Abstract
Background
To demonstrate the association of irisin levels with impaired glucose before and after laparoscopic sleeve gastrectomy (LSG) in patients with obesity.
Methods
Thirty-six patients with obesity undergoing LSG were included. We tested the irisin levels before and after LSG and conducted an evaluation of baseline irisin levels with elevated glucose as well as irisin changes with weight loss and its association with glucose control after LSG.
Results
Anthropometric measurements, body fat index, and metabolic parameters were significantly improved in 3 months following LSG (all p < 0.05). Baseline irisin levels were significantly higher in obesity with elevated fasting glucose than that with normal glucose (2.98 [2.37, 3.63] vs. 3.72 [3.06, 5.32], p = 0.031). After adjustment for sex, gender, and body mass index (BMI), obesity with higher irisin levels was prone to have impaired fasting glucose (OR = 2.499, 95% CI = 1.047–5.964). According to receiver operating characteristic curve analysis, the diagnostic accuracy and sensitivity of baseline irisin levels on impaired fasting glucose were 75% and 77.8%. Irisin levels decreased from 3.29 (2.67, 4.43) to 2.82 (2.41, 3.25) ng/mL (p = 0.009) after LSG. The decreases of weight, BMI, and FFA were more in irisin changes group (△irisin ≥ 0.5) than in no irisin changes group (△irisin < 0.5). And △irisin was negatively associated with postprandial glucose (PG) at 3 months after LSG (0.5 h-PG, r = − 0.478, p = 0.029; 2 h-PG, r = − 0.406, p = 0.017).
Conclusions
Elevated baseline irisin levels indicated the impaired glucose in obesity. The decrease of irisin with weight loss provided more evidence for the contribution of serum irisin secretion by fat mass in obesity.
Graphical Abstract
Similar content being viewed by others
References
Ng ACT, et al. Diabesity: the combined burden of obesity and diabetes on heart disease and the role of imaging. Nat Rev Cardiol. 2021;18(4):291–304.
Fryar CD, Carroll MD, Ogden CL. Prevalence of overweight, obesity, and severe obesity among adults aged 20 and over: United States, 1960–1962 through 2015–2016. 2018. CDC https://www.cdc.gov/nchs/data/hestat/obesity_adult_15_16/obesity_adult_15_16.htm#Tables. Accessed 20 June 2022.
Fryar CD, Carroll MD, Ogden CL. Prevalence of overweight, obesity, and severe obesity among children and adolescents aged 2–19 years: United States, 1963–1965 through 2015–2016. CDC. 2018. https://www.cdc.gov/nchs/data/hestat/obesity_child_15_16/obesity_child_15_16.htm#Figure. Accessed 20 June 2022.
Chooi YC, Ding C, Magkos F. The epidemiology of obesity. Metabolism. 2019;92:6–10.
Ogurtsova K, et al. IDF Diabetes Atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract. 2017;128:40–50.
Institute for Health Metrics and Evaluation. Global Health Data Exchange. GBD results tool. http://ghdx.healthdata.org/gbd-results-tool (accessed Jan 10, 2021).
Grönroos S, et al. Effect of laparoscopic sleeve gastrectomy vs Roux-en-Y gastric bypass on weight loss and quality of life at 7 years in patients with morbid obesity: the SLEEVEPASS Randomized Clinical Trial. JAMA Surg. 2021;156(2):137–46.
Valenzano A, Tartaglia N, Ambrosi A, Tafuri D, Monda M, Messina A, Sessa F, Campanozzi A, Monda V, Cibelli G, Messina G, Polito R. The metabolic rearrangements of Bariatric surgery: focus on Orexin-A and the Adiponectin system. J Clin Med. 2020;9(10):3327. https://doi.org/10.3390/jcm9103327.
Eickhoff H. Central modulation of energy homeostasis and cognitive performance after bariatric surgery. Adv Neurobiol. 2017;19:213–36.
Boström P, et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481(7382):463–8.
Maak S, et al. Progress and challenges in the biology of FNDC5 and irisin. Endocr Rev. 2021;42(4):436–56.
Seale P, et al. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest. 2011;121(1):96–105.
Xin C, et al. Irisin improves fatty acid oxidation and glucose utilization in type 2 diabetes by regulating the AMPK signaling pathway. Int J Obes (Lond). 2016;40(3):443–51.
Marrano N, Biondi G, Borrelli A, Cignarelli A, Perrini S, Laviola L, Giorgino F, Natalicchio A. Irisin and incretin hormones: similarities, differences, and implications in type 2 diabetes and obesity. Biomolecules. 2021;11(2):286. https://doi.org/10.3390/biom11020286.
Demirpence M, et al. The effect of sleeve gastrectomy on serum irisin levels in patients with morbid obesity. Endokrynol Pol. 2016;67(5):481–6.
Crujeiras AB, et al. Longitudinal variation of circulating irisin after an energy restriction-induced weight loss and following weight regain in obese men and women. Am J Hum Biol. 2014;26(2):198–207.
Garvey WT, et al. American Association of Clinical Endocrinologists and American College of Endocrinology Comprehensive Clinical Practice guidelines for medical care of patients with obesity. Endocr Pract. 2016;22(Suppl 3):1–203.
