress may play a pivotal role in T2DM development in obese patients. Little is known about the changes in the adipose tissue after Roux-Y gastric bypass (RYGB) in non-severely obese patients (BMI < 35 kg/m2) and since these patients have more T2DM-associated complications than obese patients (“obesity paradox”), we investigated changes in adipose tissue function in a cohort of BMI <35 kg/m2 with insulin-dependent T2DM after RYGB surgery which resolves T2DM.

Methods

Twenty patients with insulin-dependent T2DM and BMI <35 kg/m2 underwent RYGB. Insulin-resistance, leptin, oxidative stress, and cytokines were determined over 24 months. Expression of cytokines and NF-kappaB pathway genes were measured in leukocytes (PBMC). Adipose tissue inflammation was examined histologically preoperatively and 24 months after RGYB in subcutaneous adipose tissue.

Results

Insulin-resistance, leptin, oxidative stress as well as adipose tissue inflammation decreased significantly after RYGB. Similarly, systemic inflammation was reduced and peripheral blood mononuclear cells (PBMCs) were reprogrammed towards an M2-type inflammation. Loss of BMI correlated with leptin levels (r = 0.891, p < 0.0001), insulin resistance (r = 0.527, p = 0.003), and oxidative stress (r = 0.592, p = 0.016). Leptin correlated with improved insulin resistance (r = 0.449, p = 0.032) while reduced leptin showed a strong association with improved oxidative stress (r = 0.809, p = 0.001). Lastly, reduced oxidative stress correlated strongly with improved insulin-resistance (r = 0.776, p = 0.001).

Conclusions

RYGB improves adipose tissue function and inflammation. Leptin as marker for adipose tissue dysfunction may be the mediating factor between insulin resistance and oxidative stress and thereby likely improving T2DM.
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Literature
1.
go back to reference Wild S, Roglic G, Green A, Sicree R, King H (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27:1047–1053CrossRefPubMed Wild S, Roglic G, Green A, Sicree R, King H (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27:1047–1053CrossRefPubMed
2.
3.
go back to reference Picot J, Jones J, Colquitt JL et al (2009) The clinical effectiveness and cost-effectiveness of bariatric (weight loss) surgery for obesity: a systematic review and economic evaluation. Health Technol Assess 13(41):1–190, 215–357 Picot J, Jones J, Colquitt JL et al (2009) The clinical effectiveness and cost-effectiveness of bariatric (weight loss) surgery for obesity: a systematic review and economic evaluation. Health Technol Assess 13(41):1–190, 215–357
4.
go back to reference Franz MJ, Boucher JL, Rutten-Ramos S, Van Wormer JJ (2015) Lifestyle weight-loss intervention outcomes in overweight and obese adults with type 2 diabetes: a systematic review and meta-analysis of randomized clinical trials. J Acad Nutr Diet 115:1447–1463CrossRefPubMed Franz MJ, Boucher JL, Rutten-Ramos S, Van Wormer JJ (2015) Lifestyle weight-loss intervention outcomes in overweight and obese adults with type 2 diabetes: a systematic review and meta-analysis of randomized clinical trials. J Acad Nutr Diet 115:1447–1463CrossRefPubMed
5.
go back to reference Mingrone G, Panunzi S, De Gaetano A et al (2015) Bariatric-metabolic surgery versus conventional medical treatment in obese patients with type 2 diabetes: 5 year follow-up of an open-label, single-centre, randomised controlled trial. Lancet 386:964–973CrossRefPubMed Mingrone G, Panunzi S, De Gaetano A et al (2015) Bariatric-metabolic surgery versus conventional medical treatment in obese patients with type 2 diabetes: 5 year follow-up of an open-label, single-centre, randomised controlled trial. Lancet 386:964–973CrossRefPubMed
6.
