Skip to main content

Advertisement

Log in

Comparative efficacy of exercise training processes in improving nonalcoholic fatty liver disease: a systematic review and meta-analysis

  • Review Article
  • Published:
Irish Journal of Medical Science (1971 -) Aims and scope Submit manuscript

Abstract

Objectives

This systematic review and meta-analysis aimed to evaluate the efficacy of exercise training in patients with nonalcoholic fatty liver disease (NAFLD).

Methods

We searched PubMed, Cochrane Library, Web of Science, and Embase for relevant research from January 2001 to December 2021. The efficacy of exercise training was analyzed.

Results

A total of 21 articles, involving 1733 patients, were included. Exercise training, including resistance training, aerobic exercise training, and high-intensity training, showed the efficacy in reducing weight (MD = 3.46, 95% CI [1.94, 4.98]), BMI (MD = 0.89, 95% CI [0.17, 1.61]), and ALT (MD = 6.66, 95% CI [3.27, 10.04]) and AST (MD = 3.14, 95% CI [0.35, 5.93]) levels in patients with NAFLD. When the exercise training lasted for ≥ 20 weeks, the total cholesterol (TC) (MD = 0.13, 95% CI [0.04, 0.22]), triglyceride (TG) (MD = 0.29, 95% CI [0.12, 0.47]), and blood glucose (GLU) (MD =  − 0.18, 95% CI [0.10, 0.26]) levels significantly reduced. Compared with the exercise training group, the exercise training combined with probiotics group showed more efficiency in reducing the ALT, AST, TG, and TC levels. However, the exercise training combined with a hypoglycemic agent group showed no obvious efficiency compared with the exercise training group.

Conclusion

Exercise training can improve NAFLD. The improvement was more obvious when exercise was performed for ≥ 20 weeks. Probiotics may enhance the efficiency of exercise training.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Kessoku T, Imajo K, Kobayashi T et al (2020) Lubiprostone in patients with non-alcoholic fatty liver disease: a randomised, double-blind, placebo-controlled, phase 2a trial. The lancet Gastroenterology & hepatology 5(11):996–1007. https://doi.org/10.1016/s2468-1253(20)30216-8

    Article  Google Scholar 

  2. Cai J, Zhang XJ, Ji YX et al (2020) Nonalcoholic fatty liver disease pandemic fuels the upsurge in cardiovascular diseases. Circ Res 126(5):679–704. https://doi.org/10.1161/CIRCRESAHA.119.316337

    Article  CAS  Google Scholar 

  3. Hariri M, Gholami A, Mirhafez SR et al (2020) A pilot study of the effect of curcumin on epigenetic changes and DNA damage among patients with non-alcoholic fatty liver disease: a randomized, double-blind, placebo-controlled, clinical trial. Complement Ther Med. https://doi.org/10.1016/j.ctim.2020.102447

    Article  Google Scholar 

  4. Yao J, Meng M, Yang S et al (2018) Effect of aerobic and resistance exercise on liver enzyme and blood lipids in Chinese patients with nonalcoholic fatty liver disease: a randomized controlled trial. Int J Clin Exp Med 11(5):4867–4874

    Google Scholar 

  5. Wong VW, Wong GL, Chan RS et al (2018) Beneficial effects of lifestyle intervention in non-obese patients with non-alcoholic fatty liver disease. J Hepatol 69(6):1349–1356. https://doi.org/10.1016/j.jhep.2018.08.011

    Article  Google Scholar 

  6. Takahashi A, Abe K, Fujita M et al (2020) Simple resistance exercise decreases cytokeratin 18 and fibroblast growth factor 21 levels in patients with nonalcoholic fatty liver disease: a retrospective clinical study. Medicine (Baltimore) 99(22):e20399. https://doi.org/10.1097/md.0000000000020399

    Article  CAS  Google Scholar 

  7. Sáez-Lara MJ, Robles-Sanchez C, Ruiz-Ojeda FJ et al (2016) Effects of probiotics and synbiotics on obesity, insulin resistance syndrome, type 2 diabetes and non-alcoholic fatty liver disease: a review of human clinical trials. Int J Mol Sci 17(6). https://doi.org/10.3390/ijms17060928

  8. Lavine JE, Schwimmer JB, Van Natta ML et al (2011) Effect of vitamin E or metformin for treatment of nonalcoholic fatty liver disease in children and adolescents: the TONIC randomized controlled trial. JAMA 305(16):1659–1668. https://doi.org/10.1001/jama.2011.520

