The effect of exercise training on serum levels of adipokines related to energy homeostasis (adropin, asprosin) and insulin resistance in patients with type 2 diabetes or obesity: A Systematic review and meta-Analysis

Document Type : Review Article I Open Access I Released under (CC BY-NC 4.0) license

Authors

1 Master of Exercise Physiology, Department of Physical Education and Sports Sciences, University of Yasouj, Yasouj, Iran.

2 Professor, Department of Sports Sciences,University of Birjand, Birjand, Iran.

3 Associate Professor, Department of Sports Sciences, Faculty of Sports Sciences, Islamic Azad University, Shiraz Branch, Shiraz, Iran.

Abstract

Aim:  Physical activity as a practical solution plays an important role in increasing adropin and decreasing asprosin and improving insulin resistance and preventing the complications of obesity and overweight. The aim of this study was to investigate the effects of  Physical activity on the serum levels of adipokines related to energy homeostasis (adropin, asprosin) and insulin resistance in patients with type 2 diabetes or obesity. Methods: A systematic search of English and Farsi articles published in PubMed, Web of Science, SID and Magiran databases was conducted until October 2023. Meta-analysis was performed to investigate the effect of  Physical activity on serum levels of adipokines related to energy homeostasis (adropin, asprosin) and insulin resistance in patients with type 2 diabetes or obesity. Mean difference and 95% confidence interval (CI) were calculated using random effect model. Heterogeneity was evaluated using the (I2) test, and publication bias was evaluated by visual analysis of the funnel plot and Egger's test. Findings: A total of 15 studies including 16 sports interventions and 343 subjects in patients with type 2 diabetes or obesity were meta-analyzed. The results showed that exercise training caused a significant increase in serum adropin [SMD=1.05 mg/dL (1.32 To 0.77), P=0/001], It also caused a significant decrease in serum asprosin [SMD=-0.92 mg/dL (-0.46 To -1.38), P=0/001], fasting glucose [SMD=-0.71 mg/dL (-0.45 To -0.97), P=0/001], Insulin [SMD=-0.59 mg/dL (-0.32 To -0.86), P=0/001] And HOMA-IR [SMD=-0.73 mg/dL (-0.47 To -0.99), P=0/001] compared to the control group in patients with type 2 diabetes or obesity. Conclusions:  The results of the present study showed that aerobic exercises have the greatest effect in increasing adropin and decreases in asprosine, fasting glucose, insulin and insulin resistance compared to resistance and combined exercises. Exercise reduces insulin resistance in overweight men, leading to the prevention of diabetes and cardiovascular diseases. It seems that changes caused by physical activity, adropin and asprosin play a role.

