Abstract
Background/Objectives:
Inflammation, oxidative stress and dysregulation of adipokines are thought to be pathophysiological mechanisms linking obesity to the development of insulin resistance and atherosclerosis. In adults, bariatric surgery reduces inflammation and oxidative stress, and beneficially changes the levels of several adipokines, but little is known about the postsurgical changes among adolescents.
Subjects/Methods:
In two separate longitudinal cohorts we evaluated change from baseline of interleukin-6 (IL-6), tumor necrosis factor-alpha (TNF-α), monocyte chemo-attractant protein-1 (MCP-1), oxidized low-density lipoprotein cholesterol (oxLDL), adiponectin, leptin and resistin up to 12 months following elective laparoscopic Roux-en-Y gastric bypass (RYGB) or vertical sleeve gastrectomy (VSG) surgery in adolescents with severe obesity.
Results:
In cohort 1, which consisted of 39 adolescents (mean age 16.5±1.6 years; 29 females) undergoing either RYGB or VSG, IL-6 (baseline: 2.3±3.4 pg ml−1 vs 12 months: 0.8±0.6 pg ml−1, P<0.01), leptin (baseline: 178±224 ng ml−1 vs 12 months: 41.4±31.9 ng ml−1, P<0.001) and oxLDL (baseline: 41.6±11.6 U l−1 vs 12 months: 35.5±11.1 U l−1, P=0.001) significantly decreased and adiponectin significantly increased (baseline: 5.4±2.4 μg ml−1 vs 12 months: 13.5±8.9 μg ml−1, P<0.001). In cohort 2, which consisted of 13 adolescents (mean age 16.5±1.6 years; 10 females) undergoing RYGB, results were similar: IL-6 (baseline: 1.7±0.9 pg ml−1 vs 12 months: 0.4±0.9 pg ml−1, P<0.05) and leptin (baseline: 92.9±31.3 ng ml−1 vs 12 months: 37.3±33.4 ng ml−1, P<0.001) significantly decreased and adiponectin significantly increased (baseline: 6.1±2.9 μg ml−1 vs 12 months: 15.4±8.0 μg ml−1, P<0.001). When the cohorts were combined to evaluate changes at 12 months, oxLDL also significantly decreased (baseline: 39.8±16.7 U l−1 vs 12 months: 32.7±11.9 U l−1, P=0.03).
Conclusions:
Bariatric surgery produced robust improvements in markers of inflammation, oxidative stress and several adipokines among adolescents with severe obesity, suggesting potential reductions in risk for type 2 diabetes and cardiovascular disease.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Kelly AS, Metzig AM, Schwarzenberg SJ, Norris AL, Fox CK, Steinberger J . Hyperleptinemia and hypoadiponectinemia in extreme pediatric obesity. Metab Syndr Relat Disord 2012; 10: 123–127.
Norris AL, Steinberger J, Steffen LM, Metzig AM, Schwarzenberg SJ, Kelly AS . Circulating oxidized LDL and inflammation in extreme pediatric obesity. Obesity (Silver Spring) 2011; 19: 1415–1419.
Kapiotis S, Holzer G, Schaller G, Haumer M, Widhalm H, Weghuber D et al. A proinflammatory state is detectable in obese children and is accompanied by functional and morphological vascular changes. Arterioscler Thromb Vasc Biol 2006; 26: 2541–2546.
Kelly AS, Barlow SE, Rao G, Inge TH, Hayman LL, Steinberger J et al. Severe obesity in children and adolescents: identification, associated health risks, and treatment approaches: a scientific statement from the American Heart Association. Circulation 2013; 128: 1689–1712.
Weiss R, Dziura J, Burgert TS, Tamborlane WV, Taksali SE, Yeckel CW et al. Obesity and the metabolic syndrome in children and adolescents. N Engl J Med 2004; 350: 2362–2374.
Alqahtani AR, Antonisamy B, Alamri H, Elahmedi M, Zimmerman VA . Laparoscopic sleeve gastrectomy in 108 obese children and adolescents aged 5 to 21 years. Ann Surg 2012; 256: 266–273.
Inge TH, Jenkins TM, Zeller M, Dolan L, Daniels SR, Garcia VF et al. Baseline BMI is a strong predictor of Nadir BMI after adolescent gastric bypass. J Pediatr 2010; 156: 103–108.
O'Brien PE, Sawyer SM, Laurie C, Brown WA, Skinner S, Veit F et al. Laparoscopic adjustable gastric banding in severely obese adolescents: a randomized trial. JAMA 2010; 303: 519–526.
Auguet T, Terra X, Hernandez M, Sabench F, Porras JA, Orellana-Gavalda JM et al. Clinical and adipocytokine changes after bariatric surgery in morbidly obese women. Obesity (Silver Spring) 2014; 22: 188–194.