Shoukry A, et al. Circulating serum irisin levels in obesity and type 2 diabetes mellitus. IUBMB Life. 2016;68(7):544–56.
Zhang R, et al. Association of circulating irisin levels with adiposity and glucose metabolic profiles in a middle-aged chinese population: a cross-sectional study. Diabetes Metab Syndr Obes. 2020;13:4105–12.
Huh JY, et al. FNDC5 and irisin in humans: I. Predictors of circulating concentrations in serum and plasma and II. mRNA expression and circulating concentrations in response to weight loss and exercise. Metabolism. 2012;61(12):1725–38.
Gonzalez-Gil AM, Elizondo-Montemayor L. The role of exercise in the interplay between myokines, hepatokines, osteokines, adipokines, and modulation of inflammation for energy substrate redistribution and fat mass loss: a review. nutrients. 2020;12(6):1899. https://doi.org/10.3390/nu12061899
Roca-Rivada A, et al. FNDC5/irisin is not only a myokine but also an adipokine. PLoS ONE. 2013;8(4): e60563.
Kurdiova T, et al. Effects of obesity, diabetes and exercise on Fndc5 gene expression and irisin release in human skeletal muscle and adipose tissue: in vivo and in vitro studies. J Physiol. 2014;592(5):1091–107.
Polyzos SA, et al. Irisin: a renaissance in metabolism? Metabolism. 2013;62(8):1037–44.
Crujeiras AB, et al. Association between circulating irisin levels and the promotion of insulin resistance during the weight maintenance period after a dietary weight-lowering program in obese patients. Metabolism. 2014;63(4):520–31.
Park KH, et al. Circulating irisin in relation to insulin resistance and the metabolic syndrome. J Clin Endocrinol Metab. 2013;98(12):4899–907.
Stengel A, et al. Circulating levels of irisin in patients with anorexia nervosa and different stages of obesity–correlation with body mass index. Peptides. 2013;39:125–30.
Zhang C, et al. Lower irisin level in patients with type 2 diabetes mellitus: a case-control study and meta-analysis. J Diabetes. 2016;8(1):56–62.
Cui L, et al. Circulating irisin levels of prenatal and postnatal patients with gestational diabetes mellitus: a systematic review and meta-analysis. Cytokine. 2020;126: 154924.
Yang L, et al. Molecular identification of FNDC5 and effect of irisin on the glucose metabolism in common carp (Cyprinus carpio L.). Gen Comp Endocrinol. 2021;301:113647.
Li Q, et al. Metformin-induced autophagy and irisin improves INS-1 cell function and survival in high-glucose environment via AMPK/SIRT1/PGC-1α signal pathway. Food Sci Nutr. 2019;7(5):1695–703.
Natalicchio A, et al. The myokine irisin is released in response to saturated fatty acids and promotes pancreatic β-cell survival and insulin secretion. Diabetes. 2017;66(11):2849–56.
Yang M, et al. Circulating levels of irisin in middle-aged first-degree relatives of type 2 diabetes mellitus - correlation with pancreatic β-cell function. Diabetol Metab Syndr. 2014;6(1):133.
Zheng S, et al. Irisin alleviates FFA induced β-cell insulin resistance and inflammatory response through activating PI3K/AKT/FOXO1 signaling pathway. Endocrine. 2022;75(3):740–51.
Zhu W, Sahar NE, Javaid HMA, Pak ES, Liang G, Wang Y, Ha H, Huh JY. Exercise-induced irisin decreases inflammation and improves NAFLD by competitive binding with MD2. Cells. 2021;10(12):3306. https://doi.org/10.3390/cells10123306.
Mazur-Bialy AI. Superiority of the non-glycosylated form over the glycosylated form of irisin in the attenuation of adipocytic meta-inflammation: a potential factor in the fight against insulin resistance. Biomolecules. 2019;9(9):394. https://doi.org/10.3390/biom9090394.
Lee YJ, Heo Y, Choi JH, Park S, Kim KK, Shin DW, Kang JH. Association of circulating irisin concentrations with weight loss after Roux-en-Y gastric bypass surgery. Int J Environ Res Public Health. 2019;16(4):660. https://doi.org/10.3390/ijerph16040660.
Majorczyk M, et al. The influence of bariatric surgery on serum levels of irisin and nesfatin-1. Acta Chir Belg. 2019;119(6):363–9.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Ethics Approval and Consent to Participate
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The protocol of this study was approved by the Ethics Committee of Shanghai Tenth People’s Hospital. Informed consent was obtained from all individual participants included in the study.
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Key Points
• Obesity with higher irisin levels was prone to have impaired fasting glucose.
• Irisin levels decreased after LSG.
• BMI and FFA decreased more in irisin changes group than in no irisin changes group.
• Irisin changes were negatively associated with PG at 3 months after LSG.
Jiajing Yin and Shaoling Yang contributed equally to this work and shared first authorship.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yin, J., Yang, S., Zha, X. et al. The Association of Serum Irisin with Impaired Glucose Before and After Laparoscopic Sleeve Gastrectomy in Obesity. OBES SURG 33, 780–788 (2023). https://doi.org/10.1007/s11695-022-06426-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11695-022-06426-w