Abstract
Obesity, associated with increased risk of type 2 diabetes (T2D), cardiovascular disease, and hepatic steatosis et al., has become a major global health problem. Recently, obesity has been proven to be under a status of low-grade, chronic inflammation, which contributes to insulin resistance and T2D. Bariatric surgery is currently an effective treatment for the control of morbid obesity and T2D, which impels ongoing efforts to clarify physiological and molecular mechanisms mediating these benefits. The correlation between obesity, inflammation, and T2D has been revealed to a certain extent, and studies have shed light on the effect of bariatric surgery on inflammatory status of subjects with obesity. Based on recent findings, this review focuses on the relationship between inflammation, obesity, and bariatric surgery.
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Abbreviations
- A1c:
-
Glycated hemoglobin
- AMPK:
-
Adenosine monophosphate-activated protein kinase
- BMI:
-
Body mass index
- BP:
-
Blood pressure
- CCL3:
-
Chemokine ligand 3
- CCL4:
-
Chemokine ligand 4
- CCR2:
-
Chemokine receptor-2
- CRP:
-
C-reactive protein
- CSF-3:
-
Colony-stimulating factor 3
- CXCL10:
-
C-X-C motif chemokine 10
- ER stress:
-
Endoplasmic reticulum stress
- HFD:
-
High-fat diet
- HIF-1α:
-
Hypoxia-inducible factor 1a
- IBD:
-
Inflammatory bowel disease
- IFN-γ:
-
Interferon-γ
- IL-2:
-
Interleukin-2
- IL-4:
-
Interleukin-4
- IL-6:
-
Interleukin-6;
- IL-8:
-
Interleukin-8
- IL-15:
-
Interleukin-15
- IL-18:
-
Interleukin-18
- iNKT cells:
-
Invariant natural killer cells
- IR:
-
Insulin resistance
- JNK:
-
Jun N-terminal kinase
- LAGB:
-
Laparoscopic adjustable gastric banding
- LBPD:
-
Laparoscopic biliopancreatic diversion
- LDL-c:
-
Low-density lipoprotein cholesterol
- LRYGB:
-
Laparoscopic Roux-en-Y gastric bypass
- LSG:
-
Laparoscopic sleeve gastrectomy
- LTB4/LTB4R1:
-
Leukotriene B4/leukotriene B4 receptor 1
- MCP-1:
-
Monocyte chemotactic protein 1
- MHC II:
-
Major histocompatibility complex II
- MIF:
-
Macrophage migration inhibitory factor
- MIP:
-
Macrophage inflammatory protein
- MKP5:
-
Mitogen-activated protein kinase phosphatase 5
- NCR1:
-
NK cell-activating receptor
- NF-ΚB:
-
Nuclear factor kappa B
- NK cells:
-
Natural killer cells
- PAI-1:
-
Plasminogen activator inhibitor-1
- PLAUR:
-
Plasminogen activator urokinase receptor
- ROS:
-
Reactive oxygen species
- SAT:
-
Subcutaneous adipose tissue
- sCD40L:
-
Soluble CD40 ligand
- SG:
-
Sleeve gastrectomy
- STAMP2:
-
Six transmembrane protein of prostate
- T2D:
-
Type 2 diabetes
- TNF-α:
-
Tumor necrosis factor-α
- VAT:
-
Visceral adipose tissue
References
NCD-RisC NRFC. Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet. 2016;387(10026):1377–96.
Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444(7121):860–7.
Arnold M, Pandeya N, Byrnes G, et al. Global burden of cancer attributable to high body-mass index in 2012: a population-based study. Lancet Oncol. 2015;16(1):36–46.
Li S, Xiao J, Ji L, et al. BMI and waist circumference are associated with impaired glucose metabolism and type 2 diabetes in normal weight Chinese adults. J Diabetes Complicat. 2014;28(4):470–6.
Liu L, Lou Q, Guo X, et al. Management status and its predictive factors in patients with type 2 diabetes in China: a nationwide multicenter study. Diabetes Metab Res Rev. 2015;31(8):811–6.
