Does bariatric surgery improve adipose tissue function?

Obesity Reviews

Volumn 17, Issue 9, 2016, Pages 795-809

  Frikke Schmidt, H ^a   O'Rourke, R W ^a   Lumeng, C N ^b   Sandoval, D A ^a   Seeley, R J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Adipose; bariatric surgery; obesity

Indexed keywords

ADIPOCYTOKINE; CATECHOLAMINE; INSULIN;

ADIPOCYTE; ADIPOSE TISSUE; BARIATRIC SURGERY; BILE ACID METABOLISM; BODY FAT DISTRIBUTION; CELL SIZE; CYTOKINE RELEASE; FAT MASS; HUMAN; INFLAMMATION; INTESTINE FLORA; INTRAABDOMINAL FAT; LIPID STORAGE; LIPOLYSIS; METABOLIC REGULATION; METABOLISM; NONHUMAN; REVIEW; SUBCUTANEOUS FAT; WEIGHT REDUCTION;

EID: 84982129863     PISSN: 14677881     EISSN: 1467789X     Source Type: Journal    
DOI: 10.1111/obr.12429     Document Type: Review

References (191)

1. Arble DM, Sandoval DA, Seeley RJ. Mechanisms underlying weight loss and metabolic improvements in rodent models of bariatric surgery. Diabetologia 2015; 58: 211–20.
2. Stefater MA, Wilson-Perez HE, Chambers AP, Sandoval DA, Seeley RJ. All bariatric surgeries are not created equal: insights from mechanistic comparisons. Endocr Rev 2012; 33: 595–622.
3. Angrisani L, Santonicola A, Iovino P, Formisano G, Buchwald H, Scopinaro N. Bariatric Surgery Worldwide 2013. Obes Surg 2015; 25: 1822–32.
4. Carlin AM, Zeni TM, English WJ et al. The comparative effectiveness of sleeve gastrectomy, gastric bypass, and adjustable gastric banding procedures for the treatment of morbid obesity. Ann Surg 2013; 257: 791–7.
5. Galanakis CG, Daskalakis M, Manios A, Xyda A, Karantanas AH, Melissas J. Computed tomography-based assessment of abdominal adiposity changes and their impact on metabolic alterations following bariatric surgery. World J Surg 2014; 39: 417–23.
6. Di Taranto G, Cicione C, Visconti G et al. Qualitative and quantitative differences of adipose-derived stromal cells from superficial and deep subcutaneous lipoaspirates: a matter of fat. Cytotherapy 2015; 17: 1076–89.
7. Boyko EJ, Fujimoto WY, Leonetti DL, Newell-Morris L. Visceral adiposity and risk of type 2 diabetes: a prospective study among Japanese Americans. Diabetes Care 2000; 23: 465–71.
8. Liu J, Fox CS, Hickson DA et al. Impact of abdominal visceral and subcutaneous adipose tissue on cardiometabolic risk factors: the Jackson Heart Study. J Clin Endocrinol Metab 2010; 95: 5419–26.
9. Gallagher D, Kelley DE, Yim JE et al. Adipose tissue distribution is different in type 2 diabetes. Am J Clin Nutr 2009; 89: 807–14.
10. Ibrahim MM. Subcutaneous and visceral adipose tissue: structural and functional differences. Int J Assoc Study Obes 2010; 11: 11–8.
11. Lima MM, Pareja JC, Alegre SM et al. Visceral fat resection in humans: effect on insulin sensitivity, beta-cell function, adipokines, and inflammatory markers. Obesity (SilverSpring) 2013; 21: E182–E89.
12. 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: 448–55.
13. Dunn JP, Abumrad NN, Breitman I et al. Hepatic and peripheral insulin sensitivity and diabetes remission at 1 month after Roux-en-Y gastric bypass surgery in patients randomized to omentectomy. Diabetes Care 2012; 35: 137–42.
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. Sdralis E, Argentou M, Mead N, Kehagias I, Alexandridis T, Kalfarentzos F. A prospective randomized study comparing patients with morbid obesity submitted to sleeve gastrectomy with or without omentectomy. Obes Surg 2013; 23: 965–71.
16. Andersson DP, Thorell A, Lofgren P et al. Omentectomy in addition to gastric bypass surgery and influence on insulin sensitivity: a randomized double blind controlled trial. Clin Nutr 2014; 33: 991–6.
17. Keidar A, Appelbaum L, Schweiger C et al. Baseline abdominal lipid partitioning is associated with the metabolic response to bariatric surgery. Obes Surg 2014; 24: 1709–16.
18. Gaborit B, Abdesselam I, Kober F et al. Ectopic fat storage in the pancreas using H-MRS: importance of diabetic status and modulation with bariatric surgery-induced weight loss. Int J Obes (Lond) 2014; 39: 480–7.
19. Faria G, Pestana D, Aral M et al. Metabolic score: insights on the development and prediction of remission of metabolic syndrome after gastric bypass. Ann Surg 2014; 260: 279–86.
20. Toro-Ramos T, Goodpaster BH, Janumala I et al. Continued loss in visceral and intermuscular adipose tissue in weight-stable women following bariatric surgery. Obesity 2015; 23: 62–9.
21. Kim MK, Kim W, Kwon HS, Baek KH, Kim EK, Song KH. Effects of bariatric surgery on metabolic and nutritional parameters in severely obese Korean patients with type 2 diabetes: a prospective 2-year follow up. J Diabetes Investig 2014; 5: 221–27.
