Journal of Isfahan Medical School

Journal of Isfahan Medical School

The Effect of Exercise Training on Liver Fat Accumulation in Children and Adolescents in Individuals with Overweight and Obesity: A Systematic Review and Meta-Analysis

Document Type : Review Article

Authors
Mousa Khalafi 1
Zeinab Fathi 2
Zeinab Nasrolahi 2
1 Assistant Professor, Department of Physical Education and Sport Sciences, School of Humanities, University of Kashan, Kashan, Iran
2 MSc Student, Department of Physical Education and Sport Sciences, School of Humanities, University of Kashan, Kashan, Iran
10.48305/jims.v41.i733.0751
Abstract
Background: The prevalence of obesity in children and adolescents is associated with the accumulation of liver fat. Therefore, the purpose of this meta-analysis is to investigate the effect of exercise training on liver fat accumulation and insulin resistance in children and adolescents with overweight and obesity.
Methods: A comprehensive search was conducted in PubMed, Web of Science, Google Scholar, Magiran, and NoorMags databases from the inception to January 21, 2023. The inclusion criteria for the present meta-analysis included 1) children and adolescents, 2) exercise training, 3) overweight and obesity, 4) studies with a control group or with values measured in the pre-test stage and 4) liver fat as the main variable. To calculate the effect size, standardized mean differences (SMD), weighted mean differences (WMD) and 95% confidence intervals (CIs) were calculated using the random effect model.
Findings: A total, nine studies with eighteen exercise interventions and including 621 children and adolescent were included in the meta-analysis. Exercise result in a decrease in liver fat with a large effect size [SMD: -0.85 (CI: -1.26 to -0.43), P = 0.001], insulin [WMD: -1.32 µU/ml (CI: -2.35 to -0.30), P = 0.01] and insulin resistance [WMD: -0.61 (CI: -1.06 to -0.17), P = 0.007]. While the reduction of glucose was not statistically significant [WMD: -0.52 mg/dl (CI: -1.47 to 0.40), P = 0.26].
Conclusion: Exercise training results in the reduction of liver fat accumulation and improvement of insulin resistance in children and adolescents with overweight and obesity, which is recommended as a main strategy to reduce liver fat and improve metabolism.
Keywords
Adolescents
Child
Exercise training
Insulin resistance
Liver fat
Obesity
Subjects
  1. Wilson PW, D'Agostino RB, Sullivan L, Parise H, Kannel WB. Overweight and obesity as determinants of cardiovascular risk: the Framingham experience. Arch Intern Med 2002; 162(16): 1867-72.
  2. Sahoo K, Sahoo B, Choudhury AK, Sofi NY, Kumar R, Bhadoria AS. Childhood obesity: causes and consequences. J Family Med Prim Care 2015; 4(2): 187-92.
  3. Shaunak M, Byrne CD, Davis N, Afolabi P, Faust SN, Davies JH. Non-alcoholic fatty liver disease and childhood obesity. Arch Dis Child 2021; 106(1): 3-8.
  4. Anderson EL, Howe LD, Jones HE, Higgins JP, Lawlor DA, Fraser A. The prevalence of non-alcoholic fatty liver disease in children and adolescents: a systematic review and meta-analysis. PloS One 2015; 10(10): e014090
  5. Bellentani S, Saccoccio G, Masutti F, Crocè LS, Brandi G, Sasso F, et al. Prevalence of and risk factors for hepatic steatosis in Northern Italy. Ann Intern Med 2000; 132(2): 112-7.
  6. Hwang JH, Stein DT, Barzilai N, Cui MH, Tonelli J, Kishore P, et al. Increased intrahepatic triglyceride is associated with peripheral insulin resistance: in vivo MR imaging and spectroscopy studies. Am J Physiol Endocrinol Metab 2007; 293(6): E1663-9.
  7. García-Hermoso A, Alonso-Martinez AM, Ramírez-Vélez R, Izquierdo M. Effects of exercise intervention on health-related physical fitness and blood pressure in preschool children: A systematic review and meta-analysis of randomized controlled trials. Sports Med 2020; 50(1): 187-203.
