A Meta-Analysis of the Influence on Inflammatory Factors in Type 2 Diabetes among Middle-Aged and Elderly Patients by Various Exercise Modalities
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search Strategy
2.2. Criteria for Inclusion and Exclusion of the Literature
2.3. Study Selection and Data Extraction
2.4. Quality Evaluation
2.5. Analytical Statistics
3. Results
3.1. General Findings of Selected Research Literature
3.2. The General Characteristics of Selected Research Literature
3.3. Quality Assessment of the Selected Literature
3.4. Meta-Analysis of the Effects of Various Exercise Modalities on CRP Levels in MEPT2D
3.5. Meta-Analysis of the Effects of Various Exercise Modalities on TNF-α Levels in MEPT2D
3.6. Meta-Analysis of the Effects of Various Exercise Modalities on IL-6 Levels in MEPT2D
3.7. Meta-Analysis of the Influence on IL-10 Levels in Type 2 Diabetes among Middle-Aged and Older Patients by Various Exercise Modalities
3.8. Publication Bias and Sensitivity Analysis
4. Discussion
5. Current Research Limitations
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Kautzky-Willer, A.; Harreiter, J.; Pacini, G. Sex and Gender Differences in Risk, Pathophysiology and Complications of Type 2 Diabetes Mellitus. Endocr. Rev. 2016, 37, 278–316. [Google Scholar] [CrossRef] [Green Version]
- Böni-Schnetzler, M.; Meier, D.T. Islet inflammation in type 2 diabetes. Semin. Immunopathol. 2019, 41, 501–513. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Berbudi, A.; Rahmadika, N.; Tjahjadi, A.; Ruslami, R. Type 2 Diabetes and its Impact on the Immune System. Curr. Diabetes Rev. 2020, 16, 442–449. [Google Scholar] [CrossRef] [PubMed]
- Huang, D.; Refaat, M.; Mohammedi, K.; Jayyousi, A.; Al Suwaidi, J.; Khalil, C.A. Macrovascular Complications in Patients with Diabetes and Prediabetes. BioMed Res. Int. 2017, 2017, 7839101. [Google Scholar] [CrossRef] [PubMed]
- Perry, B.D.; Caldow, M.K.; Brennan-Speranza, T.C.; Sbaraglia, M.; Jerums, G.; Garnham, A.; Wong, C.; Levinger, P.; Haq, M.A.U.; Hare, D.L.; et al. Muscle atrophy in patients with Type 2 Diabetes Mellitus: Roles of inflammatory pathways, physical activity and exercise. Exerc. Immunol. Rev. 2016, 22, 94–109. [Google Scholar]
- Teixeira-Lemos, E.; Nunes, S.; Teixeira, F.; Reis, F. Regular physical exercise training assists in preventing type 2 diabetes development: Focus on its antioxidant and anti-inflammatory properties. Cardiovasc. Diabetol. 2011, 10, 12. [Google Scholar] [CrossRef] [Green Version]
- de Lemos, E.T.; Oliveira, J.; Pinheiro, J.P.; Reis, F. Regular Physical Exercise as a Strategy to Improve Antioxidant and Anti-Inflammatory Status: Benefits in Type 2 Diabetes Mellitus. Oxidative Med. Cell. Longev. 2012, 2012, 741545. [Google Scholar] [CrossRef]
- Karstoft, K.; Pedersen, B.K. Exercise and type 2 diabetes: Focus on metabolism and inflammation. Immunol. Cell Biol. 2016, 94, 146–150. [Google Scholar] [CrossRef] [PubMed]
- Hopps, E.; Canino, B.; Caimi, G. Effects of exercise on inflammation markers in type 2 diabetic subjects. Acta Diabetol. 2011, 48, 183–189. [Google Scholar] [CrossRef]
- Calle, M.C.; Fernandez, M.L. Effects of resistance training on the inflammatory response. Nutr. Res. Pract. 2010, 4, 259–269. [Google Scholar] [CrossRef] [Green Version]
