Efficacy of different exercise type on inflammatory cytokines in individuals with overweight or obesity: a network meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

CHEN Xiaoke , LI Jianyu , CHEN Chaofan ,  CAO Chunmei

Department of Physical Education, Tsinghua University, Beijing 100084, P. R. China;

Corresponding author：

CAO Chunmei, Email: caocm@tsinghua.edu.cn

Keywords：

Overweight; Obesity; Exercise; Inflammation; Systematic review; Network meta-analysis; Randomized controlled trials

DOI：

10.7507/1672-2531.202306137

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To systematically review the efficacy of different exercises on inflammatory cytokines in individuals with overweight or obesity. Methods The CNKI, WanFang Data, VIP, PubMed, EBSCO, Cochrane Library, Web of Science and Embase databases were electronically searched to collect randomized controlled trials (RCTs) on the efficacy of exercise on inflammatory cytokines in individuals with overweight or obesity from January, 2000 to April, 2021. Two reviewers independently screened the literature, extracted data, and assessed the risk of bias of the included studies. The network meta-analysis was then performed using Stata 16.0 software. Results A total of 63 RCTs were included, 49 of which reported the changes in IL-6, 47 of which reported the changes in TNF-α, and 16 of which reported the changes in IL-10. The results of the network meta-analysis found that compared with those in the control group, aerobic exercise (AE) (SMD=−0.9, 95%CI −1.4 to −0.5, P<0.01) and high-intensity interval training (HIIT) (SMD=−1.3, 95%CI −2.3 to −0.3, P=0.011) significantly reduced IL-6. AE (SMD=−1.3, 95%CI −1.7 to −0.9, P<0.01), combined exercise (COM) (SMD=−0.7, 95%CI −1.3 to −0.1, P=0.02), and HIIT (SMD=−1.8, 95%CI −2.6 to −0.9, P<0.01) significantly reduced TNF-α; AE (SMD=0.8, 95%CI 0.1 to 1.5, P=0.03) significantly increased IL-10. The cumulative probability ranking results showed that HIIT was the most effective in reducing IL-6 and TNF-α and increasing IL-10, followed by AE and COM, and resistance training (RT) was the least effective. Conclusion Different exercise types have different effects on improving inflammation in individuals with overweight or obesity. HIIT can be suggested as the best exercise program to improve chronic inflammation in individuals with overweight or obesity. Due to the limited quantity and quality of the included studies, more high-quality studies are needed to verify the above conclusion.

Citation： CHEN Xiaoke, LI Jianyu, CHEN Chaofan, CAO Chunmei. Efficacy of different exercise type on inflammatory cytokines in individuals with overweight or obesity: a network meta-analysis. Chinese Journal of Evidence-Based Medicine, 2024, 24(5): 565-571. doi: 10.7507/1672-2531.202306137 Copy