Hakeam HA, O’Regan PJ, Salem AM, Bamehriz FY, Jomaa LF . Inhibition of C-reactive protein in morbidly obese patients after laparoscopic sleeve gastrectomy. Obes Surg 2009; 19: 456–460.
Illan-Gomez F, Gonzalvez-Ortega M, Orea-Soler I, Alcaraz-Tafalla MS, Aragon-Alonso A, Pascual-Diaz M et al. Obesity and inflammation: change in adiponectin, C-reactive protein, tumour necrosis factor-alpha and interleukin-6 after bariatric surgery. Obes Surg 2012; 22: 950–955.
Miller GD, Nicklas BJ, Fernandez A . Serial changes in inflammatory biomarkers after Roux-en-Y gastric bypass surgery. Surg Obes Relat Dis 2011; 7: 618–624.
Rao SR . Inflammatory markers and bariatric surgery: a meta-analysis. Inflamm Res 2012; 61: 789–807.
Ruiz-Tovar J, Oller I, Galindo I, Llavero C, Arroyo A, Calero A et al. Change in levels of C-reactive protein (CRP) and serum cortisol in morbidly obese patients after laparoscopic sleeve gastrectomy. Obes Surg 2013; 23: 764–769.
Uzun H, Zengin K, Taskin M, Aydin S, Simsek G, Dariyerli N . Changes in leptin, plasminogen activator factor and oxidative stress in morbidly obese patients following open and laparoscopic Swedish adjustable gastric banding. Obes Surg 2004; 14: 659–665.
Butte NF, Brandt ML, Wong WW, Liu Y, Mehta NR, Wilson TA et al. Energetic adaptations persist after bariatric surgery in severely obese adolescents. Obesity (Silver Spring) 2015; 23: 591–601.
Balagopal PB, de Ferranti SD, Cook S, Daniels SR, Gidding SS, Hayman LL et al. Nontraditional risk factors and biomarkers for cardiovascular disease: mechanistic, research, and clinical considerations for youth: a scientific statement from the American Heart Association. Circulation 2011; 123: 2749–2769.
Inge TH, Zeller M, Harmon C, Helmrath M, Bean J, Modi A et al. Teen-Longitudinal Assessment of Bariatric Surgery: methodological features of the first prospective multicenter study of adolescent bariatric surgery. J Pediatr Surg 2007; 42: 1969–1971.
Miyano G, Jenkins TM, Xanthakos SA, Garcia VF, Inge TH . Perioperative outcome of laparoscopic Roux-en-Y gastric bypass: a children’s hospital experience. J Pediatr Surg 2013; 48: 2092–2098.
Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC . Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985; 28: 412–419.
Pai JK, Pischon T, Ma J, Manson JE, Hankinson SE, Joshipura K et al. Inflammatory markers and the risk of coronary heart disease in men and women. N Engl J Med 2004; 351: 2599–2610.
Ridker PM, Rifai N, Rose L, Buring JE, Cook NR . Comparison of C-reactive protein and low-density lipoprotein cholesterol levels in the prediction of first cardiovascular events. N Engl J Med 2002; 347: 1557–1565.
Bertoni AG, Burke GL, Owusu JA, Carnethon MR, Vaidya D, Barr RG et al. Inflammation and the incidence of type 2 diabetes: the Multi-Ethnic Study of Atherosclerosis (MESA). Diabetes Care 2010; 33: 804–810.
Hu FB, Meigs JB, Li TY, Rifai N, Manson JE . Inflammatory markers and risk of developing type 2 diabetes in women. Diabetes 2004; 53: 693–700.
Holvoet P, Mertens A, Verhamme P, Bogaerts K, Beyens G, Verhaeghe R et al. Circulating oxidized LDL is a useful marker for identifying patients with coronary artery disease. Arterioscler Thromb Vasc Biol 2001; 21: 844–848.
Yui S, Sasaki T, Miyazaki A, Horiuchi S, Yamazaki M . Induction of murine macrophage growth by modified LDLs. Arterioscler Thromb 1993; 13: 331–337.
Kelly AS, Jacobs DR Jr, Sinaiko AR, Moran A, Steffen LM, Steinberger J . Relation of circulating oxidized LDL to obesity and insulin resistance in children. Pediatr Diabetes 2010; 11: 552–555.
Bacha F, Saad R, Gungor N, Arslanian SA . Adiponectin in youth: relationship to visceral adiposity, insulin sensitivity, and beta-cell function. Diabetes Care 2004; 27: 547–552.
Maahs DM, Ogden LG, Kinney GL, Wadwa P, Snell-Bergeon JK, Dabelea D et al. Low plasma adiponectin levels predict progression of coronary artery calcification. Circulation 2005; 111: 747–753.
Verges B, Petit JM, Duvillard L, Dautin G, Florentin E, Galland F et al. Adiponectin is an important determinant of apoA-I catabolism. Arterioscler Thromb Vasc Biol 2006; 26: 1364–1369.