    Article  CAS  Google Scholar 

  9. Moher D, Shamseer L, Clarke M et al (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. https://doi.org/10.1186/2046-4053-4-1

    Article  Google Scholar 

  10. Cai GS, Su H, Zhang J (2020) Protective effect of probiotics in patients with non-alcoholic fatty liver disease. Medicine (Baltimore) 99(32):e21464. https://doi.org/10.1097/md.0000000000021464

    Article  CAS  Google Scholar 

  11. Khoo J, Hsiang JC, Taneja R et al (2019) Randomized trial comparing effects of weight loss by liraglutide with lifestyle modification in non-alcoholic fatty liver disease. Liver Int 39(5):941–949. https://doi.org/10.1111/liv.14065

    Article  CAS  Google Scholar 

  12. Duseja A, Acharya SK, Mehta M et al (2019) High potency multistrain probiotic improves liver histology in non-alcoholic fatty liver disease (NAFLD): a randomised, double-blind, proof of concept study. BMJ open gastroenterology 6(1). https://doi.org/10.1136/bmjgast-2019-000315

  13. Banitalebi E, Faramarzi M, Nasiri S et al (2019) Effects of different exercise modalities on novel hepatic steatosis indices in overweight women with type 2 diabetes. Clin Mol Hepatol 25(3):294–304. https://doi.org/10.3350/cmh.2018.0086

    Article  Google Scholar 

  14. Abdelbasset WK, Tantawy SA, Kamel DM et al (2019) A randomized controlled trial on the effectiveness of 8-week high-intensity interval exercise on intrahepatic triglycerides, visceral lipids, and health-related quality of life in diabetic obese patients with nonalcoholic fatty liver disease. Medicine (Baltimore) 98(12):e14918. https://doi.org/10.1097/md.0000000000014918

    Article  CAS  Google Scholar 

  15. Bakhshimoghaddam F, Shateri K, Sina M et al (2018) Daily consumption of synbiotic yogurt decreases liver steatosis in patients with nonalcoholic fatty liver disease: a randomized controlled clinical trial. J Nutr 148(8):1276–1284. https://doi.org/10.1093/jn/nxy088

    Article  Google Scholar 

  16. Zhang HJ, Pan LL, Ma ZM et al (2017) Long-term effect of exercise on improving fatty liver and cardiovascular risk factors in obese adults: a 1-year follow-up study. Diabetes Obes Metab 19(2):284–289. https://doi.org/10.1111/dom.12809

    Article  Google Scholar 

  17. Takahashi A, Imaizumi H, Hayashi M et al (2017) Simple resistance exercise for 24 weeks decreases alanine aminotransferase levels in patients with non-alcoholic fatty liver disease. Sports medicine international open 1(1):E2-e7. https://doi.org/10.1055/s-0042-117875

    Article  Google Scholar 

  18. Rezende RE, Duarte SM, Stefano JT et al (2016) Randomized clinical trial: benefits of aerobic physical activity for 24 weeks in postmenopausal women with nonalcoholic fatty liver disease. Menopause (New York, NY) 23(8):876–883. https://doi.org/10.1097/gme.0000000000000647

    Article  Google Scholar 

  19. Takahashi A, Abe K, Usami K et al (2015) Simple Resistance Exercise helps Patients with Non-alcoholic Fatty Liver Disease. International journal of sports medicine 36(10): 848-852. https://doi.org/10.1055/s-0035-1549853

  20. Shamsoddini A, Sobhani V, Ghamar Chehreh ME et al (2015) Effect of aerobic and resistance exercise training on liver enzymes and hepatic fat in iranian men with nonalcoholic fatty liver disease. Hepat Mon 15(10):e31434. https://doi.org/10.5812/hepatmon.31434

    Article  Google Scholar 

  21. Hallsworth K, Thoma C, Hollingsworth KG et al (2015) Modified high-intensity interval training reduces liver fat and improves cardiac function in non-alcoholic fatty liver disease: a randomized controlled trial. Clinical science (London, England : 1979) 129(12): 1097–1105. https://doi.org/10.1042/cs20150308

  22. Pugh CJ, Spring VS, Kemp GJ et al (2014) Exercise training reverses endothelial dysfunction in nonalcoholic fatty liver disease. Am J Physiol Heart Circ Physiol 307(9):H1298-1306. https://doi.org/10.1152/ajpheart.00306.2014