1.	Hotamisligil GS. Inflammation, metaflammation and immunometabolic disorders. Nature, 2017, 542(7640): 177-185.
2.	Ferrucci L, Fabbri E. Inflammageing: chronic inflammation in ageing, cardiovascular disease, and frailty. Nat Rev Cardiol, 2018, 15(9): 505-522.
3.	Chen X, Sun X, Wang C, et al. Effects of exercise on inflammatory cytokines in patients with type 2 diabetes: a meta-analysis of randomized controlled trials. Oxid Med Cell Longev, 2020, 2020: 6660557.
4.	Saltiel AR, Olefsky JM. Inflammatory mechanisms linking obesity and metabolic disease. J Clin Invest, 2017, 127(1): 1-4.
5.	Morales PE, Bucarey JL, Espinosa A. Muscle lipid metabolism: role of lipid droplets and perilipins. J Diabetes Res, 2017, 2017: 1789395.
6.	Winn NC, Cottam MA, Wasserman DH, et al. Exercise and adipose tissue immunity: outrunning inflammation. Obesity (Silver Spring), 2021, 29(5): 790-801.
7.	Karalis KP, Giannogonas P, Kodela E, et al. Mechanisms of obesity and related pathology: linking immune responses to metabolic stress. FEBS J, 2009, 276(20): 5747-5754.
8.	Walhin JP, Richardson JD, Betts JA, et al. Exercise counteracts the effects of short-term overfeeding and reduced physical activity independent of energy imbalance in healthy young men. J Physiol, 2013, 591(24): 6231-6243.
9.	Zhang G, Yu P, Liu X. Swim training attenuates inflammation and improves insulin sensitivity in mice fed with a high-fat diet. Int J Endocrinol, 2017, 2017: 5940732.
10.	Martins FM, de Paula Souza A, Nunes PRP, et al. High-intensity body weight training is comparable to combined training in changes in muscle mass, physical performance, inflammatory markers and metabolic health in postmenopausal women at high risk for type 2 diabetes mellitus: a randomized controlled clinical trial. Exp Gerontol, 2018, 107: 108-115.
11.	Barry JC, Simtchouk S, Durrer C, et al. Short-term exercise training reduces anti-inflammatory action of interleukin-10 in adults with obesity. Cytokine, 2018, 111: 460-469.
12.	Fedewa MV, Hathaway ED, Higgins S, et al. Moderate, but not vigorous, intensity exercise training reduces C-reactive protein. Acta Cardiol, 2018, 73(3): 283-290.
13.	Gerosa-Neto J, Antunes BM, Campos EZ, et al. Impact of long-term high-intensity interval and moderate-intensity continuous training on subclinical inflammation in overweight/obese adults. J Exerc Rehabil, 2016, 12(6): 575-580.
14.	Vella CA, Taylor K, Drummer D. High-intensity interval and moderate-intensity continuous training elicit similar enjoyment and adherence levels in overweight and obese adults. Eur J Sport Sci, 2017, 17(9): 1203-1211.
15.	Oh S, So R, Shida T, et al. High-intensity aerobic exercise improves both hepatic fat content and stiffness in sedentary obese men with nonalcoholic fatty liver disease. Sci Rep, 2017, 7: 43029.
16.	Chen Y, Yu CY, Deng WM. The role of pro-inflammatory cytokines in lipid metabolism of metabolic diseases. Int Rev Immunol, 2019, 38(6): 249-266.
17.	Sirico F, Bianco A, D'Alicandro G, et al. Effects of physical exercise on adiponectin, leptin, and inflammatory markers in childhood obesity: systematic review and meta-analysis. Child Obes, 2018, 14(4): 207-217.
18.	Wang S, Zhou H, Zhao C, et al. Effect of exercise training on body composition and inflammatory cytokine levels in overweight and obese individuals: a systematic review and network meta-analysis. Front Immunol, 2022, 13: 921085.
19.	Lee J. Influences of exercise interventions on overweight and obesity in children and adolescents. Public Health Nurs, 2021, 38(3): 502-516.
20.	Gleeson M, Bishop NC, Stensel DJ, et al. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol, 2011, 11(9): 607-615.
21.	Jiang N, Li Y, Shu T, et al. Cytokines and inflammation in adipogenesis: an updated review. Front Med, 2019, 13(3): 314-329.
22.	Higgins JP, Altman DG, Gøtzsche PC, et al. The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ, 2011, 343: d5928.
23.	Higgins JTJ, Chandler J, Cumpston M, et al. Cochrane handbook for systematic reviews of interventions. Cochrane, 2022.