22. Yoon DY, Kim HK, Kim JA et al. Changes in the abdominal fat distribution after gastrectomy: computed tomography assessment. ANZ J Surg 2007; 77: 121–25.
23. Boettcher M, Machann J, Stefan N et al. Intermuscular adipose tissue (IMAT): association with other adipose tissue compartments and insulin sensitivity. Journal of magnetic resonance imaging : JMRI 2009; 29: 1340–5.
24. Henninger AM, Eliasson B, Jenndahl LE, Hammarstedt A. Adipocyte hypertrophy, inflammation and fibrosis characterize subcutaneous adipose tissue of healthy, non-obese subjects predisposed to type 2 diabetes. PLoS One 2014; 9 e105262.
25. Bays HE, Gonzalez-Campoy JM, Bray GA et al. Pathogenic potential of adipose tissue and metabolic consequences of adipocyte hypertrophy and increased visceral adiposity. Expert Rev Cardiovasc Ther 2008; 6: 343–68.
26. O'Connell J, Lynch L, Cawood TJ et al. The relationship of omental and subcutaneous adipocyte size to metabolic disease in severe obesity. PLoS One 2010; 5 e9997.
27. Goossens GH, Bizzarri A, Venteclef N et al. Increased adipose tissue oxygen tension in obese compared with lean men is accompanied by insulin resistance, impaired adipose tissue capillarization, and inflammation. Circulation 2011; 124: 67–76.
28. Johannsen DL, Tchoukalova Y, Tam CS et al. Effect of 8 weeks of overfeeding on ectopic fat deposition and insulin sensitivity: testing the “adipose tissue expandability” hypothesis. Diabetes Care 2014; 37: 2789–97.
29. Cotillard A, Poitou C, Torcivia A et al. Adipocyte size threshold matters: link with risk of type 2 diabetes and improved insulin resistance after gastric bypass. J Clin Endocrinol Metab 2014; 99: E1466–70.
30. Cancello R, Zulian A, Gentilini D et al. Permanence of molecular features of obesity in subcutaneous adipose tissue of ex-obese subjects. Int J Obes (Lond) 2013; 37: 867–73.
31. Aghamohammadzadeh R, Greenstein AS, Yadav R et al. Effects of bariatric surgery on human small artery function: evidence for reduction in perivascular adipocyte inflammation, and the restoration of normal anticontractile activity despite persistent obesity. J Am Coll Cardiol 2013; 62: 128–35.
32. Andersson DP, Eriksson HD, Thorell A et al. Changes in subcutaneous fat cell volume and insulin sensitivity after weight loss. Diabetes Care 2014; 37: 1831–36.
33. Zhang H, Wang Y, Zhang J, Potter BJ, Sowers JR, Zhang C. Bariatric surgery reduces visceral adipose inflammation and improves endothelial function in type 2 diabetic mice. Arterioscler Thromb Vasc Biol 2011; 31: 2063–69.
34. Mendez-Gimenez L, Becerril S, Moncada R et al. Sleeve gastrectomy reduces hepatic steatosis by improving the coordinated regulation of aquaglyceroporins in adipose tissue and liver in obese rats. Obes Surg 2015; 25: 1723–34.
35. Cummings BP, Strader AD, Stanhope KL et al. Ileal interposition surgery improves glucose and lipid metabolism and delays diabetes onset in the UCD-T2DM rat. Gastroenterology 2010; 138: 2437–46 46.
36. Nadreau E, Baraboi ED, Samson P et al. Effects of the biliopancreatic diversion on energy balance in the rat. Int J Obes (Lond) 2006; 30: 419–29.
37. Mauriege P, Prud'homme D, Lemieux S, Tremblay A, Despres JP. Regional differences in adipose tissue lipolysis from lean and obese women: existence of postreceptor alterations. Am J Physiol 1995; 269: E341–50.
38. Arner P, Ostman J. Relationship between the tissue level of cyclic AMP and the fat cell size of human adipose tissue. J Lipid Res 1978; 19: 613–8.
39. Sancho V, Trigo MV, Martin-Duce A et al. Effect of GLP-1 on D-glucose transport, lipolysis and lipogenesis in adipocytes of obese subjects. Int J Mol Med 2006; 17: 1133–7.
40. Imbeault P, Chevrier J, Dewailly E et al. Increase in plasma pollutant levels in response to weight loss in humans is related to in vitro subcutaneous adipocyte basal lipolysis. Int J Obes Relat Metab Disord : journal of the International Association for the Study of Obesity 2001; 25: 1585–91.
41. Berman DM, Nicklas BJ, Ryan AS, Rogus EM, Dennis KE, Goldberg AP. Regulation of lipolysis and lipoprotein lipase after weight loss in obese, postmenopausal women. Obes Res 2004; 12: 32–9.
42. Hernandez TL, Sutherland JP, Wolfe P et al. Lack of suppression of circulating free fatty acids and hypercholesterolemia during weight loss on a high-fat, low-carbohydrate diet. Am J Clin Nutr 2010; 91: 578–85.
43. Reynisdottir S, Langin D, Carlstrom K, Holm C, Rossner S, Arner P. Effects of weight reduction on the regulation of lipolysis in adipocytes of women with upper-body obesity. Clin Sci 1995; 89: 421–9.