Rucker D, Padwal R, Li SK, et al. Long term pharmacotherapy for obesity and overweight: updated meta-analysis. BMJ. 2007;335(7631):1194–9.
Greenberg I, Stampfer MJ, Schwarzfuchs D, et al. Adherence and success in long-term weight loss diets: the dietary intervention randomized controlled trial (DIRECT). J Am Coll Nutr. 2009;28(2):159–68.
Colquitt JL, Pickett K, Loveman E, et al. Surgery for weight loss in adults. Cochrane Database Syst Rev. 2014;8(8):CD003641.
Knop FK, Taylor R. Mechanism of metabolic advantages after bariatric surgery: it’s all gastrointestinal factors versus it’s all food restriction. Diabetes Care. 2013;36(Suppl 2):S287–91.
Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol. 2011;11(2):98–107.
Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489(7415):242–9.
Zlotnikov-Klionsky Y, Nathansohn-Levi B, Shezen E, et al. Perforin-positive dendritic cells exhibit an immuno-regulatory role in metabolic syndrome and autoimmunity. Immunity. 2015;43(4):776–87.
Spranger J, Kroke A, Mohlig M, et al. Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European prospective investigation into cancer and nutrition (EPIC)-Potsdam Study. Diabetes. 2003;52(3):812–7.
Herder C, Illig T, Rathmann W, et al. Inflammation and type 2 diabetes: results from KORA Augsburg. Gesundheitswesen. 2005;67(Suppl 1):S115–21.
Wu H, Ghosh S, Perrard XD, et al. T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation. 2007;115(8):1029–38.
Deng T, Lyon CJ, Minze LJ, et al. Class II major histocompatibility complex plays an essential role in obesity-induced adipose inflammation. Cell Metab. 2013;17(3):411–22.
Aljada A, Mohanty P, Ghanim H, et al. Increase in intranuclear nuclear factor kappaB and decrease in inhibitor kappaB in mononuclear cells after a mixed meal: evidence for a proinflammatory effect. Am J Clin Nutr. 2004;79(4):682–90.
Watt MJ, Hevener A, Lancaster GI, et al. Ciliary neurotrophic factor prevents acute lipid-induced insulin resistance by attenuating ceramide accumulation and phosphorylation of c-Jun N-terminal kinase in peripheral tissues. Endocrinology. 2006;147(5):2077–85.
Wellen KE, Fucho R, Gregor MF, et al. Coordinated regulation of nutrient and inflammatory responses by STAMP2 is essential for metabolic homeostasis. Cell. 2007;129(3):537–48.
Ye J, Gao Z, Yin J, et al. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am J Physiol Endocrinol Metab. 2007;293(4):E1118–28.
Engin A. Adipose tissue hypoxia in obesity and its impact on preadipocytes and macrophages: hypoxia hypothesis. Adv Exp Med Biol. 2017;960:305–26.
Murphy AM, Thomas A, Crinion SJ, Kent BD, Tambuwala MM, Fabre A, et al. Intermittent hypoxia in obstructive sleep apnoea mediates insulin resistance through adipose tissue inflammation. Eur Respir J. 2017;49(4).
Ozcan U, Cao Q, Yilmaz E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science. 2004;306(5695):457–61.
Hu P, Han Z, Couvillon AD, et al. Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol Cell Biol. 2006;26(8):3071–84.
Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science. 2000;287(5453):664–6.
Cinti S, Mitchell G, Barbatelli G, et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res. 2005;46(11):2347–55.
Hotamisligil GS, Peraldi P, Budavari A, et al. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science. 1996;271(5249):665–8.
Bouter B, Geary N, Langhans W, et al. Diet-genotype interactions in the early development of obesity and insulin resistance in mice with a genetic deficiency in tumor necrosis factor-alpha. Metabolism. 2010;59(7):1065–73.
Dominguez H, Storgaard H, Rask-Madsen C, et al. Metabolic and vascular effects of tumor necrosis factor-alpha blockade with etanercept in obese patients with type 2 diabetes. J Vasc Res. 2005;42(6):517–25.