24.	Hutton B, Salanti G, Caldwell DM, et al. The PRISMA extension statement for reporting of systematic reviews incorporating network meta-analyses of health care interventions: checklist and explanations. Ann Intern Med, 2015, 162(11): 777-784.
25.	Salanti G. Indirect and mixed-treatment comparison, network, or multiple-treatments meta-analysis: many names, many benefits, many concerns for the next generation evidence synthesis tool. Res Synth Methods, 2012, 3(2): 80-97.
26.	Chaimani A, Higgins JP, Mavridis D, et al. Graphical tools for network meta-analysis in STATA. PLoS One, 2013, 8(10): e76654.
27.	Shim S, Yoon BH, Shin IS, et al. Network meta-analysis: application and practice using Stata. Epidemiol Health, 2017, 39: e2017047.
28.	Salanti G, Ades AE, Ioannidis JP. Graphical methods and numerical summaries for presenting results from multiple-treatment meta-analysis: an overview and tutorial. J Clin Epidemiol, 2011, 64(2): 163-171.
29.	Mbuagbaw L, Rochwerg B, Jaeschke R, et al. Approaches to interpreting and choosing the best treatments in network meta-analyses. Syst Rev, 2017, 6(1): 79.
30.	Cipriani A, Furukawa TA, Salanti G, et al. Comparative efficacy and acceptability of 21 antidepressant drugs for the acute treatment of adults with major depressive disorder: a systematic review and network meta-analysis. Lancet, 2018, 391(10128): 1357-1366.
31.	Wolf J, Rose-John S, Garbers C. Interleukin-6 and its receptors: a highly regulated and dynamic system. Cytokine, 2014, 70(1): 11-20.
32.	Hummasti S, Hotamisligil GS. Endoplasmic reticulum stress and inflammation in obesity and diabetes. Circ Res, 2010, 107(5): 579-591.
33.	Han Y, Liu Y, Zhao Z, et al. Does physical activity-based intervention improve systemic proinflammatory cytokine levels in overweight or obese children and adolescents. Insights from a meta-analysis of randomized control trials. Obes Facts, 2019, 12(6): 653-668.
34.	丁玲, 张森, 姜星, 等. 运动干预对肥胖机体体内瘦素等脂肪细胞因子作用的影响. 生理科学进展, 2023, 54(2): 141-147.
35.	Deng T, Lyon CJ, Bergin S, et al. Obesity, inflammation, and cancer. Annu Rev Pathol, 2016, 11: 421-449.
36.	Virdis A, Colucci R, Bernardini N, et al. Microvascular endothelial dysfunction in human obesity: role of TNF-α. J Clin Endocrinol Metab, 2019, 104(2): 341-348.
37.	Moore KW, de Waal Malefyt R, Coffman RL, et al. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol, 2001, 19: 683-765.
38.	Hong EG, Ko HJ, Cho YR, et al. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes, 2009, 58(11): 2525-2535.
39.	Hatano D, Ogasawara J, Endoh S, et al. Effect of exercise training on the density of endothelial cells in the white adipose tissue of rats. Scand J Med Sci Sports, 2011, 21(6): e115-e121.
40.	Disanzo BL, You T. Effects of exercise training on indicators of adipose tissue angiogenesis and hypoxia in obese rats. Metabolism, 2014, 63(4): 452-455.
41.	Bevilacqua MP, Nelson RM, Mannori G, et al. Endothelial-leukocyte adhesion molecules in human disease. Annu Rev Med, 1994, 45: 361-378.
42.	Chen X, Sun X, Gao D, et al. A meta-analysis of the effects of aerobic exercise on the basal level of endothelial progenitor cells in middle-aged and older adults. J Aging Phys Act, 2021, 30(4): 610-618.
43.	Di Francescomarino S, Sciartilli A, Di Valerio V, et al. The effect of physical exercise on endothelial function. Sports Med, 2009, 39(10): 797-812.
44.	You T, Arsenis NC, Disanzo BL, et al. Effects of exercise training on chronic inflammation in obesity : current evidence and potential mechanisms. Sports Med, 2013, 43(4): 243-256.
45.	Timmerman KL, Flynn MG, Coen PM, et al. Exercise training-induced lowering of inflammatory (CD14+CD16+) monocytes: a role in the anti-inflammatory influence of exercise. J Leukoc Biol, 2008, 84(5): 1271-1278.
46.	Rosa-Neto JC, Lira FS, Little JP, et al. Immunometabolism-fit: how exercise and training can modify T cell and macrophage metabolism in health and disease. Exerc Immunol Rev, 2022, 28: 29-46.
47.	Steensberg A, Fischer CP, Keller C, et al. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab, 2003, 285(2): E433-E437.