Keywords

Main Subjects


  1. Sandrini L, Di Minno A, Amadio P, Ieraci A, Tremoli E, Barbieri SS. Association between Obesity and Circulating Brain-Derived Neurotrophic Factor (BDNF) Levels: Systematic Review of Literature and Meta-Analysis. Int J Mol Sci. 2018;19(8).
  2. Lee MW, Lee M, Oh KJ. Adipose Tissue-Derived Signatures for Obesity and Type 2 Diabetes: Adipokines, Batokines and MicroRNAs. J Clin Med. 2019;8(6).
  3. Kelley DE, Goodpaster BH. Effects of exercise on glucose homeostasis in Type 2 diabetes mellitus. Med Sci Sports Exerc. 2001;33(6 Suppl):S495-501; discussion S28-9.
  4. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract. 2014;103(2):137-49.
  5. Shirinzadeh M, Shakerhosseini R, Hoshiyar rad A. Nutritional Value Assessment and Adequacy of Dietary Intake in Type 2 Diabetic Patients. Iranian Journal of Endocrinology and Metabolism. 2009;11(1):25-32.
  6. Mohamadzadeh Larijan H, Aniseh Nikravan, Aeenparast A. The role of hospital intervention in prevention of diabetes in pre-diabetes patients. Payesh (Health Monitor) Journal. 2019;18(5):465-73.
  7. Simpson SH, Corabian P, Jacobs P, Johnson JA. The cost of major comorbidity in people with diabetes mellitus. Cmaj. 2003;168(13):1661-7.
  8. Yue P, Jin H, Aillaud M, Deng AC, Azuma J, Asagami T, et al. Apelin is necessary for the maintenance of insulin sensitivity. Am J Physiol Endocrinol Metab. 2010;298(1):E59-67.
  9. Lempiäinen P, Mykkänen L, Pyörälä K, Laakso M, Kuusisto J. Insulin resistance syndrome predicts coronary heart disease events in elderly nondiabetic men. Circulation. 1999;100(2):123-8.
  10. Ingelsson E, Arnlöv J, Lind L, Sundström J. Metabolic syndrome and risk for heart failure in middle-aged men. Heart. 2006;92(10):1409-13.
  11. Lakka HM, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, Tuomilehto J, et al. The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. Jama. 2002;288(21):2709-16.
  12. Aydin S, Kuloglu T, Aydin S, Eren MN, Yilmaz M, Kalayci M, et al. Expression of adropin in rat brain, cerebellum, kidneys, heart, liver, and pancreas in streptozotocin-induced diabetes. Mol Cell Biochem. 2013;380(1-2):73-81.
  13. Aydin S. Three new players in energy regulation: preptin, adropin and irisin. Peptides. 2014;56:94-110.
  14. Wong CM, Wang Y, Lee JT, Huang Z, Wu D, Xu A, et al. Adropin is a brain membrane-bound protein regulating physical activity via the NB-3/Notch signaling pathway in mice. J Biol Chem. 2014;289(37):25976-86.
  15. Celik A, Balin M, Kobat MA, Erdem K, Baydas A, Bulut M, et al. Deficiency of a new protein associated with cardiac syndrome X; called adropin. Cardiovasc Ther. 2013;31(3):174-8.
  16. Kumar KG, Trevaskis JL, Lam DD, Sutton GM, Koza RA, Chouljenko VN, et al. Identification of adropin as a secreted factor linking dietary macronutrient intake with energy homeostasis and lipid metabolism. Cell Metab. 2008;8(6):468-81.
  17. Butler AA, Tam CS, Stanhope KL, Wolfe BM, Ali MR, O'Keeffe M, et al. Low circulating adropin concentrations with obesity and aging correlate with risk factors for metabolic disease and increase after gastric bypass surgery in humans. J Clin Endocrinol Metab. 2012;97(10):3783-91.
  18. Yuan M, Li W, Zhu Y, Yu B, Wu J. Asprosin: A Novel Player in Metabolic Diseases. Front Endocrinol (Lausanne). 2020;11:64.
  19. Zhang L, Chen C, Zhou N, Fu Y, Cheng X. Circulating asprosin concentrations are increased in type 2 diabetes mellitus and independently associated with fasting glucose and triglyceride. Clin Chim Acta. 2019;489:183-8.
  20. Nasiri R, Meshkati Z, Nasiri S. Regular aerobic/resistance exercises and garlic extract supplementation effects in pregnancy outcome of Balb/C mice. Journal of Applied Health Studies in Sport Physiology. 2017;4(2):89-96.
  21. Larsen S, Danielsen JH, Søndergård SD, Søgaard D, Vigelsoe A, Dybboe R, et al. The effect of high-intensity training on mitochondrial fat oxidation in skeletal muscle and subcutaneous adipose tissue. Scand J Med Sci Sports. 2015;25(1):e59-69.