Elgazar-Carmon V, Rudich A, Hadad N, et al. Neutrophils transiently infiltrate intra-abdominal fat early in the course of high-fat feeding. J Lipid Res. 2008;49(9):1894–903.
Patsouris D, Li PP, Thapar D, et al. Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals. Cell Metab. 2008;8(4):301–9.
Khan IM, Dai PX, Perrard JL, et al. Attenuated adipose tissue and skeletal muscle inflammation in obese mice with combined CD4+ and CD8+ T cell deficiency. Atherosclerosis. 2014;233(2):419–28.
Ying W, Wollam J, Ofrecio JM, et al. Adipose tissue B2 cells promote insulin resistance through leukotriene LTB4/LTB4R1 signaling. J Clin Invest. 2017;127(3):1019–30.
Lee BC, Kim MS, Pae M, et al. Adipose natural killer cells regulate adipose tissue macrophages to promote insulin resistance in obesity. Cell Metab. 2016;23(4):685–98.
Zeng TS, Liu FM, Zhou J, et al. Depletion of Kupffer cells attenuates systemic insulin resistance, inflammation and improves liver autophagy in high-fat diet fed mice. Endocr J. 2015;62(7):615–26.
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(3):574–87.
Ballak DB, Stienstra R, Hijmans A, et al. Combined B- and T-cell deficiency does not protect against obesity-induced glucose intolerance and inflammation. Cytokine. 2013;62(1):96–103.
Kocot J, Dziemidok P, Kielczykowska M, et al. Adipokine profile in patients with type 2 diabetes depends on degree of obesity. Med Sci Monit. 2017;23(10):4995–5004.
Olczyk P, Koprowski R, Komosinska-Vassev K, et al. Adiponectin, leptin, and leptin receptor in obese patients with type 2 diabetes treated with insulin detemir. Molecules. 2017;22(8):1274.
Shetty S, Ramos-Roman MA, Cho YR, et al. Enhanced fatty acid flux triggered by adiponectin overexpression. Endocrinology. 2012;153(1):113–22.
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(11):1288–95.
Ceddia RB, Somwar R, Maida A, et al. Globular adiponectin increases GLUT4 translocation and glucose uptake but reduces glycogen synthesis in rat skeletal muscle cells. Diabetologia. 2005;48(1):132–9.
Awazawa M, Ueki K, Inabe K, et al. Adiponectin suppresses hepatic SREBP1c expression in an AdipoR1/LKB1/AMPK dependent pathway. Biochem Biophys Res Commun. 2009;382(1):51–6.
Yuan F, Li YN, Liu YH, et al. Adiponectin inhibits the generation of reactive oxygen species induced by high glucose and promotes endothelial NO synthase formation in human mesangial cells. Mol Med Rep. 2012;6(2):449–53.
Sun K, Kusminski CM, Scherer PE. Adipose tissue remodeling and obesity. J Clin Invest. 2011;121(6):2094–101.
Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest. 2007;117(1):175–84.
Fleming BD, Mosser DM. Regulatory macrophages: setting the threshold for therapy. Eur J Immunol. 2011;41(9):2498–502.
Ebihara K, Ogawa Y, Masuzaki H, et al. Transgenic overexpression of leptin rescues insulin resistance and diabetes in a mouse model of lipoatrophic diabetes. Diabetes. 2001;50(6):1440–8.
Lord GM, Matarese G, Howard JK, et al. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature. 1998;394(6696):897–901.
Kanda H, Tateya S, Tamori Y, et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest. 2006;116(6):1494–505.
Lagathu C, Bastard JP, Auclair M, et al. Chronic interleukin-6 (IL-6) treatment increased IL-6 secretion and induced insulin resistance in adipocyte: prevention by rosiglitazone. Biochem Biophys Res Commun. 2003;311(2):372–9.
Wensveen FM, Jelencic V, Valentic S, et al. NK cells link obesity-induced adipose stress to inflammation and insulin resistance. Nat Immunol. 2015;16(4):376–85.