- DiPenta, J.M.; Green-Johnson, J.M.; Murphy, R.J. Type 2 diabetes mellitus, resistance training, and innate immunity: Is there a common link? Appl. Physiol. Nutr. Metab. 2007, 32, 1025–1035. [Google Scholar] [CrossRef] [PubMed]
- Knudsen, S.H.; Pedersen, B.K. Targeting Inflammation Through a Physical Active Lifestyle and Pharmaceuticals for the Treatment of Type 2 Diabetes. Curr. Diabetes Rep. 2015, 15, 82. [Google Scholar] [CrossRef]
- Melo, L.C.; Dativo-Medeiros, J.; Menezes-Silva, C.E.; Barbosa, F.T.; de Sousa-Rodrigues, C.F.; Rabelo, L.A. Physical Exercise on Inflammatory Markers in Type 2 Diabetes Patients: A Systematic Review of Randomized Controlled Trials. Oxidative Med. Cell. Longev. 2017, 2017, 8523728. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leiva-Valderrama, J.M.; Montes-De-Oca-Garcia, A.; Opazo-Diaz, E.; Ponce-Gonzalez, J.G.; Molina-Torres, G.; Velázquez-Díaz, D.; Galán-Mercant, A. Effects of High-Intensity Interval Training on Inflammatory Biomarkers in Patients with Type 2 Diabetes. A Systematic Review. Int. J. Environ. Res. Public Health 2021, 18, 12644. [Google Scholar] [CrossRef] [PubMed]
- Balducci, S.; Zanuso, S.; Nicolucci, A.; Fernando, F.; Cavallo, S.; Cardelli, P.; Fallucca, S.; Alessi, E.; Letizia, C.; Jimenez, A.; et al. Anti-inflammatory effect of exercise training in subjects with type 2 diabetes and the metabolic syndrome is dependent on exercise modalities and independent of weight loss. Nutr. Metab. Cardiovasc. Dis. 2010, 20, 608–617. [Google Scholar] [CrossRef]
- Okada, S.; Hiuge, A.; Makino, H.; Nagumo, A.; Takaki, H.; Konishi, H.; Goto, Y.; Yoshimasa, Y.; Miyamoto, Y. Effect of Exercise Intervention on Endothelial Function and Incidence of Cardiovascular Disease in Patients with Type 2 Diabetes. J. Atheroscler. Thromb. 2010, 17, 828–833. [Google Scholar] [CrossRef] [Green Version]
- Jorge, M.L.M.P.; de Oliveira, V.N.; Resende, N.M.; Paraiso, L.F.; Calixto, A.; Diniz, A.L.D.; Resende, E.S.; Ropelle, E.R.; Carvalheira, J.B.; Espindola, F.S.; et al. The effects of aerobic, resistance, and combined exercise on metabolic control, inflammatory markers, adipocytokines, and muscle insulin signaling in patients with type 2 diabetes mellitus. Metabolism 2011, 60, 1244–1252. [Google Scholar] [CrossRef]
- Lucotti, P.; Monti, L.D.; Setola, E.; Galluccio, E.; Gatti, R.; Bosi, E.; Piatti, P. Aerobic and resistance training effects compared to aerobic training alone in obese type 2 diabetic patients on diet treatment. Diabetes Res. Clin. Pract. 2011, 94, 395–403. [Google Scholar] [CrossRef]
- El Kader, S.A.; Gari, A.; El-Den, A.S. Impact of moderate versus mild aerobic exercise training on inflammatory cytokines in obese type 2 diabetic patients: A randomized clinical trial. Afr. Health Sci. 2013, 13, 857–863. [Google Scholar] [CrossRef] [Green Version]
- Kadoglou, N.P.E.; Fotiadis, G.; Kapelouzou, A.; Kostakis, A.; Liapis, C.D.; Vrabas, I.S. The differential anti-inflammatory effects of exercise modalities and their association with early carotid atherosclerosis progression in patients with Type 2 diabetes. Diabet. Med. 2013, 30, e41–e50. [Google Scholar] [CrossRef]
- Kim, K.B. Effect of different training mode on Interleukin-6 (IL-6) and C-reactive protein (CRP) in type 2 diabetes mellitus (T2DM) patients. J. Exerc. Nutr. Biochem. 2014, 18, 371–378. [Google Scholar] [CrossRef]