  22. Warburton DER, Bredin SSD. Health benefits of physical activity: a systematic review of current systematic reviews. Curr Opin Cardiol. 2017;32(5):541-56.
  23. Humphreys BR, McLeod L, Ruseski JE. Physical activity and health outcomes: evidence from Canada. Health Econ. 2014;23(1):33-54.
  24. Zouhal H, Zare-Kookandeh N, Haghighi MM, Daraei A, de Sousa M, Soltani M, et al. Physical activity and adipokine levels in individuals with type 2 diabetes: A literature review and practical applications. Rev Endocr Metab Disord. 2021;22(4):987-1011.
  25. Rahim Pour R, Mehrabani J. The effect of treadmill aerobic training on adipolin, glucose and insulin in type 2 diabetic male rats. Journal of Applied Health Studies in Sport Physiology. 2018;5(1):93-105.
  26. Moradi G, Ghahramani M. The effect of aerobic and interval training on adropine levels and insulin resistance in overweight men. Journal of Sports and Biomotor Sciences. 2022;14(27):13-23.
  27. Ramezankhani A, Soori R, Ravasi A, Akbarnejad A. An Investigation of the Effects of Long-Term Exercise on Serum Adropin Levels and Improvement of HOMA-IR in Obese Sedentary Women. Journal of Sport Biosciences. 2019;11(3):239-51.
  28. Shiroyeh A, Emami F, Sanaee M, Tarighi R. The Effect of Aerobic Training on Preptin, Adropin and Insulin Resistance in Overweight Men. Journal of Ardabil University of Medical Sciences. 2020;20(4):551-61.
  29. Afroundeh R, bahram ME. The effect of resistance training with body weight (TRX) on serum levels of Perpetin, Adropine and metabolic factors associated with metabolic syndrome in overweight elderly men. Feyz Medical Sciences Journal. 2022;26(3):292-301.
  30. Dolataabadi P, Amirsasan R, Vakili J. The effect of high-intensity interval training on serum Asprosin and lipid profile of overweight and obese women. Journal of Practical Studies of Biosciences in Sport. 2023;11(27):22-33.
  31. Dolataabadi P, Amirsasan R, Vakili J. The effect of high-intensity circuit training on serum asprosin, lipid profile and some fitness factors in overweight and obese women. Journal of Applied Health Studies in Sport Physiology. 2023;10(1):14-26.
  32. Ghalavand A, Mohammadpour M, Rahmani Ghobadi M, Motamedi P, Hovsepian A. Changes in the Serum Levels of Metabotropic Biomarkers (Asprosin and BDNF) in Adaptation to Aerobic Interval Training. Journal of Ilam University of Medical Sciences. 2023;31(2):86-96.
  33. Khalafi M, Malandish A, Rosenkranz SK, Ravasi AA. Effect of resistance training with and without caloric restriction on visceral fat: A systemic review and meta-analysis. Obes Rev. 2021;22(9):e13275.
  34. Kazeminasab F, Sharafifard F, Miraghajani M, Behzadnejad N, Rosenkranz SK. The effects of exercise training on insulin resistance in children and adolescents with overweight or obesity: a systematic review and meta-analysis. Front Endocrinol (Lausanne). 2023;14:1178376.
  35. Khalafi M, Alamdari KA, Symonds ME, Nobari H, Carlos-Vivas J. Impact of acute exercise on immediate and following early post-exercise FGF-21 concentration in adults: systematic review and meta-analysis. Hormones (Athens). 2021;20(1):23-33.
  36. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. Bmj. 1997;315(7109):629-34.
  37. Alizadeh R, Golestani N, Moradi L, Rezaeinejad N. Effect of Aerobic Exercise with Maximal Fat Oxidation Intensity, on Adropin and Insulin Resistance among Overweight Women. Iranian Journal of Endocrinology and Metabolism. 2018;20(2):81-8.
  38. Golestani F, Mogharnasi M, Erfani-Far M, Abtahi-Eivari SH. The effects of spirulina under high-intensity interval training on levels of nesfatin-1, omentin-1, and lipid profiles in overweight and obese females: A randomized, controlled, single-blind trial. J Res Med Sci. 2021;26:10.
  39. Duerrschmid C, He Y, Wang C, Li C, Bournat JC, Romere C, et al. Asprosin is a centrally acting orexigenic hormone. Nat Med. 2017;23(12):1444-53.