44. Kullberg J, Sundbom M, Haenni A et al. Gastric bypass promotes more lipid mobilization than a similar weight loss induced by low-calorie diet. J Obes 2011; 2011: 959601.
45. 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: 2093–102.
46. Pardina E, Ferrer R, Baena-Fustegueras JA et al. Only C-reactive protein, but not TNF-alpha or IL6, reflects the improvement in inflammation after bariatric surgery. Obes Surg 2012; 22: 131–39.
47. Soriguer F, Garcia-Serrano S, Garcia-Almeida JM et al. Changes in the serum composition of free-fatty acids during an intravenous glucose tolerance test. Obesity (SilverSpring) 2009; 17: 10–15.
48. Kim MK, Jang EH, Hong OK et al. Changes in serum levels of bone morphogenic protein 4 and inflammatory cytokines after bariatric surgery in severely obese korean patients with type 2 diabetes. Int J Endocrinol 2013; 2013: 681205.
49. Carvalho BM, Oliveira AG, Ueno M et al. Modulation of double-stranded RNA-activated protein kinase in insulin sensitive tissues of obese humans. Obesity (SilverSpring) 2013; 21: 2452–57.
50. Maymo-Masip E, Fernandez-Veledo S, Garcia EA et al. The rise of soluble TWEAK levels in severely obese subjects after bariatric surgery may affect adipocyte-cytokine production induced by TNFalpha. J Clin Endocrinol Metab 2013; 98: E1323–E33.
51. Dharuri H, 't Hoen PA, van Klinken JB et al. Downregulation of the acetyl-CoA metabolic network in adipose tissue of obese diabetic individuals and recovery after weight loss. Diabetologia 2014; 57: 2384–92.
52. Xu J, Donepudi AC, Moscovitz JE, Slitt AL. Keap1-knockdown decreases fasting-induced fatty liver via altered lipid metabolism and decreased fatty acid mobilization from adipose tissue. PLoS One 2013; 8 e79841.
53. Chambers KT, Chen Z, Crawford PA et al. Liver-specific PGC-1beta deficiency leads to impaired mitochondrial function and lipogenic response to fasting-refeeding. PLoS One 2012; 7 e52645.
54. Liang G, Yang J, Horton JD, Hammer RE, Goldstein JL, Brown MS. Diminished hepatic response to fasting/refeeding and liver X receptor agonists in mice with selective deficiency of sterol regulatory element-binding protein-1c. J Biol Chem 2002; 277: 9520–8.
55. Curry TB, Roberts SK, Basu R et al. Gastric bypass surgery is associated with near-normal insulin suppression of lipolysis in nondiabetic individuals. Am J Physiol Endocrinol Metab 2011; 300: E746–E51.
56. de Weijer BA, Aarts E, Janssen IM et al. Hepatic and peripheral insulin sensitivity do not improve 2 weeks after bariatric surgery. Obesity 2013; 21: 1143–7.
57. Albers PH, Bojsen-Moller KN, Dirksen C et al. Enhanced insulin signaling in human skeletal muscle and adipose tissue following gastric bypass surgery. Am J Physiol Regul Integr Comp Physiol 2015; 309: R510–24.
58. Li SQ, Zhou Y, Wang Y, Liu Y, Geng DH, Liu JG. Upregulation of IRS-1 expression in Goto–Kakizaki rats following Roux-en-Y gastric bypass surgery: resolution of type 2 diabetes? Tohoku J Exp Med 2011; 225: 179–86.
59. Bonhomme S, Guijarro A, Keslacy S et al. Gastric bypass up-regulates insulin signaling pathway. Nutrition 2011; 27: 73–80.
60. Cummings BP, Bettaieb A, Graham JL et al. Bile-acid-mediated decrease in endoplasmic reticulum stress: a potential contributor to the metabolic benefits of ileal interposition surgery in UCD-T2DM rats. Dis Model Mech 2013; 6: 443–56.
61. Collins P, Williams G. Drug treatment of obesity: from past failures to future successes? Br J Clin Pharmacol 2001; 51: 13–25.
62. Koppo K, Siklova-Vitkova M, Klimcakova E et al. Catecholamine and insulin control of lipolysis in subcutaneous adipose tissue during long-term diet-induced weight loss in obese women. Am J Physiol Endocrinol Metab 2012; 302: E226–32.
63. Bairras C, Mauriege P, Bukowiecki L, Atgie C. Regulation of lypolysis in white adipose tissues of lean and obese Zucker rats. J Physiol Biochem 2007; 63: 287–96.
64. Lambert GW, Straznicky NE, Lambert EA, Dixon JB, Schlaich MP. Sympathetic nervous activation in obesity and the metabolic syndrome—causes, consequences and therapeutic implications. Pharmacol Ther 2010; 126: 159–72.
65. Kaartinen JM, LaNoue KF, Martin LF, Vikman HL, Ohisalo JJ. Beta-adrenergic responsiveness of adenylate cyclase in human adipocyte plasma membranes in obesity and after massive weight reduction. Metabolism 1995; 44: 1288–92.
66. Neinast MD, Frank AP, Zechner JF et al. Activation of natriuretic peptides and the sympathetic nervous system following Roux-en-Y gastric bypass is associated with gonadal adipose tissues browning. Mol Metab 2015; 4: 427–36.