go back to reference Muller-Stich BP, Senft JD, Warschkow R, et al. (2014) Surgical versus medical treatment of type 2 diabetes mellitus in nonseverely obese patients: a systematic review and meta-analysis. Ann Surg Muller-Stich BP, Senft JD, Warschkow R, et al. (2014) Surgical versus medical treatment of type 2 diabetes mellitus in nonseverely obese patients: a systematic review and meta-analysis. Ann Surg
7.
go back to reference Buchwald H, Estok R, Fahrbach K et al (2009) Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med 122:248–256 e245CrossRefPubMed Buchwald H, Estok R, Fahrbach K et al (2009) Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med 122:248–256 e245CrossRefPubMed
8.
go back to reference Schauer PR, Bhatt DL, Kirwan JP, et al. (2014) Bariatric surgery versus intensive medical therapy for diabetes −3-year outcomes. N Engl J Med Schauer PR, Bhatt DL, Kirwan JP, et al. (2014) Bariatric surgery versus intensive medical therapy for diabetes −3-year outcomes. N Engl J Med
11.
go back to reference Le KA, Mahurkar S, Alderete TL et al (2011) Subcutaneous adipose tissue macrophage infiltration is associated with hepatic and visceral fat deposition, hyperinsulinemia, and stimulation of NF-kappaB stress pathway. Diabetes 60:2802–2809CrossRefPubMedPubMedCentral Le KA, Mahurkar S, Alderete TL et al (2011) Subcutaneous adipose tissue macrophage infiltration is associated with hepatic and visceral fat deposition, hyperinsulinemia, and stimulation of NF-kappaB stress pathway. Diabetes 60:2802–2809CrossRefPubMedPubMedCentral
12.
go back to reference Aroor AR, DeMarco VG (2014) Oxidative stress and obesity: the chicken or the egg? Diabetes 63:2216–2218CrossRefPubMed Aroor AR, DeMarco VG (2014) Oxidative stress and obesity: the chicken or the egg? Diabetes 63:2216–2218CrossRefPubMed
14.
go back to reference Amato MC, Pizzolanti G, Torregrossa V, Misiano G, Milano S, Giordano C (2014) Visceral adiposity index (VAI) is predictive of an altered adipokine profile in patients with type 2 diabetes. PLoS One 9:e91969CrossRefPubMedPubMedCentral Amato MC, Pizzolanti G, Torregrossa V, Misiano G, Milano S, Giordano C (2014) Visceral adiposity index (VAI) is predictive of an altered adipokine profile in patients with type 2 diabetes. PLoS One 9:e91969CrossRefPubMedPubMedCentral
15.
go back to reference Gruen ML, Hao M, Piston DW, Hasty AH (2007) Leptin requires canonical migratory signaling pathways for induction of monocyte and macrophage chemotaxis. Am J Physiol Cell Physiol 293:C1481–C1488CrossRefPubMed Gruen ML, Hao M, Piston DW, Hasty AH (2007) Leptin requires canonical migratory signaling pathways for induction of monocyte and macrophage chemotaxis. Am J Physiol Cell Physiol 293:C1481–C1488CrossRefPubMed
16.
go back to reference Surmi BK, Hasty AH (2008) Macrophage infiltration into adipose tissue: initiation, propagation and remodeling. Futur Lipidol 3:545–556CrossRef Surmi BK, Hasty AH (2008) Macrophage infiltration into adipose tissue: initiation, propagation and remodeling. Futur Lipidol 3:545–556CrossRef
17.
go back to reference Friedman JM, Halaas JL (1998) Leptin and the regulation of body weight in mammals. Nature 395:763–770CrossRefPubMed Friedman JM, Halaas JL (1998) Leptin and the regulation of body weight in mammals. Nature 395:763–770CrossRefPubMed
18.
go back to reference Rizzo MR, Barbieri M, Marfella R, Paolisso G (2012) Reduction of oxidative stress and inflammation by blunting daily acute glucose fluctuations in patients with type 2 diabetes: role of dipeptidyl peptidase-IV inhibition. Diabetes Care 35:2076–2082CrossRefPubMedPubMedCentral Rizzo MR, Barbieri M, Marfella R, Paolisso G (2012) Reduction of oxidative stress and inflammation by blunting daily acute glucose fluctuations in patients with type 2 diabetes: role of dipeptidyl peptidase-IV inhibition. Diabetes Care 35:2076–2082CrossRefPubMedPubMedCentral
19.