  8. González‐Ruíz K, Correa‐Bautista JE, Izquierdo M, García‐Hermoso A, Martínez‐Vizcaíno V, Lobelo F, et al. Exercise dose on hepatic fat and cardiovascular health in adolescents with excess of adiposity. Pediatr Obes 2022; 17(4): e12869.
  9. Klein S, Burke LE, Bray GA, Blair S, Allison DB, Pi-Sunyer X, et al. Clinical implications of obesity with specific focus on cardiovascular disease: a statement for professionals from the American Heart Association Council on Nutrition, Physical Activity, and Metabolism: endorsed by the American College of Cardiology Foundation. Circulation 2004; 110(18): 2952-67.
  10. Villareal DT, Chode S, Parimi N, Sinacore DR, Hilton T, Armamento-Villareal R, et al. Weight loss, exercise, or both and physical function in obese older adults. N Engl J Med 2011; 364(13): 1218-29.
  11. Trost SG, Loprinzi PD. Exercise-promoting healthy lifestyles in children and adolescents. J Clin Lipidol 2008; 2(3): 162-8.
  12. Keating SE, Hackett DA, George J, Johnson NA. Exercise and non-alcoholic fatty liver disease: a systematic review and meta-analysis. J Hepatol 2012; 57(1): 157-66.
  13. Khalafi M, Symonds ME. The impact of high intensity interval training on liver fat content in overweight or obese adults: A meta-analysis. Physiol Behav 2021; 236: 113416.
  14. Medrano M, Arenaza L, Ramírez‐Vélez R, Ortega FB, Ruiz JR, Labayen I. Prevalence of responders for hepatic fat, adiposity and liver enzyme levels in response to a lifestyle intervention in children with overweight/obesity: EFIGRO randomized controlled trial. Pediatr Diabetes 2020; 21(2): 215-23.
  15. Petersen KF, Dufour S, Befroy D, Lehrke M, Hendler RE, Shulman GI. Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes 2005; 54(3): 603-8.
  16. Iraji H, Minasian V, Kelishadi R. Changes in liver enzymes and metabolic profile in adolescents with fatty liver following exercise interventions. Pediatr Gastroenterol Hepatol Nutr 2021; 24(1): 54-64.
  17. Labayen I, Medrano M, Arenaza L, Maiz E, Oses M, Martinez-Vizcaino V, et al. Effects of exercise in addition to a family-based lifestyle intervention program on hepatic fat in children with overweight. Diabetes Care 2020; 43(2): 306-13.
  18. Lee S, Bacha F, Hannon T, Kuk JL, Boesch C, Arslanian S. Effects of aerobic versus resistance exercise without caloric restriction on abdominal fat, intrahepatic lipid, and insulin sensitivity in obese adolescent boys: a randomized, controlled trial. Diabetes 2012; 61(11): 2787-95.
  19. Lee S, Deldin AR, White D, Kim Y, Libman I, Rivera-Vega M, et al. Aerobic exercise but not resistance exercise reduces intrahepatic lipid content and visceral fat and improves insulin sensitivity in obese adolescent girls: a randomized controlled trial. Am J Physiol Endocrinol Metab 2013; 305(10): E1222-9.
  20. Lee S, Libman I, Hughan K, Kuk JL, Jeong JH, Zhang D, et al. Effects of exercise modality on insulin resistance and ectopic fat in adolescents with overweight and obesity: a randomized clinical trial. J Pediatr 2019; 206: 91-8. e1.
  21. van der Heijden GJ, Wang ZJ, Chu ZD, Sauer PJ, Haymond MW, Rodriguez LM, et al. A 12‐week aerobic exercise program reduces hepatic fat accumulation and insulin resistance in obese, Hispanic adolescents. Obesity (Silver Spring) 2010; 18(2): 384-90.