67. Mauriege P, Imbeault P, Langin D et al. Regional and gender variations in adipose tissue lipolysis in response to weight loss. J Lipid Res 1999; 40: 1559–71.
68. Bucerius J, Vijgen GH, Brans B et al. Impact of bariatric surgery on carotid artery inflammation and the metabolic activity in different adipose tissues. Medicine 2015; 94: e725.
69. Vijgen GH, Bouvy ND, Teule GJ et al. Increase in brown adipose tissue activity after weight loss in morbidly obese subjects. J Clin Endocrinol Metab 2012; 97: E1229–E33.
70. Hankir MK, Bronisch F, Hintschich C, Krugel U, Seyfried F, Fenske WK. Differential effects of Roux-en-Y gastric bypass surgery on brown and beige adipose tissue thermogenesis. Metabolism 2015; 64: 1240–9.
71. Baraboi ED, Li W, Labbe SM et al. Metabolic changes induced by the biliopancreatic diversion in diet-induced obesity in male rats: the contributions of sleeve gastrectomy and duodenal switch. Endocrinology 2015; 156: 1316–29.
72. Lindqvist A, de la Cour CD, Hakanson R, Erlanson-Albertsson C. Ghrelin affects gastrectomy-induced decrease in UCP1 and beta3-AR mRNA expression in mice. Regul Pept 2007; 142: 24–8.
73. Rachid B, van de Sande-Lee S, Rodovalho S et al. Distinct regulation of hypothalamic and brown/beige adipose tissue activities in human obesity. Int J Obes (Lond) 2015; 39: 1515–22.
74. Lehr S, Hartwig S, Sell H. Adipokines: a treasure trove for the discovery of biomarkers for metabolic disorders. Proteomics Clin Appl 2012; 6: 91–101.
75. Sainz N, Barrenetxe J, Moreno-Aliaga MJ, Martinez JA. Leptin resistance and diet-induced obesity: central and peripheral actions of leptin. Metabolism 2015; 64: 35–46.
76. La Cava A, Alviggi C, Matarese G. Unraveling the multiple roles of leptin in inflammation and autoimmunity. J Mol Med 2004; 82: 4–11.
77. Mohan V, Deepa R, Pradeepa R et al. Association of low adiponectin levels with the metabolic syndrome—the Chennai Urban Rural Epidemiology Study (CURES-4). Metabolism 2005; 54: 476–81.
78. Meyer LK, Ciaraldi TP, Henry RR, Wittgrove AC, Phillips SA. Adipose tissue depot and cell size dependency of adiponectin synthesis and secretion in human obesity. Adipocyte 2013; 2: 217–26.
79. Yamauchi T, Kamon J, Minokoshi Y et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 2002; 8: 1288–95.
80. Chang YH, Chang DM, Lin KC, Shin SJ, Lee YJ. Visfatin in overweight/obesity, type 2 diabetes mellitus, insulin resistance, metabolic syndrome and cardiovascular diseases: a meta-analysis and systemic review. Diabetes Metab Res Rev 2011; 27: 515–27.
81. Ferland DJ, Watts SW. Chemerin: a comprehensive review elucidating the need for cardiovascular research. Pharm Res: the official journal of the Italian Pharmacological Society 2015; 99: 351–61.
82. Abdennour M, Reggio S, Le NG et al. Association of adipose tissue and liver fibrosis with tissue stiffness in morbid obesity: links with diabetes and BMI loss after gastric bypass. J Clin Endocrinol Metab 2014; 99: 898–907.
83. Lee YJ, Heo YS, Park HS, Lee SH, Lee SK, Jang YJ. Serum SPARC and matrix metalloproteinase-2 and metalloproteinase-9 concentrations after bariatric surgery in obese adults. Obes Surg 2014; 24: 604–10.
84. Chen J, Pamuklar Z, Spagnoli A, Torquati A. Serum leptin levels are inversely correlated with omental gene expression of adiponectin and markedly decreased after gastric bypass surgery. Surg Endosc 2012; 26: 1476–80.
85. Kim MJ, Marchand P, Henegar C et al. Fate and complex pathogenic effects of dioxins and polychlorinated biphenyls in obese subjects before and after drastic weight loss. Environ Health Perspect 2011; 119: 377–83.
86. Tschoner A, Sturm W, Engl J et al. Plasminogen activator inhibitor 1 and visceral obesity during pronounced weight loss after bariatric surgery. NutrMetab Cardiovasc Dis 2012; 22: 340–46.
87. Bobbioni-Harsch E, Morel P, Huber O et al. Energy economy hampers body weight loss after gastric bypass. J Clin Endocrinol Metab 2000; 85: 4695–700.
88. Oberbach A, Schlichting N, Neuhaus J et al. Establishing of a reliable multiple reaction monitoring-based method for the quantification of obesity associated comorbidities in serum and adipose tissue requires intensive clinical validation. J Proteome Res 2014; 13: 5784–800.
89. Haluzikova D, Lacinova Z, Kavalkova P et al. Laparoscopic sleeve gastrectomy differentially affects serum concentrations of FGF-19 and FGF-21 in morbidly obese subjects. Obesity (SilverSpring) 2013; 21: 1335–42.
90. Auguet T, Terra X, Hernandez M et al. Clinical and adipocytokine changes after bariatric surgery in morbidly obese women. Obesity (SilverSpring) 2014; 22: 188–94.