    Article  CAS  Google Scholar 

  23. Pugh CJ, Cuthbertson DJ, Sprung VS et al (2013) Exercise training improves cutaneous microvascular function in nonalcoholic fatty liver disease. Am J Physiol Endocrinol Metab 305(1):E50-58. https://doi.org/10.1152/ajpendo.00055.2013

    Article  CAS  Google Scholar 

  24. Al-Jiffri O, Al-Sharif FM, Abd El-Kader SM et al (2013) Weight reduction improves markers of hepatic function and insulin resistance in type-2 diabetic patients with non-alcoholic fatty liver. Afr Health Sci 13(3):667–672. https://doi.org/10.4314/ahs.v13i3.21

    Article  CAS  Google Scholar 

  25. Sullivan S, Kirk EP, Mittendorfer B et al (2012) Randomized trial of exercise effect on intrahepatic triglyceride content and lipid kinetics in nonalcoholic fatty liver disease. Hepatology 55(6):1738–1745. https://doi.org/10.1002/hep.25548

    Article  CAS  Google Scholar 

  26. Bozzetto L, Prinster A, Annuzzi G et al (2012) Liver fat is reduced by an isoenergetic MUFA diet in a controlled randomized study in type 2 diabetic patients. Diabetes Care 35(7):1429–1435. https://doi.org/10.2337/dc12-0033

    Article  CAS  Google Scholar 

  27. Chen S-M, Liu C-Y, Li S-R et al (2008) Effects of therapeutic lifestyle program on ultrasound-diagnosed nonalcoholic fatty liver disease. J Chin Med Assoc 71(11):551–558. https://doi.org/10.1016/s1726-4901(08)70168-0

    Article  CAS  Google Scholar 

  28. Jia GY, Han T, Gao L et al (2018) Effect of aerobic exercise and resistance exercise in improving non-alcoholic fatty liver disease: a randomized controlled trial. Zhonghua gan zang bing za zhi [Chinese journal of hepatology] 26(1):34–41. https://doi.org/10.3760/cma.j.issn.1007-3418.2018.01.009

    Article  CAS  Google Scholar 

  29. Whitsett M, VanWagner LB (2015) Physical activity as a treatment of non-alcoholic fatty liver disease: a systematic review. World J Hepatol 7(16):2041–2052. https://doi.org/10.4254/wjh.v7.i16.2041

    Article  Google Scholar 

  30. Lule KO, Akarsu E, Sayiner ZA et al (2022) The effects of metformin, pioglitazone, exenatide and exercise on fatty liver in obese diabetic rats: the role of IRS-1 and SOCS-3 molecules. Inflammopharmacology. https://doi.org/10.1007/s10787-021-00916-6

    Article  Google Scholar 

  31. Yu Y, Yu L, Cheng N et al (2021) Exercise alleviates the apolipoprotein A5-toll-like receptor 4 axis impairment in mice with high-fat diet-induced non-alcoholic steatohepatitis. Front Physiol. https://doi.org/10.3389/fphys.2021.783341

    Article  Google Scholar 

  32. Charatcharoenwitthaya P, Kuljiratitikal K, Aksornchanya O et al (2021) Moderate-intensity aerobic vs resistance exercise and dietary modification in patients with nonalcoholic fatty liver disease: a randomized clinical trial. Clinical and translational gastroenterology 12(3): e00316. https://doi.org/10.14309/ctg.0000000000000316

  33. Iwanaga S, Hashida R, Takano Y et al (2020) Hybrid training system improves insulin resistance in patients with nonalcoholic fatty liver disease: a randomized controlled pilot study. Tohoku J Exp Med 252(1):23–32. https://doi.org/10.1620/tjem.252.23

    Article  CAS  Google Scholar 

  34. Gomes Anunciação P, Doederlein Polito M (2011) A review on post-exercise hypotension in hypertensive individuals. Arq Bras Cardiol 96(5):e100-109

    Google Scholar 

  35. Boutcher YN, Boutcher SH (2017) Exercise intensity and hypertension: what’s new? J Hum Hypertens 31(3):157–164. https://doi.org/10.1038/jhh.2016.62