  22. van der Heijden GJ, Wang ZJ, Chu Z, Toffolo G, Manesso E, Sauer PJ, et al. Strength exercise improves muscle mass and hepatic insulin sensitivity in obese youth. Med Sci Sports Exerc 2010; 42(11): 1973-80.
  23. Ramírez-Vélez R, García-Hermoso A, Hackney AC, Izquierdo M. Effects of exercise training on Fetuin-a in obese, type 2 diabetes and cardiovascular disease in adults and elderly: a systematic review and Meta-analysis. Lipids Health Dis 2019; 18(1): 23.
  24. Maillard F, Pereira B, Boisseau N. Effect of high-intensity interval training on total, abdominal and visceral fat mass: a meta-analysis. Sports Med 2018; 48: 269-88.
  25. Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions. Hoboken, NJ: Cochrane Collaboration; 2008.
  26. Wan X, Wang W, Liu J, Tong T. Estimating the
    sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol 2014; 14: 135.
  27. Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions version 5.0.1. Hoboken, NJ: The Cochrane Collaboration; 2008.
  28. De Morton NA. The PEDro scale is a valid measure of the methodological quality of clinical trials: a demographic study. Aust J Physiother 2009; 55(2): 129-33.
  29. Duval S, Tweedie R. Trim and fill: a simple funnel‐plot-based method of testing and adjusting for publication bias in meta‐ Biometrics 2000; 56(2): 455-63.
  30. Kotronen A, Juurinen L, Tiikkainen M, Vehkavaara S, Yki-Järvinen H. Increased liver fat, impaired insulin clearance, and hepatic and adipose tissue insulin resistance in type 2 diabetes. Gastroenterology 2008; 135(1): 122-30.
  31. Kolak M, Westerbacka J, Velagapudi VR, Wågsäter D, Yetukuri L, Makkonen J, et al. Adipose tissue inflammation and increased ceramide content characterize subjects with high liver fat content independent of obesity. Diabetes 2007; 56(8): 1960-8.
  32. Geurtsen ML, Santos S, Felix JF, Duijts L, Vernooij MW, Gaillard R, et al. Liver fat and cardiometabolic risk factors among school‐age children. Hepatology 2020; 72(1): 119-29.
  33. Sargeant JA, Gray LJ, Bodicoat DH, Willis SA, Stensel DJ, Nimmo MA, et al. The effect of exercise training on intrahepatic triglyceride and hepatic insulin sensitivity: a systematic review and meta-analysis. Obes Rev 2018; 19(10): 1446-59.
  34. Medrano M, Cadenas-Sanchez C, Alvarez-Bueno C, Cavero-Redondo I, Ruiz JR, Ortega FB, et al. Evidence-based exercise recommendations to reduce hepatic fat content in youth-a systematic review and meta-analysis. Prog Cardiovasc Dis 2018; 61(2): 222-31.
  35. Smart NA, King N, McFarlane JR, Graham PL, Dieberg G. Effect of exercise training on liver function in adults who are overweight or exhibit fatty liver disease: a systematic review and meta-analysis. Br J Sports Med 2018; 52(13): 834-43.
  36. Chaston TB, Dixon J. Factors associated with percent change in visceral versus subcutaneous abdominal fat during weight loss: findings from a systematic review. Int J Obes (Lond) 2008; 32(4): 619-28.
  37. Keating SE, Hackett DA, Parker HM, O’Connor HT, Gerofi JA, Sainsbury A, et al. Effect of aerobic exercise training dose on liver fat and visceral adiposity. J Hepatol 2015; 63(1): 174-82.
  38. Franz MJ, VanWormer JJ, Crain AL, Boucher JL, Histon T, Caplan W, et al. Weight-loss outcomes: a systematic review and meta-analysis of weight-loss clinical trials with a minimum 1-year follow-up. J Am Diet Assoc 2007; 107(10): 1755-67.
  39. Jakobsen MU, Berentzen T, Sørensen T, Overvad K. Abdominal obesity and fatty liver. Epidemiol Rev 2007; 29(1): 77-87.