1. Hotamisligil GS. Inflammation, metaflammation and immunometabolic disorders. Nature, 2017, 542(7640): 177-185.
2. Ferrucci L, Fabbri E. Inflammageing: chronic inflammation in ageing, cardiovascular disease, and frailty. Nat Rev Cardiol, 2018, 15(9): 505-522.
3. Chen X, Sun X, Wang C, et al. Effects of exercise on inflammatory cytokines in patients with type 2 diabetes: a meta-analysis of randomized controlled trials. Oxid Med Cell Longev, 2020, 2020: 6660557.
4. Saltiel AR, Olefsky JM. Inflammatory mechanisms linking obesity and metabolic disease. J Clin Invest, 2017, 127(1): 1-4.
5. Morales PE, Bucarey JL, Espinosa A. Muscle lipid metabolism: role of lipid droplets and perilipins. J Diabetes Res, 2017, 2017: 1789395.
6. Winn NC, Cottam MA, Wasserman DH, et al. Exercise and adipose tissue immunity: outrunning inflammation. Obesity (Silver Spring), 2021, 29(5): 790-801.
7. Karalis KP, Giannogonas P, Kodela E, et al. Mechanisms of obesity and related pathology: linking immune responses to metabolic stress. FEBS J, 2009, 276(20): 5747-5754.
8. Walhin JP, Richardson JD, Betts JA, et al. Exercise counteracts the effects of short-term overfeeding and reduced physical activity independent of energy imbalance in healthy young men. J Physiol, 2013, 591(24): 6231-6243.
9. Zhang G, Yu P, Liu X. Swim training attenuates inflammation and improves insulin sensitivity in mice fed with a high-fat diet. Int J Endocrinol, 2017, 2017: 5940732.
10. Martins FM, de Paula Souza A, Nunes PRP, et al. High-intensity body weight training is comparable to combined training in changes in muscle mass, physical performance, inflammatory markers and metabolic health in postmenopausal women at high risk for type 2 diabetes mellitus: a randomized controlled clinical trial. Exp Gerontol, 2018, 107: 108-115.
11. Barry JC, Simtchouk S, Durrer C, et al. Short-term exercise training reduces anti-inflammatory action of interleukin-10 in adults with obesity. Cytokine, 2018, 111: 460-469.
12. Fedewa MV, Hathaway ED, Higgins S, et al. Moderate, but not vigorous, intensity exercise training reduces C-reactive protein. Acta Cardiol, 2018, 73(3): 283-290.
13. Gerosa-Neto J, Antunes BM, Campos EZ, et al. Impact of long-term high-intensity interval and moderate-intensity continuous training on subclinical inflammation in overweight/obese adults. J Exerc Rehabil, 2016, 12(6): 575-580.
14. Vella CA, Taylor K, Drummer D. High-intensity interval and moderate-intensity continuous training elicit similar enjoyment and adherence levels in overweight and obese adults. Eur J Sport Sci, 2017, 17(9): 1203-1211.
15. Oh S, So R, Shida T, et al. High-intensity aerobic exercise improves both hepatic fat content and stiffness in sedentary obese men with nonalcoholic fatty liver disease. Sci Rep, 2017, 7: 43029.
16. Chen Y, Yu CY, Deng WM. The role of pro-inflammatory cytokines in lipid metabolism of metabolic diseases. Int Rev Immunol, 2019, 38(6): 249-266.
17. Sirico F, Bianco A, D'Alicandro G, et al. Effects of physical exercise on adiponectin, leptin, and inflammatory markers in childhood obesity: systematic review and meta-analysis. Child Obes, 2018, 14(4): 207-217.
18. Wang S, Zhou H, Zhao C, et al. Effect of exercise training on body composition and inflammatory cytokine levels in overweight and obese individuals: a systematic review and network meta-analysis. Front Immunol, 2022, 13: 921085.
19. Lee J. Influences of exercise interventions on overweight and obesity in children and adolescents. Public Health Nurs, 2021, 38(3): 502-516.
20. Gleeson M, Bishop NC, Stensel DJ, et al. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol, 2011, 11(9): 607-615.
21. Jiang N, Li Y, Shu T, et al. Cytokines and inflammation in adipogenesis: an updated review. Front Med, 2019, 13(3): 314-329.
22. Higgins JP, Altman DG, Gøtzsche PC, et al. The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ, 2011, 343: d5928.
23. Higgins JTJ, Chandler J, Cumpston M, et al. Cochrane handbook for systematic reviews of interventions. Cochrane, 2022.
24. Hutton B, Salanti G, Caldwell DM, et al. The PRISMA extension statement for reporting of systematic reviews incorporating network meta-analyses of health care interventions: checklist and explanations. Ann Intern Med, 2015, 162(11): 777-784.