Spite M, Hellmann J, Tang Y, et al. Deficiency of the leukotriene B4 receptor, BLT-1, protects against systemic insulin resistance in diet-induced obesity. J Immunol. 2011;187(4):1942–9.
Li P, Oh DY, Bandyopadhyay G, et al. LTB4 promotes insulin resistance in obese mice by acting on macrophages, hepatocytes and myocytes. Nat Med. 2015;21(3):239–47.
Cai D, Yuan M, Frantz DF, et al. Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat Med. 2005;11(2):183–90.
Saghizadeh M, Ong JM, Garvey WT, et al. The expression of TNF alpha by human muscle. Relationship to insulin resistance. J Clin Invest. 1996;97(4):1111–6.
Ehses JA, Perren A, Eppler E, et al. Increased number of islet-associated macrophages in type 2 diabetes. Diabetes. 2007;56(9):2356–70.
De Souza CT, Araujo EP, Bordin S, et al. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology. 2005;146(10):4192–9.
Baffy G. Kupffer cells in non-alcoholic fatty liver disease: the emerging view. J Hepatol. 2009;51(1):212–23.
Khan IM, Perrard XY, Brunner G, et al. Intermuscular and perimuscular fat expansion in obesity correlates with skeletal muscle T cell and macrophage infiltration and insulin resistance. Int J Obes. 2015;39(11):1607–18.
Le NH, Kim CS, Park T, et al. Quercetin protects against obesity-induced skeletal muscle inflammation and atrophy. Mediat Inflamm. 2014;2014(2014):834294.
Hong EG, Ko HJ, Cho YR, et al. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes. 2009;58(11):2525–35.
Luck H, Tsai S, Chung J, et al. Regulation of obesity-related insulin resistance with gut anti-inflammatory agents. Cell Metab. 2015;21(4):527–42.
Monteiro-Sepulveda M, Touch S, Mendes-Sa C, et al. Jejunal T cell inflammation in human obesity correlates with decreased enterocyte insulin signaling. Cell Metab. 2015;22(1):113–24.
Obici S, Rossetti L. Minireview: nutrient sensing and the regulation of insulin action and energy balance. Endocrinology. 2003;144(12):5172–8.
Zhang X, Zhang G, Zhang H, et al. Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity. Cell. 2008;135(1):61–73.
Carter PL. The evolution of bariatric surgery. Am J Surg. 2015;209(5):779–82.
Biertho L, Lebel S, Marceau S, et al. Perioperative complications in a consecutive series of 1000 duodenal switches. Surg Obes Relat Dis. 2013;9(1):63–8.
Salminen P, Helmio M, Ovaska J, et al. Effect of laparoscopic sleeve gastrectomy vs laparoscopic Roux-en-Y gastric bypass on weight loss at 5 years among patients with morbid obesity: the SLEEVEPASS randomized clinical trial. JAMA. 2018;319(3):241–54.
Shen X, Zhang X, Bi J, et al. Long-term complications requiring reoperations after laparoscopic adjustable gastric banding: a systematic review. Surg Obes Relat Dis. 2015;11(4):956–64.
Adams TD, Davidson LE, Litwin SE, et al. Weight and metabolic outcomes 12 years after gastric bypass. N Engl J Med. 2017;377(12):1143–55.
Dixon JB, O’Brien PE, Playfair J, et al. Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial. JAMA. 2008;299(3):316–23.
Ikramuddin S, Korner J, Lee WJ, et al. Roux-en-Y gastric bypass vs intensive medical management for the control of type 2 diabetes, hypertension, and hyperlipidemia: the Diabetes Surgery Study randomized clinical trial. JAMA. 2013;309(21):2240–9.
Wentworth JM, Playfair J, Laurie C, et al. Multidisciplinary diabetes care with and without bariatric surgery in overweight people: a randomised controlled trial. Lancet Diabetes Endocrinol. 2014;2(7):545–52.
Schauer PR, Kashyap SR, Wolski K, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med. 2012;366(17):1567–76.