go back to reference Youn JY, Siu KL, Lob HE, Itani H, Harrison DG, Cai H (2014) Role of vascular oxidative stress in obesity and metabolic syndrome. Diabetes 63:2344–2355CrossRefPubMedPubMedCentral Youn JY, Siu KL, Lob HE, Itani H, Harrison DG, Cai H (2014) Role of vascular oxidative stress in obesity and metabolic syndrome. Diabetes 63:2344–2355CrossRefPubMedPubMedCentral
20.
go back to reference Xu XJ, Apovian C, Hess D, Carmine B, Saha A, Ruderman N (2015) Improved insulin sensitivity 3 months after RYGB surgery is associated with increased subcutaneous adipose tissue AMPK activity and decreased oxidative stress. Diabetes 64:3155–3159CrossRefPubMedPubMedCentral Xu XJ, Apovian C, Hess D, Carmine B, Saha A, Ruderman N (2015) Improved insulin sensitivity 3 months after RYGB surgery is associated with increased subcutaneous adipose tissue AMPK activity and decreased oxidative stress. Diabetes 64:3155–3159CrossRefPubMedPubMedCentral
21.
go back to reference Chatterjee S, Ganini D, Tokar EJ et al (2013) Leptin is key to peroxynitrite-mediated oxidative stress and Kupffer cell activation in experimental non-alcoholic steatohepatitis. J Hepatol 58:778–784CrossRefPubMed Chatterjee S, Ganini D, Tokar EJ et al (2013) Leptin is key to peroxynitrite-mediated oxidative stress and Kupffer cell activation in experimental non-alcoholic steatohepatitis. J Hepatol 58:778–784CrossRefPubMed
22.
go back to reference Shi X, Chen Y, Nadeem L, Xu G (2013) Beneficial effect of TNF-alpha inhibition on diabetic peripheral neuropathy. J Neuroinflammation 10:69PubMedPubMedCentral Shi X, Chen Y, Nadeem L, Xu G (2013) Beneficial effect of TNF-alpha inhibition on diabetic peripheral neuropathy. J Neuroinflammation 10:69PubMedPubMedCentral
23.
24.
go back to reference Furukawa S, Fujita T, Shimabukuro M et al (2004) Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 114:1752–1761CrossRefPubMedPubMedCentral Furukawa S, Fujita T, Shimabukuro M et al (2004) Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 114:1752–1761CrossRefPubMedPubMedCentral
25.
go back to reference Woelnerhanssen B, Peterli R, Steinert RE, Peters T, Borbely Y, Beglinger C (2011) 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 7:561–568CrossRefPubMed Woelnerhanssen B, Peterli R, Steinert RE, Peters T, Borbely Y, Beglinger C (2011) 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 7:561–568CrossRefPubMed
26.
go back to reference Murri M, Garcia-Fuentes E, Garcia-Almeida JM et al (2010) Changes in oxidative stress and insulin resistance in morbidly obese patients after bariatric surgery. Obes Surg 20:363–368CrossRefPubMed Murri M, Garcia-Fuentes E, Garcia-Almeida JM et al (2010) Changes in oxidative stress and insulin resistance in morbidly obese patients after bariatric surgery. Obes Surg 20:363–368CrossRefPubMed
27.
go back to reference Muller-Stich BP, Billeter AT, Fleming T, Fischer L, Buchler MW, Nawroth PP (2014) Nitrosative stress but not glycemic parameters correlate with improved neuropathy in nonseverely obese diabetic patients after roux-Y gastric bypass. Surg Obes Relat Dis Off J Am Soc Bariatric Surg Muller-Stich BP, Billeter AT, Fleming T, Fischer L, Buchler MW, Nawroth PP (2014) Nitrosative stress but not glycemic parameters correlate with improved neuropathy in nonseverely obese diabetic patients after roux-Y gastric bypass. Surg Obes Relat Dis Off J Am Soc Bariatric Surg
28.