25. Salanti G. Indirect and mixed-treatment comparison, network, or multiple-treatments meta-analysis: many names, many benefits, many concerns for the next generation evidence synthesis tool. Res Synth Methods, 2012, 3(2): 80-97.
26. Chaimani A, Higgins JP, Mavridis D, et al. Graphical tools for network meta-analysis in STATA. PLoS One, 2013, 8(10): e76654.
27. Shim S, Yoon BH, Shin IS, et al. Network meta-analysis: application and practice using Stata. Epidemiol Health, 2017, 39: e2017047.
28. Salanti G, Ades AE, Ioannidis JP. Graphical methods and numerical summaries for presenting results from multiple-treatment meta-analysis: an overview and tutorial. J Clin Epidemiol, 2011, 64(2): 163-171.
29. Mbuagbaw L, Rochwerg B, Jaeschke R, et al. Approaches to interpreting and choosing the best treatments in network meta-analyses. Syst Rev, 2017, 6(1): 79.
30. Cipriani A, Furukawa TA, Salanti G, et al. Comparative efficacy and acceptability of 21 antidepressant drugs for the acute treatment of adults with major depressive disorder: a systematic review and network meta-analysis. Lancet, 2018, 391(10128): 1357-1366.
31. Wolf J, Rose-John S, Garbers C. Interleukin-6 and its receptors: a highly regulated and dynamic system. Cytokine, 2014, 70(1): 11-20.
32. Hummasti S, Hotamisligil GS. Endoplasmic reticulum stress and inflammation in obesity and diabetes. Circ Res, 2010, 107(5): 579-591.
33. Han Y, Liu Y, Zhao Z, et al. Does physical activity-based intervention improve systemic proinflammatory cytokine levels in overweight or obese children and adolescents. Insights from a meta-analysis of randomized control trials. Obes Facts, 2019, 12(6): 653-668.
34. 丁玲, 张森, 姜星, 等. 运动干预对肥胖机体体内瘦素等脂肪细胞因子作用的影响. 生理科学进展, 2023, 54(2): 141-147.
35. Deng T, Lyon CJ, Bergin S, et al. Obesity, inflammation, and cancer. Annu Rev Pathol, 2016, 11: 421-449.
36. Virdis A, Colucci R, Bernardini N, et al. Microvascular endothelial dysfunction in human obesity: role of TNF-α. J Clin Endocrinol Metab, 2019, 104(2): 341-348.
37. Moore KW, de Waal Malefyt R, Coffman RL, et al. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol, 2001, 19: 683-765.
38. Hong EG, Ko HJ, Cho YR, et al. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes, 2009, 58(11): 2525-2535.
39. Hatano D, Ogasawara J, Endoh S, et al. Effect of exercise training on the density of endothelial cells in the white adipose tissue of rats. Scand J Med Sci Sports, 2011, 21(6): e115-e121.
40. Disanzo BL, You T. Effects of exercise training on indicators of adipose tissue angiogenesis and hypoxia in obese rats. Metabolism, 2014, 63(4): 452-455.
41. Bevilacqua MP, Nelson RM, Mannori G, et al. Endothelial-leukocyte adhesion molecules in human disease. Annu Rev Med, 1994, 45: 361-378.
42. Chen X, Sun X, Gao D, et al. A meta-analysis of the effects of aerobic exercise on the basal level of endothelial progenitor cells in middle-aged and older adults. J Aging Phys Act, 2021, 30(4): 610-618.
43. Di Francescomarino S, Sciartilli A, Di Valerio V, et al. The effect of physical exercise on endothelial function. Sports Med, 2009, 39(10): 797-812.
44. You T, Arsenis NC, Disanzo BL, et al. Effects of exercise training on chronic inflammation in obesity : current evidence and potential mechanisms. Sports Med, 2013, 43(4): 243-256.
45. Timmerman KL, Flynn MG, Coen PM, et al. Exercise training-induced lowering of inflammatory (CD14+CD16+) monocytes: a role in the anti-inflammatory influence of exercise. J Leukoc Biol, 2008, 84(5): 1271-1278.
46. Rosa-Neto JC, Lira FS, Little JP, et al. Immunometabolism-fit: how exercise and training can modify T cell and macrophage metabolism in health and disease. Exerc Immunol Rev, 2022, 28: 29-46.
47. Steensberg A, Fischer CP, Keller C, et al. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab, 2003, 285(2): E433-E437.

Previous Article
Efficacy of intensive care unit diaries on patients and relatives: a meta-analysis
Next Article
Permanent neonatal diabetes mellitus case reports: a systematic review

Chinese Journal of Evidence-Based Medicine

Efficacy of different exercise type on inflammatory cytokines in individuals with overweight or obesity: a network meta-analysis

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content