Schauer PR, Bhatt DL, Kirwan JP, et al. Bariatric surgery versus intensive medical therapy for diabetes—3-year outcomes. N Engl J Med. 2014;370(21):2002–13.
Mingrone G, Panunzi S, De Gaetano A, et al. 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. 2015;386(9997):964–73.
Schauer PR, Bhatt DL, Kirwan JP, et al. Bariatric surgery versus intensive medical therapy for diabetes—5-year outcomes. N Engl J Med. 2017;376(7):641–51.
Pradhan AD, Manson JE, Rifai N, et al. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA. 2001;286(3):327–34.
Randell EW, Twells LK, Gregory DM, et al. Pre-operative and post-operative changes in CRP and other biomarkers sensitive to inflammatory status in patients with severe obesity undergoing laparoscopic sleeve gastrectomy. Clin Biochem. 2017.
Herrera MF, Pantoja JP, Velazquez-Fernandez D, et al. Potential additional effect of omentectomy on metabolic syndrome, acute-phase reactants, and inflammatory mediators in grade III obese patients undergoing laparoscopic Roux-en-Y gastric bypass: a randomized trial. Diabetes Care. 2010;33(7):1413–8.
Mallipedhi A, Prior SL, Barry JD, et al. Changes in inflammatory markers after sleeve gastrectomy in patients with impaired glucose homeostasis and type 2 diabetes. Surg Obes Relat Dis. 2014;10(6):1123–8.
Cancello R, Rouault C, Guilhem G, et al. Urokinase plasminogen activator receptor in adipose tissue macrophages of morbidly obese subjects. Obes Facts. 2011;4(1):17–25.
Dillard TH, Purnell JQ, Smith MD, et al. Omentectomy added to Roux-en-Y gastric bypass surgery: a randomized, controlled trial. Surg Obes Relat Dis. 2013;9(2):269–75.
Alfadda AA, Turjoman AA, Moustafa AS, et al. A proteomic analysis of excreted and circulating proteins from obese patients following two different weight-loss strategies. Exp Biol Med (Maywood). 2014;239(5):568–80.
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(6):2892–6.
Sdralis E, Argentou M, Mead N, et al. A prospective randomized study comparing patients with morbid obesity submitted to sleeve gastrectomy with or without omentectomy. Obes Surg. 2013;23(7):965–71.
Garcia-Fuentes E, Garcia-Almeida JM, Garcia-Arnes J, et al. Plasma visfatin concentrations in severely obese subjects are increased after intestinal bypass. Obesity (Silver Spring). 2007;15(10):2391–5.
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(1–2):96–102.
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(11):4619–23.
Pardina E, Ferrer R, Rivero J, et al. Alterations in the common pathway of coagulation during weight loss induced by gastric bypass in severely obese patients. Obesity (Silver Spring). 2012;20(5):1048–56.
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(11):1464–74.
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(8):2277–86.
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 (Silver Spring). 2013;21(3):E182–9.
Carvalho BM, Oliveira AG, Ueno M, et al. Modulation of double-stranded RNA-activated protein kinase in insulin sensitive tissues of obese humans. Obesity (Silver Spring). 2013;21(12):2452–7.
Fenske WK, Dubb S, Bueter M, et al. Effect of bariatric surgery-induced weight loss on renal and systemic inflammation and blood pressure: a 12-month prospective study. Surg Obes Relat Dis. 2013;9(4):559–68.
Toubal A, Clement K, Fan R, et al. SMRT-GPS2 corepressor pathway dysregulation coincides with obesity-linked adipocyte inflammation. J Clin Invest. 2013;123(1):362–79.
Bueter M, Dubb SS, Gill A, et al. Renal cytokines improve early after bariatric surgery. Br J Surg. 2010;97(12):1838–44.
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(1):131–9.
Hand LE, Usan P, Cooper GJ, et al. Adiponectin induces A20 expression in adipose tissue to confer metabolic benefit. Diabetes. 2015;64(1):128–36.