go back to reference Sharma AM, Kushner RF (2009) A proposed clinical staging system for obesity. Int J Obes 33:289–295CrossRef Sharma AM, Kushner RF (2009) A proposed clinical staging system for obesity. Int J Obes 33:289–295CrossRef
29.
go back to reference Padwal RS, Pajewski NM, Allison DB, Sharma AM (2011) Using the Edmonton obesity staging system to predict mortality in a population-representative cohort of people with overweight and obesity. CMAJ: Can Med Assoc J J l'Assoc Med Can 183:E1059–E1066CrossRef Padwal RS, Pajewski NM, Allison DB, Sharma AM (2011) Using the Edmonton obesity staging system to predict mortality in a population-representative cohort of people with overweight and obesity. CMAJ: Can Med Assoc J J l'Assoc Med Can 183:E1059–E1066CrossRef
30.
31.
go back to reference Costanzo P, Cleland JG, Pellicori P et al (2015) The obesity paradox in type 2 diabetes mellitus: relationship of body mass index to prognosis: a cohort study. Ann Intern Med 162:610–618CrossRefPubMed Costanzo P, Cleland JG, Pellicori P et al (2015) The obesity paradox in type 2 diabetes mellitus: relationship of body mass index to prognosis: a cohort study. Ann Intern Med 162:610–618CrossRefPubMed
32.
go back to reference Muller-Stich BP, Fischer L, Kenngott HG et al (2013) Gastric bypass leads to improvement of diabetic neuropathy independent of glucose normalization—results of a prospective cohort study (DiaSurg 1 study). Ann Surg 258:760–765 discussion 765-766CrossRefPubMed Muller-Stich BP, Fischer L, Kenngott HG et al (2013) Gastric bypass leads to improvement of diabetic neuropathy independent of glucose normalization—results of a prospective cohort study (DiaSurg 1 study). Ann Surg 258:760–765 discussion 765-766CrossRefPubMed
33.
go back to reference Billeter AT, Probst P, Fischer L, et al. (2015) Risk of malnutrition, trace metal, and vitamin deficiency post roux-en-Y gastric bypass-a prospective study of 20 patients with BMI <35 kg/m. Obes Surg Billeter AT, Probst P, Fischer L, et al. (2015) Risk of malnutrition, trace metal, and vitamin deficiency post roux-en-Y gastric bypass-a prospective study of 20 patients with BMI <35 kg/m. Obes Surg
34.
go back to reference Billeter ATKS, Zeier M, Scheurlen K, Fischer L, Schulte TM, Kenngott HG, Israel B, Knefeli P, Büchler MW, Nawroth PP, Müller-Stich BP (2016) Renal function in type 2 diabetes following gastric bypass—a prospective cohort study in mildly obese insulin-dependent patients. Dtsch Arztebl Int 113:2016 Billeter ATKS, Zeier M, Scheurlen K, Fischer L, Schulte TM, Kenngott HG, Israel B, Knefeli P, Büchler MW, Nawroth PP, Müller-Stich BP (2016) Renal function in type 2 diabetes following gastric bypass—a prospective cohort study in mildly obese insulin-dependent patients. Dtsch Arztebl Int 113:2016
35.
go back to reference Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419CrossRefPubMed Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419CrossRefPubMed
37.
go back to reference Nguyen D (2013) Quantifying chromogen intensity in immunohistochemistry via reciprocal intensity. Protocol Exch Nguyen D (2013) Quantifying chromogen intensity in immunohistochemistry via reciprocal intensity. Protocol Exch
38.
go back to reference Spandidos A, Wang X, Wang H, Seed B (2010) PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 38:D792–D799CrossRefPubMed Spandidos A, Wang X, Wang H, Seed B (2010) PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 38:D792–D799CrossRefPubMed
39.