91. Ferrer R, Pardina E, Rossell J et al. Decreased lipases and fatty acid and glycerol transporter could explain reduced fat in diabetic morbidly obese. Obesity (SilverSpring) 2014; 22: 2379–87.
92. Chen J, Spagnoli A, Torquati A. Omental gene expression of adiponectin correlates with degree of insulin sensitivity before and after gastric bypass surgery. Obes Surg 2012; 22: 472–77.
93. Sideleva O, Suratt BT, Black KE et al. Obesity and asthma: an inflammatory disease of adipose tissue not the airway. Am J Respir Crit Care Med 2012; 186: 598–605.
94. Savu MK, Phillips SA, Oh DK et al. Response of adiponectin and its receptors to changes in metabolic state after gastric bypass surgery: dissociation between adipose tissue expression and circulating levels. Surg Obes Relat Dis 2009; 5: 172–80.
95. Cawthorn WP, Scheller EL, Learman BS et al. Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction. Cell Metab 2014; 20: 368–75.
96. Coughlin CC, Finck BN, Eagon JC et al. Effect of marked weight loss on adiponectin gene expression and plasma concentrations. Obesity (SilverSpring) 2007; 15: 640–45.
97. Terra X, Auguet T, Quesada I et al. Increased levels and adipose tissue expression of visfatin in morbidly obese women: the relationship with pro-inflammatory cytokines. Clin Endocrinol(Oxf) 2012; 77: 691–98.
98. Shrestha C, He H, Liu Y, Zhu S, Xiong J, Mo Z. Changes in adipokines following laparoscopic Roux-en-Y gastric bypass surgery in Chinese individuals with type 2 diabetes mellitus and BMI of 22–30 kg.m(−2.) Int J Endocrinol 2013; 2013: 240971.
99. Terra X, Auguet T, Guiu-Jurado E et al. Long-term changes in leptin, chemerin and ghrelin levels following different bariatric surgery procedures: Roux-en-Y gastric bypass and sleeve gastrectomy. Obes Surg 2013; 23: 1790–8.
100. Sell H, Divoux A, Poitou C et al. Chemerin correlates with markers for fatty liver in morbidly obese patients and strongly decreases after weight loss induced by bariatric surgery. J Clin Endocrinol Metab 2010; 95: 2892–6.
101. Ress C, Tschoner A, Engl J et al. Effect of bariatric surgery on circulating chemerin levels. Eur J Clin Invest 2010; 40: 277–80.
102. Parlee SD, Wang Y, Poirier P et al. Biliopancreatic diversion with duodenal switch modifies plasma chemerin in early and late post-operative periods. Obesity 2015; 23: 1201–8.
103. Sams VG, Blackledge C, Wijayatunga N et al. Effect of bariatric surgery on systemic and adipose tissue inflammation. Surg Endosc 2015. doi: 10.1007/s00464-015-4638-3.
104. Grant R, Youm YH, Ravussin A, Dixit VD. Quantification of adipose tissue leukocytosis in obesity. Methods Mol Biol 2013; 1040: 195–209.
105. Xu H, Barnes GT, Yang Q et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112: 1821–30.
106. Skurk T, Alberti-Huber C, Herder C, Hauner H. Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab 2007; 92: 1023–33.
107. Suganami T, Mieda T, Itoh M, Shimoda Y, Kamei Y, Ogawa Y. Attenuation of obesity-induced adipose tissue inflammation in C3H/HeJ mice carrying a Toll-like receptor 4 mutation. Biochem Biophys Res Commun 2007; 354: 45–9.
108. Viana EC, Araujo-Dasilio KL, Miguel GP et al. Gastric bypass and sleeve gastrectomy: the same impact on IL-6 and TNF-alpha. Prospective clinical trial. Obes Surg 2013; 23: 1252–61.
109. Kardassis D, Schonander M, Sjostrom L, Karason K. Carotid artery remodelling in relation to body fat distribution, inflammation and sustained weight loss in obesity. J Intern Med 2014; 275: 534–43.
110. Catalan V, Gomez-Ambrosi J, Ramirez B et al. Proinflammatory cytokines in obesity: impact of type 2 diabetes mellitus and gastric bypass. Obes Surg 2007; 17: 1464–74.
111. Appachi S, Kelly KR, Schauer PR et al. Reduced cardiovascular risk following bariatric surgeries is related to a partial recovery from “adiposopathy”. Obes Surg 2011; 21: 1928–36.
112. Gregor MF, Yang L, Fabbrini E et al. Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss. Diabetes 2009; 58: 693–700.
113. Toubal A, Clement K, Fan R et al. SMRT-GPS2 corepressor pathway dysregulation coincides with obesity-linked adipocyte inflammation. J Clin Invest 2013; 123: 362–79.
114. Eissing L, Scherer T, Todter K et al. De novo lipogenesis in human fat and liver is linked to ChREBP-beta and metabolic health. Nat Commun 2013; 4: 1528.
115. Iannelli A, Anty R, Schneck AS, Tran A, Hebuterne X, Gugenheim J. Evolution of low-grade systemic inflammation, insulin resistance, anthropometrics, resting energy expenditure and metabolic syndrome after bariatric surgery: a comparative study between gastric bypass and sleeve gastrectomy. J Visc Surg 2013; 150: 269–75.