Haider DG, Schindler K, Prager G, et al. Serum retinol-binding protein 4 is reduced after weight loss in morbidly obese subjects. J Clin Endocrinol Metab. 2007;92(3):1168–71.
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(2):207–18.
Moschen AR, Wieser V, Gerner RR, et al. Adipose tissue and liver expression of SIRT1, 3, and 6 increase after extensive weight loss in morbid obesity. J Hepatol. 2013;59(6):1315–22.
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 (Silver Spring). 2013;21(7):1335–42.
Catalan V, Gomez-Ambrosi J, Rodriguez A, et al. Increased circulating and visceral adipose tissue expression levels of YKL-40 in obesity-associated type 2 diabetes are related to inflammation: impact of conventional weight loss and gastric bypass. J Clin Endocrinol Metab. 2011;96(1):200–9.
Moschen AR, Molnar C, Geiger S, et al. Anti-inflammatory effects of excessive weight loss: potent suppression of adipose interleukin 6 and tumour necrosis factor alpha expression. Gut. 2010;59(9):1259–64.
Gumbau V, Bruna M, Canelles E, et al. A prospective study on inflammatory parameters in obese patients after sleeve gastrectomy. Obes Surg. 2014;24(6):903–8.
Farey JE, Fisher OM, Levert-Mignon AJ, et al. Decreased levels of circulating cancer-associated protein biomarkers following bariatric surgery. Obes Surg. 2017;27(3):578–85.
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(8):1252–61.
Swarbrick MM, Stanhope KL, Austrheim-Smith IT, et al. Longitudinal changes in pancreatic and adipocyte hormones following Roux-en-Y gastric bypass surgery. Diabetologia. 2008;51(10):1901–11.
Whitson BA, Leslie DB, Kellogg TA, et al. Adipokine response in diabetics and nondiabetics following the Roux-en-Y gastric bypass: a preliminary study. J Surg Res. 2007;142(2):295–300.
Holdstock C, Lind L, Engstrom BE, et al. CRP reduction following gastric bypass surgery is most pronounced in insulin-sensitive subjects. Int J Obes. 2005;29(10):1275–80.
Ballesteros-Pomar MD, Calleja S, Diez-Rodriguez R, et al. Inflammatory status is different in relationship to insulin resistance in severely obese people and changes after bariatric surgery or diet-induced weight loss. Exp Clin Endocrinol Diabetes. 2014;122(10):592–6.
Garrido-Sanchez L, Tome M, Santiago-Fernandez C, et al. Adipose tissue biomarkers involved in early resolution of type 2 diabetes after bariatric surgery. Surg Obes Relat Dis. 2017;13(1):70–7.
Querfeld U. Vitamin D and inflammation. Pediatr Nephrol. 2013;28(4):605–10.
Liu Y, Aron-Wisnewsky J, Marcelin G, et al. Accumulation and changes in composition of collagens in subcutaneous adipose tissue after bariatric surgery. J Clin Endocrinol Metab. 2016;101(1):293–304.
Moreno-Navarrete JM, Ortega F, Gomez-Serrano M, et al. The MRC1/CD68 ratio is positively associated with adipose tissue lipogenesis and with muscle mitochondrial gene expression in humans. PLoS One. 2013;8(8):e70810.
Frikke-Schmidt H, Zamarron BF, O'Rourke RW, et al. Weight loss independent changes in adipose tissue macrophage and T cell populations after sleeve gastrectomy in mice. Mol Metab. 2017;6(4):317–26.
Zhang H, Wang Y, Zhang J, et al. Bariatric surgery reduces visceral adipose inflammation and improves endothelial function in type 2 diabetic mice. Arterioscler Thromb Vasc Biol. 2011;31(9):2063–9.
Bradley D, Conte C, Mittendorfer B, et al. Gastric bypass and banding equally improve insulin sensitivity and beta cell function. J Clin Invest. 2012;122(12):4667–74.
Xu XJ, Apovian C, Hess D, et al. Improved insulin sensitivity 3 months after RYGB surgery is associated with increased subcutaneous adipose tissue AMPK activity and decreased oxidative stress. Diabetes. 2015;64(9):3155–9.