- Mavros, Y.; Kay, S.; Simpson, K.A.; Baker, M.K.; Wang, Y.; Zhao, R.R.; Meiklejohn, J.; Climstein, M.; O’Sullivan, A.J.; De Vos, N.; et al. Reductions in C-reactive protein in older adults with type 2 diabetes are related to improvements in body composition following a randomized controlled trial of resistance training. J. Cachex Sarcopenia Muscle 2014, 5, 111–120. [Google Scholar] [CrossRef]
- El-Kader, S.M.A.; Al-Jiffri, O.H.; Al-Shreef, F.M. Aerobic exercises alleviate symptoms of fatigue related to inflammatory cytokines in obese patients with type 2 diabetes. Afr. Health Sci. 2015, 15, 1142–1148. [Google Scholar] [CrossRef] [Green Version]
- Annibalini, G.; Lucertini, F.; Agostini, D.; Vallorani, L.; Gioacchini, A.; Barbieri, E.; Guescini, M.; Casadei, L.; Passalia, A.; Del Sal, M.; et al. Concurrent Aerobic and Resistance Training Has Anti-Inflammatory Effects and Increases Both Plasma and Leukocyte Levels of IGF-1 in Late Middle-Aged Type 2 Diabetic Patients. Oxidative Med. Cell. Longev. 2017, 2017, 3937842. [Google Scholar] [CrossRef] [PubMed]
- Mallard, A.R.; Hollekim-Strand, S.M.; Coombes, J.S.; Ingul, C.B. Exercise intensity, redox homeostasis and inflammation in type 2 diabetes mellitus. J. Sci. Med. Sport 2017, 20, 893–898. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miller, E.G.; Sethi, P.; Nowson, C.A.; Dunstan, D.W.; Daly, R.M. Effects of progressive resistance training and weight loss versus weight loss alone on inflammatory and endothelial biomarkers in older adults with type 2 diabetes. Eur. J. Appl. Physiol. 2017, 117, 1669–1678. [Google Scholar] [CrossRef]
- Martins, F.M.; de Paula Souza, A.; Nunes, P.R.P.; Michelin, M.A.; Murta, E.F.C.; Resende, E.; de Oliveira, E.P.; Orsatti, F.L. 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. [Google Scholar] [CrossRef]
- Dadrass, A.; Salamat, K.M.; Hamidi, K.; Azizbeigi, K. Anti-inflammatory effects of vitamin D and resistance training in men with type 2 diabetes mellitus and vitamin D deficiency: A randomized, double-blinded, placebo-controlled clinical trial. J. Diabetes Metab. Disord. 2019, 18, 323–331. [Google Scholar] [CrossRef]
- Rech, A.; Botton, C.E.; Lopez, P.; Quincozes-Santos, A.; Umpierre, D.; Pinto, R.S. Effects of short-term resistance training on endothelial function and inflammation markers in elderly patients with type 2 diabetes: A randomized controlled trial. Exp. Gerontol. 2019, 118, 19–25. [Google Scholar] [CrossRef] [PubMed]
- Abd El-Kader, S.M.; Al-Jiffri, O.H.; Neamatallah, Z.A.; AlKhateeb, A.M.; AlFawaz, S.S. Weight reduction ameliorates inflammatory cytokines, adipocytokines and endothelial dysfunction biomarkers among Saudi patients with type 2 diabetes. Afr. Health Sci. 2020, 20, 1329–1336. [Google Scholar] [CrossRef]
- Magalhães, J.P.; Santos, D.A.; Correia, I.R.; Hetherington-Rauth, M.; Ribeiro, R.; Raposo, J.F.; Matos, A.; Bicho, M.D.; Sardinha, L.B. Impact of combined training with different exercise intensities on inflammatory and lipid markers in type 2 diabetes: A secondary analysis from a 1-year randomized controlled trial. Cardiovasc. Diabetol. 2020, 19, 169. [Google Scholar] [CrossRef] [PubMed]
- Su, X.; He, J.; Cui, J.; Li, H.; Men, J. The effects of aerobic exercise combined with resistance training on inflammatory factors and heart rate variability in middle-aged and elderly women with type 2 diabetes mellitus. Ann. Noninvasive Electrocardiol. 2022, 27, e12996. [Google Scholar] [CrossRef] [PubMed]