116. Poitou C, Dalmas E, Renovato M et al. CD14dimCD16+ and CD14+ CD16+ monocytes in obesity and during weight loss: relationships with fat mass and subclinical atherosclerosis. Arterioscler Thromb Vasc Biol 2011; 31: 2322–30.
117. Cancello R, Henegar C, Viguerie N et al. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 2005; 54: 2277–86.
118. Aron-Wisnewsky J, Tordjman J, Poitou C et al. Human adipose tissue macrophages: m1 and m2 cell surface markers in subcutaneous and omental depots and after weight loss. J Clin Endocrinol Metab 2009; 94: 4619–23.
119. Poitou C, Perret C, Mathieu F et al. Bariatric surgery induces disruption in inflammatory signaling pathways mediated by immune cells in adipose tissue: a RNA-Seq study. PLoS One 2015; 10 e0125718.
120. Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 2007; 117: 524–9.
121. Vila IK, Badin PM, Marques MA et al. Immune cell Toll-like receptor 4 mediates the development of obesity- and endotoxemia-associated adipose tissue fibrosis. Cell Rep 2014; 7: 1116–29.
122. Divoux A, Tordjman J, Lacasa D et al. Fibrosis in human adipose tissue: composition, distribution, and link with lipid metabolism and fat mass loss. Diabetes 2010; 59: 2817–25.
123. Hu C, Zhang G, Sun D, Han H, Hu S. Duodenal–jejunal bypass improves glucose metabolism and adipokine expression independently of weight loss in a diabetic rat model. Obes Surg 2013; 23: 1436–44.
124. Lancha A, Moncada R, Valenti V et al. Effect of sleeve gastrectomy on osteopontin circulating levels and expression in adipose tissue and liver in rats. Obes Surg 2014; 24: 1702–08.
125. Stefater MA, Sandoval DA, Chambers AP et al. Sleeve gastrectomy in rats improves postprandial lipid clearance by reducing intestinal triglyceride secretion. Gastroenterology 2011; 141: 939–49.
126. 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 2014; 22: 390–400.
127. He B, Liu L, Yu C, Wang Y, Han P. Roux-en-Y gastric bypass reduces lipid overaccumulation in liver by upregulating hepatic autophagy in obese diabetic rats. Obes Surg 2014; 25: 109–18.
128. De Giorgi S, Campos V, Egli L et al. Long-term effects of Roux-en-Y gastric bypass on postprandial plasma lipid and bile acids kinetics in female non diabetic subjects: a cross-sectional pilot study. Clin Nutr 2014; 34: 911–7.
129. Kohli R, Myronovych A, Tan BK et al. Bile acid signaling: mechanism for bariatric surgery, cure for NASH? Dig Dis 2015; 33: 440–6.
130. Gadaleta RM, Cariello M, Sabba C, Moschetta A. Tissue-specific actions of FXR in metabolism and cancer. Biochim Biophys Acta 1851; 2015: 30–9.
131. Teodoro JS, Rolo AP, Palmeira CM. Hepatic FXR: key regulator of whole-body energy metabolism. Trends in endocrinology and metabolism: TEM 2011; 22: 458–66.
132. Ryan KK, Tremaroli V, Clemmensen C et al. FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature 2014; 509: 183–8.
133. McGavigan AK, Garibay D, Henseler ZM et al. TGR5 contributes to glucoregulatory improvements after vertical sleeve gastrectomy in mice. Gut 2015. doi: 10.1136/gutjnl-2015-309871.
134. Sharma NK, Das SK, Mondal AK et al. Endoplasmic reticulum stress markers are associated with obesity in nondiabetic subjects. J Clin Endocrinol Metab 2008; 93: 4532–41.
135. Chang YC, Hee SW, Hsieh ML, Jeng YM, Chuang LM. The role of organelle stresses in diabetes mellitus and obesity: implication for treatment. Anal Cell Pathol 2015; 2015: 972891.
136. Lips MA, de Groot GH, Berends FJ et al. Calorie restriction and Roux-en-Y gastric bypass have opposing effects on circulating FGF21 in morbidly obese subjects. Clin Endocrinol (Oxf) 2014; 81: 862–70.
137. Jansen PL, van Aarts WJE et al. Alterations of hormonally active fibroblast growth factors after Roux-en-Y gastric bypass surgery. Dig Dis 2011; 29: 48–51.
138. Adams AC, Kharitonenkov A. FGF21: the center of a transcriptional nexus in metabolic regulation. Curr Diabetes Rev 2012; 8: 285–93.
139. Jahansouz C, Xu H, Hertzel AV et al. Bile acids increase independently from hypocaloric restriction after bariatric surgery. Ann Surg 2015. doi: 10.1097/SLA.0000000000001552.
140. Roesch SL, Styer AM, Wood GC et al. Perturbations of fibroblast growth factors 19 and 21 in type 2 diabetes. PLoS One 2015; 10 e0116928.
141. Ferrante AW Jr. Macrophages, fat, and the emergence of immunometabolism. J Clin Invest 2013; 123: 4992–3.
142. Magalhaes I, Pingris K, Poitou C et al. Mucosal-associated invariant T cell alterations in obese and type 2 diabetic patients. J Clin Invest 2015; 125: 1752–62.
143. Lynch L, Nowak M, Varghese B et al. Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production. Immunity 2012; 37: 574–87.