go back to reference Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408CrossRefPubMed Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408CrossRefPubMed
40.
go back to reference Weisberg SP, Hunter D, Huber R et al (2006) CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 116:115–124CrossRefPubMed Weisberg SP, Hunter D, Huber R et al (2006) CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 116:115–124CrossRefPubMed
41.
go back to reference Strissel KJ, Stancheva Z, Miyoshi H et al (2007) Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 56:2910–2918CrossRefPubMed Strissel KJ, Stancheva Z, Miyoshi H et al (2007) Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 56:2910–2918CrossRefPubMed
42.
go back to reference Folli F, Corradi D, Fanti P et al (2011) The role of oxidative stress in the pathogenesis of type 2 diabetes mellitus micro- and macrovascular complications: avenues for a mechanistic-based therapeutic approach. Curr Diabetes Rev 7:313–324CrossRefPubMed Folli F, Corradi D, Fanti P et al (2011) The role of oxidative stress in the pathogenesis of type 2 diabetes mellitus micro- and macrovascular complications: avenues for a mechanistic-based therapeutic approach. Curr Diabetes Rev 7:313–324CrossRefPubMed
43.
go back to reference Evans JL, Goldfine ID, Maddux BA, Grodsky GM (2002) Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 23:599–622CrossRefPubMed Evans JL, Goldfine ID, Maddux BA, Grodsky GM (2002) Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 23:599–622CrossRefPubMed
44.
go back to reference Yanagawa T, Taniguchi A, Fukushima M et al (2007) Leptin, triglycerides, and interleukin 6 are independently associated with C-reactive protein in Japanese type 2 diabetic patients. Diabetes Res Clin Pract 75:2–6CrossRefPubMed Yanagawa T, Taniguchi A, Fukushima M et al (2007) Leptin, triglycerides, and interleukin 6 are independently associated with C-reactive protein in Japanese type 2 diabetic patients. Diabetes Res Clin Pract 75:2–6CrossRefPubMed
45.
go back to reference Stefanovic A, Kotur-Stevuljevic J, Spasic S, Bogavac-Stanojevic N, Bujisic N (2008) The influence of obesity on the oxidative stress status and the concentration of leptin in type 2 diabetes mellitus patients. Diabetes Res Clin Pract 79:156–163CrossRefPubMed Stefanovic A, Kotur-Stevuljevic J, Spasic S, Bogavac-Stanojevic N, Bujisic N (2008) The influence of obesity on the oxidative stress status and the concentration of leptin in type 2 diabetes mellitus patients. Diabetes Res Clin Pract 79:156–163CrossRefPubMed
46.
go back to reference Pandey G, Shihabudeen MS, David HP, Thirumurugan E, Thirumurugan K (2015) Association between hyperleptinemia and oxidative stress in obese diabetic subjects. J Diabetes Metab Disord 14:24CrossRefPubMedPubMedCentral Pandey G, Shihabudeen MS, David HP, Thirumurugan E, Thirumurugan K (2015) Association between hyperleptinemia and oxidative stress in obese diabetic subjects. J Diabetes Metab Disord 14:24CrossRefPubMedPubMedCentral
47.
go back to reference Fischer S, Hanefeld M, Haffner SM et al (2002) Insulin-resistant patients with type 2 diabetes mellitus have higher serum leptin levels independently of body fat mass. Acta Diabetol 39:105–110CrossRefPubMed Fischer S, Hanefeld M, Haffner SM et al (2002) Insulin-resistant patients with type 2 diabetes mellitus have higher serum leptin levels independently of body fat mass. Acta Diabetol 39:105–110CrossRefPubMed
48.
go back to reference Malmstrom R, Taskinen MR, Karonen SL, Yki-Jarvinen H (1996) Insulin increases plasma leptin concentrations in normal subjects and patients with NIDDM. Diabetologia 39:993–996CrossRefPubMed Malmstrom R, Taskinen MR, Karonen SL, Yki-Jarvinen H (1996) Insulin increases plasma leptin concentrations in normal subjects and patients with NIDDM. Diabetologia 39:993–996CrossRefPubMed
49.