  40. Verheggen RJH, Maessen MFH, Green DJ, Hermus ARM, Hopman MTE, Thijssen DHT. A systematic review and meta‐analysis on the effects of exercise training versus hypocaloric diet: distinct effects on body weight and visceral adipose tissue. Obes Rev 2016; 17(8): 664-90.
  41. Seppälä-Lindroos A, Vehkavaara S, Häkkinen AM, Goto T, Westerbacka J, Sovijärvi A, et al. Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal men. J Clin Endocrinol Metab 2002; 87(7): 3023-8.
  42. Polyzos SA, Kountouras J, Mantzoros CS. Obesity and nonalcoholic fatty liver disease: From pathophysiology to therapeutics. Metabolism 2019; 92: 82-97.
  43. Ismail I, Keating SE, Baker MK, Johnson NA. A systematic review and meta‐analysis of the effect of aerobic vs. resistance exercise training on visceral fat. Obes Rev 2012; 13(1): 68-91.
  44. Bacchi E, Negri C, Targher G, Faccioli N, Lanza M, Zoppini G, et al. Both resistance training and aerobic training reduce hepatic fat content in type 2 diabetic subjects with nonalcoholic fatty liver disease (the RAED2 Randomized Trial). Hepatology 2013; 58(4): 1287-95.
  45. Khalafi M, Azali Alamdari K, Symonds ME, Rohani H, Sakhaei MH. A comparison of the impact of exercise training with dietary intervention versus dietary intervention alone on insulin resistance and glucose regulation in individual with overweight or obesity: a systemic review and meta-analysis. Crit Rev Food Sci Nutr 2022: 1-15.
  46. Sargeant JA, Gray LJ, Bodicoat DH, Willis SA, Stensel DJ, Nimmo MA, et al. The effect of exercise training on intrahepatic triglyceride and hepatic insulin sensitivity: a systematic review and meta‐ Obes Rev 2018; 19(10): 1446-59.
  47. Marson EC, Delevatti RS, Prado AKG, Netto N, Kruel LFM. Effects of aerobic, resistance, and combined exercise training on insulin resistance markers in overweight or obese children and adolescents: A systematic review and meta-analysis. Prev Med 2016; 93: 211-8.
  48. 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.
  49. Iaccarino G, Franco D, Sorriento D, Strisciuglio T, Barbato E, Morisco C. Modulation of Insulin Sensitivity by Exercise Training: Implications for Cardiovascular Prevention. J Cardiovasc Transl Res 2021; 14(2): 256-70.
  50. Battista F, Ermolao A, van Baak MA, Beaulieu K, Blundell JE, Busetto L, et al. Effect of exercise on cardiometabolic health of adults with overweight or obesity: Focus on blood pressure, insulin resistance, and intrahepatic fat-A systematic review and meta‐ Obes Rev 2021; 22 (Suppl 4): e13269.
  51. Tiikkainen M, Tamminen M, Häkkinen AM, Bergholm R, Vehkavaara S, Halavaara J, et al. Liver‐fat accumulation and insulin resistance in obese women with previous gestational diabetes. Obes Res
    2002; 10(9): 859-67.
  52. Kotronen A, Vehkavaara S, Seppala-Lindroos A, Bergholm R, Yki-Järvinen H. Effect of liver fat on insulin clearance. Am J Physiol Endocrinol Metab 2007; 293(6): E1709-15.
  53. Campbell DT. Experimental and quasi-experimental
    designs for research on teaching. In: Gitomer D, Bell C, editors. Handbook of research on teaching. 5th Washington, DC: American Educational Research Association; 2016. p. 171-246.
  54. Knapp TR. Why is the one-group pretest-posttest design still used? Clin Nurs Res 2016; 25(5): 467-72.
Journal of Isfahan Medical School
Volume 41, Issue 733
1st Week, November
November and December 2023
Pages 751-763

  • Receive Date 21 July 2023
  • Accept Date 11 September 2023