144. Magalhaes I, Kiaf B, Lehuen A. iNKT and MAIT cell alterations in diabetes. Front Immunol 2015; 6: 341.
145. Schipper HS, Rakhshandehroo M, van de Graaf SF et al. Natural killer T cells in adipose tissue prevent insulin resistance. J Clin Invest 2012; 122: 3343–54.
146. Cantu RC, Goodman HM. Effects of denervation and fasting on white adipose tissue. Am J Physiol 1967; 212: 207–12.
147. Youngstrom TG, Bartness TJ. White adipose tissue sympathetic nervous system denervation increases fat pad mass and fat cell number. Am J Physiol 1998; 275: R1488–93.
148. Shi H, Bartness TJ. White adipose tissue sensory nerve denervation mimics lipectomy-induced compensatory increases in adiposity. Am J Physiol Regul Integr Comp Physiol 2005; 289: R514–R20.
149. Wu J, Bostrom P, Sparks LM et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 2012; 150: 366–76.
150. Seale P, Conroe HM, Estall J et al. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest 2011; 121: 96–105.
151. Harms M, Seale P. Brown and beige fat: development, function and therapeutic potential. Nat Med 2013; 19: 1252–63.
152. Umemura A, Sasaki A, Nitta H, Otsuka K, Suto T, Wakabayashi G. Effects of changes in adipocyte hormones and visceral adipose tissue and the reduction of obesity-related comorbidities after laparoscopic sleeve gastrectomy in Japanese patients with severe obesity. Endocr J 2014; 61: 381–91.
153. Pardina E, Baena-Fustegueras JA, Catalan R et al. Increased expression and activity of hepatic lipase in the liver of morbidly obese adult patients in relation to lipid content. Obes Surg 2009; 19: 894–904.
154. Torriani M, Oliveira AL, Azevedo DC, Bredella MA, Yu EW. Effects of Roux-en-Y gastric bypass surgery on visceral and subcutaneous fat density by computed tomography. Obes Surg 2015; 25: 381–5.
155. Pardina E, Baena-Fustegueras JA, Fort JM et al. Hepatic and visceral adipose tissue 11betaHSD1 expressions are markers of body weight loss after bariatric surgery. Obesity 2015; 23: 1856–63.
156. Dadson P, Landini L, Helmio M et al. Effect of bariatric surgery on adipose tissue glucose metabolism in different depots in patients with or without type 2 diabetes. Diabetes Care 2016; 39: 292–9.
157. Bazzocchi A, Ponti F, Cariani S et al. Visceral Fat and body composition changes in a female population after RYGBP: a two-year follow-up by DXA. Obes Surg 2014.
158. Hansen M, Lund MT, Gregers E et al. Adipose tissue mitochondrial respiration and lipolysis before and after a weight loss by diet and RYGB. Obesity 2015; 23: 2022–9.
159. 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: 2175–82.
160. Catalan V, Gomez-Ambrosi J, Rodriguez A et al. Increased levels of chemerin and its receptor, chemokine-like receptor-1, in obesity are related to inflammation: tumor necrosis factor-alpha stimulates mRNA levels of chemerin in visceral adipocytes from obese patients. Surg Obes Relat Dis : official journal of the American Society for Bariatric Surgery 2013; 9: 306–14.
161. 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 (SilverSpring) 2009; 17: 1671–77.
162. Domienik-Karlowicz J, Rymarczyk Z, Dzikowska-Diduch O et al. Emerging markers of atherosclerosis before and after bariatric surgery. Obes Surg 2015; 25: 486–93.
163. Netto BD, Bettini SC, Clemente AP et al. Roux-en-Y gastric bypass decreases pro-inflammatory and thrombotic biomarkers in individuals with extreme obesity. Obes Surg 2015; 25: 1010–8.
164. Lindegaard KK, Jorgensen NB, Just R, Heegaard PM, Madsbad S. Effects of Roux-en-Y gastric bypass on fasting and postprandial inflammation-related parameters in obese subjects with normal glucose tolerance and in obese subjects with type 2 diabetes. Diabetol Metab Syndr 2015; 7: 12.
165. Xu XJ, Apovian C, Hess D, Carmine B, Saha A, Ruderman N. Improved insulin sensitivity 3 months after RYGB surgery is associated with increased subcutaneous adipose tissue AMPK activity and decreased oxidative stress. Diabetes 2015; 64: 3155–9.
166. Kelly AS, Ryder JR, Marlatt KL, Rudser KD, Jenkins T, Inge TH. Changes in inflammation, oxidative stress and adipokines following bariatric surgery among adolescents with severe obesity. Int J Obes (Lond) 2015; 40: 275–80.
167. Urbanova M, Dostalova I, Trachta P et al. Serum concentrations and subcutaneous adipose tissue mRNA expression of omentin in morbid obesity and type 2 diabetes mellitus: the effect of very-low-calorie diet, physical activity and laparoscopic sleeve gastrectomy. Physiol Res 2014; 63: 207–18.
168. Bruna M, Gumbau V, Guaita M et al. Prospective study of gluco-lipidic hormone and peptide levels in morbidly obese patients after sleeve gastrectomy. Cir Esp 2014; 92: 175–81.
169. Trachta P, Dostalova I, Haluzikova D et al. Laparoscopic sleeve gastrectomy ameliorates mRNA expression of inflammation-related genes in subcutaneous adipose tissue but not in peripheral monocytes of obese patients. Mol Cell Endocrinol 2014; 383: 96–102.