go back to reference Kitade H, Sawamoto K, Nagashimada M et al (2012) CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes 61:1680–1690CrossRefPubMedPubMedCentral Kitade H, Sawamoto K, Nagashimada M et al (2012) CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes 61:1680–1690CrossRefPubMedPubMedCentral
50.
go back to reference Kanda H, Tateya S, Tamori Y et al (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116:1494–1505CrossRefPubMedPubMedCentral Kanda H, Tateya S, Tamori Y et al (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116:1494–1505CrossRefPubMedPubMedCentral
51.
53.
go back to reference Kousathana F, Georgitsi M, Lambadiari V, Giamarellos-Bourboulis EJ, Dimitriadis G, Mouktaroudi M (2017) Defective production of interleukin-1 beta in patients with type 2 diabetes mellitus: restoration by proper glycemic control. Cytokine 90:177–184CrossRefPubMed Kousathana F, Georgitsi M, Lambadiari V, Giamarellos-Bourboulis EJ, Dimitriadis G, Mouktaroudi M (2017) Defective production of interleukin-1 beta in patients with type 2 diabetes mellitus: restoration by proper glycemic control. Cytokine 90:177–184CrossRefPubMed
54.
55.
go back to reference Henriksen EJ, Diamond-Stanic MK, Marchionne EM (2011) Oxidative stress and the etiology of insulin resistance and type 2 diabetes. Free Radic Biol Med 51:993–999CrossRefPubMed Henriksen EJ, Diamond-Stanic MK, Marchionne EM (2011) Oxidative stress and the etiology of insulin resistance and type 2 diabetes. Free Radic Biol Med 51:993–999CrossRefPubMed
56.
go back to reference Panunzi S, De Gaetano A, Carnicelli A, Mingrone G (2015) Predictors of remission of diabetes mellitus in severely obese individuals undergoing bariatric surgery: do BMI or procedure choice matter? A meta-analysis. Ann Surg 261:459–467CrossRefPubMed Panunzi S, De Gaetano A, Carnicelli A, Mingrone G (2015) Predictors of remission of diabetes mellitus in severely obese individuals undergoing bariatric surgery: do BMI or procedure choice matter? A meta-analysis. Ann Surg 261:459–467CrossRefPubMed
57.
go back to reference Farb MG, Bigornia S, Mott M et al (2011) Reduced adipose tissue inflammation represents an intermediate cardiometabolic phenotype in obesity. J Am Coll Cardiol 58:232–237CrossRefPubMedPubMedCentral Farb MG, Bigornia S, Mott M et al (2011) Reduced adipose tissue inflammation represents an intermediate cardiometabolic phenotype in obesity. J Am Coll Cardiol 58:232–237CrossRefPubMedPubMedCentral
58.
go back to reference Tamboli RA, Breitman I, Marks-Shulman PA et al (2014) Early weight regain after gastric bypass does not affect insulin sensitivity but is associated with elevated ghrelin. Obesity 22:1617–1622CrossRefPubMedPubMedCentral Tamboli RA, Breitman I, Marks-Shulman PA et al (2014) Early weight regain after gastric bypass does not affect insulin sensitivity but is associated with elevated ghrelin. Obesity 22:1617–1622CrossRefPubMedPubMedCentral
Metadata
Title
Gastric bypass simultaneously improves adipose tissue function and insulin-dependent type 2 diabetes mellitus
Authors
Adrian T. Billeter
Spiros Vittas
Barbara Israel
Katharina M. Scheurlen
Asa Hidmark
Thomas H. Fleming
Stefan Kopf
Markus W. Büchler
Beat P. Müller-Stich
Publication date
01-09-2017
Publisher
Springer Berlin Heidelberg
Published in
Langenbeck's Archives of Surgery / Issue 6/2017
Print ISSN: 1435-2443
Electronic ISSN: 1435-2451
DOI
https://doi.org/10.1007/s00423-017-1601-x

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