Terra X, Auguet T, Guiu-Jurado E, Berlanga A, Orellana-Gavalda JM, Hernandez M 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: 1790–1798.
Cambuli VM, Musiu MC, Incani M, Paderi M, Serpe R, Marras V et al. Assessment of adiponectin and leptin as biomarkers of positive metabolic outcomes after lifestyle intervention in overweight and obese children. J Clin Endocrinol Metab 2008; 93: 3051–3057.
Gallistl S, Sudi KM, Aigner R, Borkenstein M . Changes in serum interleukin-6 concentrations in obese children and adolescents during a weight reduction program. Int J Obes Relat Metab Disord 2001; 25: 1640–1643.
Murer SB, Knopfli BH, Aeberli I, Jung A, Wildhaber J, Wildhaber-Brooks J et al. Baseline leptin and leptin reduction predict improvements in metabolic variables and long-term fat loss in obese children and adolescents: a prospective study of an inpatient weight-loss program. Am J Clin Nutr 2011; 93: 695–702.
Reinehr T, Roth C, Menke T, Andler W . Adiponectin before and after weight loss in obese children. J Clin Endocrinol Metab 2004; 89: 3790–3794.
Roberts CK, Izadpanah A, Angadi SS, Barnard RJ . Effects of an intensive short-term diet and exercise intervention: comparison between normal-weight and obese children. Am J Physiol Regul Integr Comp Physiol 2013; 305: R552–R557.
Roth CL, Kratz M, Ralston MM, Reinehr T . Changes in adipose-derived inflammatory cytokines and chemokines after successful lifestyle intervention in obese children. Metabolism 2011; 60: 445–452.
Ryder JR, Vega-Lopez S, Gaesser GA, Buman MP, Shaibi GQ . Heterogeneous vascular responses to lifestyle intervention in obese Latino adolescents. Metab Syndr Relat Disord 2014; 12: 509–515.
Kelly AS, Steinberger J, Olson TP, Dengel DR . In the absence of weight loss, exercise training does not improve adipokines or oxidative stress in overweight children. Metabolism 2007; 56: 1005–1009.
Balagopal P, George D, Patton N, Yarandi H, Roberts WL, Bayne E et al. Lifestyle-only intervention attenuates the inflammatory state associated with obesity: a randomized controlled study in adolescents. J Pediatr 2005; 146: 342–348.
Danielsson P, Kowalski J, Ekblom O, Marcus C . Response of severely obese children and adolescents to behavioral treatment. Arch Pediatr Adolesc Med 2012; 166: 1103–1108.
Acknowledgements
Funding for the cohort 1 project was provided by the National Institutes of Health: Teen-LABS Grant number U01 DK072493/UM1 DK072493 (awarded to THI) and the National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health, through Grant 8 UL1TR000077. Funding for the cohort 2 project was provided by the National Institute of Diabetes, Digestive, and Kidney, National Institutes of Health through Grants R03DK068228 (awarded to THI) and the National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health, through Grant 8 UL1 TR000077. Support also came from National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health, through Grant UL1TR000114. JRR was supported by a training grant from the NIH/NIDDK (T32-DK083250). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. Funding to perform the biomarker assays was provided by the University of Minnesota, Department of Pediatrics. We thank Dr Angela Mortari and Mr Michael Ehrhardt for performing the assays.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
ASK is a consultant for Novo Nordisk Pharmaceuticals and Takeda Pharmaceuticals as well as serves as the signatory author for a clinical trial sponsored by Novo Nordisk but does not accept personal or professional payment for his services. THI has served as consultant to NPS Pharma and Sanofi (not pertaining to this work) and has obtained grant support from Ethicon Endosurgery (not pertaining to this work). The remaining authors declare no conflict of interest.
Rights and permissions
About this article
Cite this article
Kelly, A., Ryder, J., Marlatt, K. et al. Changes in inflammation, oxidative stress and adipokines following bariatric surgery among adolescents with severe obesity. Int J Obes 40, 275–280 (2016). https://doi.org/10.1038/ijo.2015.174
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ijo.2015.174
This article is cited by
-
Laparoscopic sleeve gastrectomy for obesity treatment in adolescents and young adults: a systematic review and meta-analysis
Langenbeck's Archives of Surgery (2023)
-
Changes in adipokine levels and metabolic profiles following bariatric surgery
BMC Endocrine Disorders (2022)
-
Early unhealthy eating habits underlie morpho-functional changes in the liver and adipose tissue in male rats
Histochemistry and Cell Biology (2022)
-
Effects of sleeve gastrectomy on bone mass, microstructure of femurs and bone metabolism associated serum factors in obese rats
BMC Endocrine Disorders (2021)
-
Inflammatory responses to dietary and surgical weight loss in male and female mice
Biology of Sex Differences (2019)