170. Costa Justus JF, Ligocki Campos AC, Figueroa AL et al. Early effect of bariatric surgery on the circadian rhythms of adipokines in morbidly obese women. Metab Syndr Relat Disord 2016; 14: 16–22.
171. Montecucco F, Lenglet S, Quercioli A et al. Gastric bypass in morbid obese patients is associated with reduction in adipose tissue inflammation via N-oleoylethanolamide (OEA)-mediated pathways. Thromb Haemost 2015; 113: 838–50.
172. Butte NF, Brandt ML, Wong WW et al. Energetic adaptations persist after bariatric surgery in severely obese adolescents. Obesity 2015; 23: 591–601.
173. Chang EJ, Lee SK, Song YS et al. IL-34 is associated with obesity, chronic inflammation, and insulin resistance. J Clin Endocrinol Metab 2014; 99: E1263–E71.
174. Moreno-Navarrete JM, Novelle MG, Catalan V et al. Insulin resistance modulates iron-related proteins in adipose tissue. Diabetes Care 2014; 37: 1092–100.
175. Iannelli A, Martini F, Rodolphe A et al. Body composition, anthropometrics, energy expenditure, systemic inflammation, in premenopausal women 1 year after laparoscopic Roux-en-Y gastric bypass. Surg Endosc 2014; 28: 500–07.
176. Barazzoni R, Palmisano S, Gortan Cappellari G et al. Gastric bypass-induced weight loss alters obesity-associated patterns of plasma pentraxin-3 and systemic inflammatory markers. Surg Obes Relat Dis : official journal of the American Society for Bariatric Surgery 2016; 12: 23–32.
177. Mocanu AO, Mulya A, Huang H et al. Effect of Roux-en-Y gastric bypass on the NLRP3 inflammasome in adipose tissue from obese rats. PLoS One 2015; 10 e0139764.
178. Vaittinen M, Walle P, Kuosmanen E et al. FADS2 genotype regulates delta-6 desaturase activity and inflammation in human adipose tissue. J Lipid Res 2016; 57: 56–65.
179. Oliveira Cda S, Beserra BT, Cunha RS et al. Impact of Roux-en-Y gastric bypass on lipid and inflammatory profiles. Rev Col Bras Cir 2015; 42: 305–10.
180. Gjessing HR, Nielsen HJ, Mellgren G, Gudbrandsen OA. Energy intake, nutritional status and weight reduction in patients one year after laparoscopic sleeve gastrectomy. Springer plus 2013; 2: 352.
181. Moncada R, Rodriguez A, Becerril S et al. Sleeve gastrectomy decreases body weight, whole-body adiposity, and blood pressure even in aged diet-induced obese rats. Obes Surg 2015. doi: 10.1007/s11695-015-1919-9.
182. Moncada R, Becerril S, Rodriguez A et al. Sleeve gastrectomy reduces body weight and improves metabolic profile also in obesity-prone rats. Obes Surg 2015. doi: 10.1007/s11695-015-1915-0.
183. Wen Y, Lin N, Yan HT et al. Down-regulation of renal gluconeogenesis in type II diabetic rats following Roux-en-Y gastric bypass surgery: a potential mechanism in hypoglycemic effect. Obes Facts 2015; 8: 110–24.
184. Kawano Y, Ohta M, Hirashita T, Masuda T, Inomata M, Kitano S. Effects of sleeve gastrectomy on lipid metabolism in an obese diabetic rat model. Obes Surg 2013; 23: 1947–56.
185. Cummings BP, Bettaieb A, Graham JL et al. Vertical sleeve gastrectomy improves glucose and lipid metabolism and delays diabetes onset in UCD-T2DM rats. Endocrinology 2012; 153: 3620–32.
186. Rideout DA, Peng Y, Rakita SS et al. Roux-en-Y gastric bypass alters tumor necrosis factor-alpha but not adiponectin signaling in immediate postoperative period in obese rats. Surg Obes Relat Dis 2010; 6: 676–80.
187. Nausheen S, Shah IH, Pezeshki A, Sigalet DL, Chelikani PK. Effects of sleeve gastrectomy and ileal transposition, alone and in combination, on food intake, body weight, gut hormones, and glucose metabolism in rats. Am J Physiol EndocrinolMetab 2013; 305: E507–E18.
188. Rodriguez A, Becerril S, Valenti V et al. Short-term effects of sleeve gastrectomy and caloric restriction on blood pressure in diet-induced obese rats. Obes Surg 2012; 22: 1481–90.
189. Bielohuby M, Stemmer K, Berger J et al. Carbohydrate content of post-operative diet influences the effect of vertical sleeve gastrectomy on body weight reduction in obese rats. Obes Surg 2012; 22: 140–51.
190. Oberbach A, Neuhaus J, Schlichting N, Kugler J, Baumann S, Till H. Sleeve gastrectomy reduces xanthine oxidase and uric acid in a rat model of morbid obesity. Surg Obes Relat Dis 2014; 10: 684–90.
191. Schneck AS, Iannelli A, Patouraux S et al. Effects of sleeve gastrectomy in high fat diet-induced obese mice: respective role of reduced caloric intake, white adipose tissue inflammation and changes in adipose tissue and ectopic fat depots. Surg Endosc 2014; 28: 592–602.