    Article  CAS  Google Scholar 

  36. Kelley GA, Kelley KS (2008) Efficacy of aerobic exercise on coronary heart disease risk factors. Prev Cardiol 11(2):71–75. https://doi.org/10.1111/j.1751-7141.2008.08037.x

    Article  CAS  Google Scholar 

  37. Boutcher SH (2011) High-intensity intermittent exercise and fat loss. Journal of obesity. https://doi.org/10.1155/2011/868305

    Article  Google Scholar 

  38. Trapp EG, Chisholm DJ, Freund J et al (2005) (2008) The effects of high-intensity intermittent exercise training on fat loss and fasting insulin levels of young women. Int J Obes 32(4):684–691. https://doi.org/10.1038/sj.ijo.0803781

    Article  CAS  Google Scholar 

  39. Hashida R, Kawaguchi T, Bekki M et al (2017) Aerobic vs. resistance exercise in non-alcoholic fatty liver disease: a systematic review. J Hepatol 66(1): 142–152. https://doi.org/10.1016/j.jhep.2016.08.023

  40. Wang Y, Li N, Yang JJ et al (2020) Probiotics and fructo-oligosaccharide intervention modulate the microbiota-gut brain axis to improve autism spectrum reducing also the hyper-serotonergic state and the dopamine metabolism disorder. Pharmacol Res. https://doi.org/10.1016/j.phrs.2020.104784

    Article  Google Scholar 

  41. Liu M, Ding J, Zhang H et al (2020) Lactobacillus casei LH23 modulates the immune response and ameliorates DSS-induced colitis via suppressing JNK/p-38 signal pathways and enhancing histone H3K9 acetylation. Food Funct. https://doi.org/10.1039/d0fo00546k

    Article  Google Scholar 

  42. Jang HR, Park HJ, Kang D et al (2019) A protective mechanism of probiotic Lactobacillus against hepatic steatosis via reducing host intestinal fatty acid absorption. Exp Mol Med 51(8):1–14. https://doi.org/10.1038/s12276-019-0293-4

    Article  CAS  Google Scholar 

  43. Scorletti E, Afolabi PR, Miles EA et al (2020) Synbiotics alter fecal microbiomes, but not liver fat or fibrosis, in a randomized trial of patients with nonalcoholic fatty liver disease. Gastroenterology 158(6):1597-1610.e1597. https://doi.org/10.1053/j.gastro.2020.01.031

    Article  CAS  Google Scholar 

  44. Loomba R, Ling L, Dinh DM et al (2021) The commensal microbe veillonella as a marker for response to an FGF19 analog in NASH. Hepatology 73(1):126–143. https://doi.org/10.1002/hep.31523

    Article  CAS  Google Scholar 

  45. Eguchi Y, Kitajima Y, Hyogo H et al (2015) Pilot study of liraglutide effects in non-alcoholic steatohepatitis and non-alcoholic fatty liver disease with glucose intolerance in Japanese patients (LEAN-J). Hepatol Res 45(3):269–278. https://doi.org/10.1111/hepr.12351

    Article  CAS  Google Scholar 

  46. Armstrong MJ, Hull D, Guo K et al (2016) Glucagon-like peptide 1 decreases lipotoxicity in non-alcoholic steatohepatitis. J Hepatol 64(2):399–408. https://doi.org/10.1016/j.jhep.2015.08.038

    Article  CAS  Google Scholar 

  47. Bhat A, Sebastiani G, Bhat M (2015) Systematic review: preventive and therapeutic applications of metformin in liver disease. World J Hepatol 7(12):1652–1659. https://doi.org/10.4254/wjh.v7.i12.1652

    Article  Google Scholar 

Download references

Funding

This article was supported by Qingdao Science and Technology Benefit People Demonstration and Guidance Project (21–43-02–0016). Qingdao Science and Technology Benefit People Demonstration and Guidance Project,21–43-02–0016.

Author information

Authors and Affiliations

Authors

Contributions

X.Y and Y.W conduct preliminary search, extract information, calculate information, and write the paper. J.L revises the paper. W.H designs the experiment. J.D approves the final version.

Corresponding author

Correspondence to Jianping Duan.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, X., Wang, Y., Lai, J. et al. Comparative efficacy of exercise training processes in improving nonalcoholic fatty liver disease: a systematic review and meta-analysis. Ir J Med Sci 192, 131–142 (2023). https://doi.org/10.1007/s11845-022-02988-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11845-022-02988-x

Keywords

Navigation