  40. Long W, Xie X, Du C, Zhao Y, Zhang C, Zhan D, et al. Decreased Circulating Levels of Asprosin in Obese Children. Horm Res Paediatr. 2019;91(4):271-7.
  41. Ugur K, Aydin S. Saliva and Blood Asprosin Hormone Concentration Associated with Obesity. Int J Endocrinol. 2019;2019:2521096.
  42. Saremi A, Asghari M, Ghorbani A. Effects of aerobic training on serum omentin-1 and cardiometabolic risk factors in overweight and obese men. J Sports Sci. 2010;28(9):993-8.
  43. Asgari A, Niyazi A, Nejatian Hoseinpour A, Setayesh S, Fazolahzade Mousavi R, Mohammad Rahimi GR. The effect of exercise training on serum Omentin-1 levels, glycemic control and body composition in adults population: a systematic review and meta-analysis of randomized controlled trials. International Journal of Diabetes in Developing Countries. 2023.
  44. Amanat S, Sinaei E, Panji M, MohammadporHodki R, Bagheri-Hosseinabadi Z, Asadimehr H, et al. A Randomized Controlled Trial on the Effects of 12 Weeks of Aerobic, Resistance, and Combined Exercises Training on the Serum Levels of Nesfatin-1, Irisin-1 and HOMA-IR. Front Physiol. 2020;11:562895.
  45. Kwak MS, Kim D, Chung GE, Kim W, Kim YJ, Yoon JH. Role of physical activity in nonalcoholic fatty liver disease in terms of visceral obesity and insulin resistance. Liver Int. 2015;35(3):944-52.
  46. Sayın O, Tokgöz Y, Arslan N. Investigation of adropin and leptin levels in pediatric obesity-related nonalcoholic fatty liver disease. J Pediatr Endocrinol Metab. 2014;27(5-6):479-84.
  47. Westerterp-Plantenga MS, Verwegen CR, Ijedema MJ, Wijckmans NE, Saris WH. Acute effects of exercise or sauna on appetite in obese and nonobese men. Physiol Behav. 1997;62(6):1345-54.
  48. Hemmati Moghadam A, Rahmani Ghobadi M, SafiKhani H. The Effect of Six Weeks of High-Intensity CrossFit Training on Serum Asprosin, Body Fat Percentage and Insulin Resistance in Men with Type 2 Diabetes. Journal of Police Medicine. 2023;12(1):1-13.
  49. shirmohamadzade M, ghorbanzadeh B, gorbanian B, saberi y. Examining the Musculoskeletal Condition and Physical Fitness Related to the Health of Physical Protection Personnel. Journal of Police Medicine. 2022;11(1):1-12.
  50. Sampath Kumar A, Maiya AG, Shastry BA, Vaishali K, Ravishankar N, Hazari A, et al. Exercise and insulin resistance in type 2 diabetes mellitus: A systematic review and meta-analysis. Ann Phys Rehabil Med. 2019;62(2):98-103.
  51. Ghalavand A, Rahmani Ghobadi M. Effect of Exercise and Insulin Signaling on Glucose Transporter Type 4 in Skeletal Muscles: A narrative review. The Journal of Shahid Sadoughi University of Medical Sciences. 2023;31(1):6244-57.
  52. da Silva DE, Grande AJ, Roever L, Tse G, Liu T, Biondi-Zoccai G, et al. High-Intensity Interval Training in Patients with Type 2 Diabetes Mellitus: a Systematic Review. Curr Atheroscler Rep. 2019;21(2):8.
  53. Jiménez-Maldonado A, García-Suárez PC, Rentería I, Moncada-Jiménez J, Plaisance EP. Impact of high-intensity interval training and sprint interval training on peripheral markers of glycemic control in metabolic syndrome and type 2 diabetes. Biochim Biophys Acta Mol Basis Dis. 2020;1866(8):165820.
  54. Sünnetçi Silistre E, Hatipoğl HU. Increased serum circulating asprosin levels in children with obesity. Pediatr Int. 2020;62(4):467-76.
  55. Holloszy JO. Exercise-induced increase in muscle insulin sensitivity. J Appl Physiol (1985). 2005;99(1):338-43.
  56. Wang CY, Lin TA, Liu KH, Liao CH, Liu YY, Wu VC, et al. Serum asprosin levels and bariatric surgery outcomes in obese adults. Int J Obes (Lond). 2019;43(5):1019-25.
  57. Ceylan H, Saygın Ö, Özel Türkcü Ü. Assessment of acute aerobic exercise in the morning versus evening on asprosin, spexin, lipocalin-2, and insulin level in overweight/obese versus normal weight adult men. Chronobiol Int. 2020;37(8):1252-68.
  58. Zhang H, Hu W, Zhang G. Circulating asprosin levels are increased in patients with type 2 diabetes and associated with early-stage diabetic kidney disease. Int Urol Nephrol. 2020;52(8):1517-22.