Hagman DK, Larson I, Kuzma JN, et al. The short-term and long-term effects of bariatric/metabolic surgery on subcutaneous adipose tissue inflammation in humans. Metabolism. 2017;70(5):12–22.
Liu L, Feng J, Zhang G, et al. Visceral adipose tissue is more strongly associated with insulin resistance than subcutaneous adipose tissue in Chinese subjects with pre-diabetes. Curr Med Res Opin. 2017;34(1):1–7.
Kratz M, Coats BR, Hisert KB, et al. Metabolic dysfunction drives a mechanistically distinct proinflammatory phenotype in adipose tissue macrophages. Cell Metab. 2014;20(4):614–25.
Xu X, Grijalva A, Skowronski A, et al. Obesity activates a program of lysosomal-dependent lipid metabolism in adipose tissue macrophages independently of classic activation. Cell Metab. 2013;18(6):816–30.
Kosteli A, Sugaru E, Haemmerle G, et al. Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J Clin Invest. 2010;120(10):3466–79.
Pendyala S, Neff LM, Suarez-Farinas M, et al. Diet-induced weight loss reduces colorectal inflammation: implications for colorectal carcinogenesis. Am J Clin Nutr. 2011;93(2):234–42.
Li S, Vinci A, Behnsen J, et al. Bariatric surgery attenuates colitis in an obese murine model. Surg Obes Relat Dis. 2017;13(4):661–8.
Aminian A, Andalib A, Ver MR, et al. Outcomes of bariatric surgery in patients with inflammatory bowel disease. Obes Surg. 2016;26(6):1186–90.
Yin YN, Yu QF, Fu N, et al. Effects of four Bifidobacteria on obesity in high-fat diet induced rats. World J Gastroenterol. 2010;16(27):3394–401.
Xie N, Cui Y, Yin YN, et al. Effects of two lactobacillus strains on lipid metabolism and intestinal microflora in rats fed a high-cholesterol diet. BMC Complement Altern Med. 2011;11(3):53.
Guo Y, Huang ZP, Liu CQ, et al. Modulation of the gut microbiome: a systematic review of the effect of bariatric surgery. Eur J Endocrinol. 2017;178(1):43–56.
Liu R, Hong J, Xu X, et al. Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention. Nat Med. 2017;23(7):859–68.
Wang C, He B, Piao D, et al. Roux-en-Y esophagojejunostomy ameliorates renal function through reduction of renal inflammatory and fibrotic markers in diabetic nephropathy. Obes Surg. 2016;26(7):1402–13.
Neff KJ, Elliott JA, Corteville C, et al. Effect of Roux-en-Y gastric bypass and diet-induced weight loss on diabetic kidney disease in the Zucker diabetic fatty rat. Surg Obes Relat Dis. 2017;13(1):21–7.
Fu C, Sheu WHH, Lee IT, et al. Weight loss reduces serum monocyte chemoattractant protein-1 concentrations in association with improvements in renal injury in obese men with metabolic syndrome. Clin Chem Lab Med. 2015;53(4):623–9.
Funding
This study was supported by the National Key R&D Program of China (2016YFC1305000, 2016YFC1305001), the National Science and Technology Infrastructure Program (2015BAI12B13), the Key Project of Chinese Ministry of Education(113050A), the National Basic Research Program of China (2014CB910500), National Natural Science Foundation of China (81770775, 91749118, 81370017, 81130015 and 81000316), the Planned Science and Technology Project of Hunan Province (2017RS3015) and Natural Science Foundation of Hunan Province, China (14JJ3034).
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Zhang, C., Zhang, J., Liu, Z. et al. More than an Anti-diabetic Bariatric Surgery, Metabolic Surgery Alleviates Systemic and Local Inflammation in Obesity. OBES SURG 28, 3658–3668 (2018). https://doi.org/10.1007/s11695-018-3400-z
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DOI: https://doi.org/10.1007/s11695-018-3400-z