  59. Hong T, Li JY, Wang YD, Qi XY, Liao ZZ, Bhadel P, et al. High Serum Asprosin Levels Are Associated with Presence of Metabolic Syndrome. Int J Endocrinol. 2021;2021:6622129.
  60. Klika B, Jordan C. HIGH-INTENSITY CIRCUIT TRAINING USING BODY WEIGHT: Maximum Results With Minimal Investment. ACSM's Health & Fitness Journal. 2013;17(3):8-13.
  61. Kermani S, Alizadeh R, Moradi L. The effect of eight weeks of resistance training on adropin plasma level and insulin resistance index in overweight men. Journal of Sport and Exercise Physiology. 2021;14(1):31-7.
  62. Ghafari M, Faramarzi M, banitalebi E. Comparison Effect of Continuous and Interval Training on Glycemic Factors in Type 2 Diabetic Patients: A Systematic Review and Meta-Analysis of Internal Articles. Sport Physiology. 2021;13(51):17-42.
  63. Grace A, Chan E, Giallauria F, Graham PL, Smart NA. Clinical outcomes and glycaemic responses to different aerobic exercise training intensities in type II diabetes: a systematic review and meta-analysis. Cardiovasc Diabetol. 2017;16(1):37.
  64. Thomas GN, Jiang CQ, Taheri S, Xiao ZH, Tomlinson B, Cheung BM, et al. A systematic review of lifestyle modification and glucose intolerance in the prevention of type 2 diabetes. Curr Diabetes Rev. 2010;6(6):378-87.
  65. Suh SH, Paik IY, Jacobs K. Regulation of blood glucose homeostasis during prolonged exercise. Mol Cells. 2007;23(3):272-9.
  66. O'Gorman DJ, Karlsson HK, McQuaid S, Yousif O, Rahman Y, Gasparro D, et al. Exercise training increases insulin-stimulated glucose disposal and GLUT4 (SLC2A4) protein content in patients with type 2 diabetes. Diabetologia. 2006;49(12):2983-92.
  67. Roshdi bonab R, Ebrahim K, Ghazalianghazaliyan F, Afrasiabi Rad A. The effect of eight weeks combined exercise training on the levels of adropin and VEGFR-2 in obese men with hypertension. Razi Journal of Medical Sciences. 2019;26(8):78-88.
  68. Asadi V, Azizbeigi K, Khosravi N, Hagh Nazari N. Effect of Exercise Training on Omentin-1 and Vaspin: Comparison of Continuous Endurance, Circuit Resistance, and High Intensity Interval Trainings in Obese Young Men. The Scientific Journal of Rehabilitation Medicine. 2019;8(4):103-12.
  69. rahmati m, Shariatzadeh Joneydi M, Azari N. The Effects of Endurance Exercise on Some Related Variables of Type II Diabetes: Systematic Review and Meta-Analysis of Studies in Iran. Sport Physiology. 2019;11(41):81-104.
  70. Howarth FC, Marzouqi FM, Al Saeedi AM, Hameed RS, Adeghate E. The effect of a heavy exercise program on the distribution of pancreatic hormones in the streptozotocin-induced diabetic rat. Jop. 2009;10(5):485-91.
  71. Kim ES, Im JA, Kim KC, Park JH, Suh SH, Kang ES, et al. Improved insulin sensitivity and adiponectin level after exercise training in obese Korean youth. Obesity (Silver Spring). 2007;15(12):3023-30.
  72. Henriksen EJ. Invited review: Effects of acute exercise and exercise training on insulin resistance. J Appl Physiol (1985). 2002;93(2):788-96.
  73. Bonen A, Dohm GL, van Loon LJ. Lipid metabolism, exercise and insulin action. Essays Biochem. 2006;42:47-59.
  74. Omidi Ghanbari R, Soori R, Hemmatfar A. The Effect of High Running on Serum Adropine and Insulin Resistance Index in Adolescent Obese Boys. Razi Journal of Medical Sciences. 2020;26(12):128-37.
  75. Omidi ghanbari R, Soori R, Hemmatfar A. THE EFFECT OF A PERIOD OF AEROBIC EXERCISE WITH LOW INTENSITY ON ADROPIN LEVELS AND INSULIN RESISTANCE INDEX IN OBESE SEDENTARY ADOLESCENT BOYS. Iranian Journal of Diabetes and Lipid Disorders. 2019;18(5):266-74.
  76. Sharabiani S, Rajabi H, Motamedi P, Dehkhoda M, Kaviani M. The Effect of 8 Weeks of Combined Training on Serum Adropin and Nitric Oxide in Hypertensive Postmenopausal Women. Sport Physiology & Management Investigations. 2019;11(1):129-43.
  77. Hosseini H, Abedi B, Fatolahi H. The Effect of Aerobic water-based training on Adropin levels, insulin resistance and Lipid profile in ageing Men. scientific magazine yafte. 2019;21(1):99-110.