- Damas, F.; Phillips, S.M.; Libardi, C.A.; Vechin, F.C.; Lixandrão, M.E.; Jannig, P.R.; Costa, L.A.R.; Bacurau, A.V.; Snijders, T.; Parise, G.; et al. Resistance training-induced changes in integrated myofibrillar protein synthesis are related to hypertrophy only after attenuation of muscle damage. J. Physiol. 2016, 594, 5209–5222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Swift, D.L.; Johannsen, N.M.; Earnest, C.P.; Blair, S.N.; Church, T.S. Effect of Exercise Training Modality on C-Reactive Protein in Type 2 Diabetes. Med. Sci. Sports Exerc. 2012, 44, 1028–1034. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pinti, M.V.; Fink, G.K.; Hathaway, Q.A.; Durr, A.J.; Kunovac, A.; Hollander, J.M. Mitochondrial dysfunction in type 2 diabetes mellitus: An organ-based analysis. Am. J. Physiol. Metab. 2019, 316, E268–E285. [Google Scholar] [CrossRef]
- Hall, M.M.; Rajasekaran, S.; Thomsen, T.W.; Peterson, A.R. Lactate: Friend or Foe. PM&R 2016, 8, S8–S15. [Google Scholar] [CrossRef]
- Zembron-Lacny, A.; Tylutka, A.; Zeromska, A.; Kasperska, A.; Wolny-Rokicka, E. Does High Volume of Exercise Training Increase Aseptic Vascular Inflammation in Male Athletes? Am. J. Men Health 2019, 13, 3. [Google Scholar] [CrossRef] [Green Version]
- Schramm, D.-S.T.; Predel, H.-G. Volumen- und Elektrolytstörungen bei Ausdauersport. Internist 2006, 47, 1145–1150. [Google Scholar] [CrossRef]
- Ejensen, J.; Rustad, P.I.; Kolnes, A.J.; Lai, Y.-C. The Role of Skeletal Muscle Glycogen Breakdown for Regulation of Insulin Sensitivity by Exercise. Front. Physiol. 2011, 2, 112. [Google Scholar] [CrossRef] [Green Version]
- de Oliveira Teles, G.; da Silva, C.S.; Rezende, V.R.; Rebelo, A.C.S. Acute Effects of High-Intensity Interval Training on Diabetes Mellitus: A Systematic Review. Int. J. Environ. Res. Public Health 2022, 19, 7049. [Google Scholar] [CrossRef]
- Lehmann, M.J.; Lormes, W.; Opitz-Gress, A.; Steinacker, J.M.; Netzer, N.; Foster, C.; Gastmann, U. Training and overtraining: An overview and experimental results in endurance sports. J. Sports Med. Phys. Fit. 1997, 37, 7–17. [Google Scholar]
- Monteiro, R.; Azevedo, I. Chronic Inflammation in Obesity and the Metabolic Syndrome. Mediat. Inflamm. 2010, 2010, 289645. [Google Scholar] [CrossRef] [PubMed]
- Ouchi, N.; Parker, J.L.; Lugus, J.J.; Walsh, K. Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 2011, 11, 85–97. [Google Scholar] [CrossRef] [PubMed]
NO. | Authors Nation | Year | Age/BMI | Sample Size (Male/Female) | Training Mode | Frequency | Duration | Other Intervention | Outcomes | |
---|---|---|---|---|---|---|---|---|---|---|
Control Group | Intervention Group | Control Intervention Group Group | ||||||||
1 | Balducci S et al. [15] <Italy> | 2009 | 60.6 ± 9.3 (30.9 ± 1.1) | 64.3 ± 8.1 (30.1 ± 1.0) | 22 (14/8) 20 (12/18) | AT, CT | 60 min/session 3 sessions/week | 12 months | Diet control and medication | TNF-α, CRP, IL-6I L-10 |
2 | Okada S et al. [16] <Japan> | 2010 | 64.5 ± 5.9 (24.5 ± 2.9) | 61.9 ± 8.6 (25.7 ± 3.2) | 17 (11/6) 21 (10/11) | RT | 60 min/session 3 sessions/week | 12 weeks | Diet control and medication | CRP |
3 | Jorge ML et al. [17] <Brazil> | 2011 | 53.4 ± 9.8 (29.59 ± 4.9) | 52.1 ± 8.7 (30.42 ± 3.53) | 12 (4/8) 36 (14/22) | AT, RT, CT | 90 min/session 3 sessions/week | 12 months | None | TNF-α, CRP, IL-6 |
4 | Lucotti P et al. [18] <Italy> | 2011 | 58.1 ± 9.9 (38.8 ± 4.5) | 61.5 ± 11.5 (37.5 ± 4.2) | 27 (10/17) 20 (7/13) | AT, CT | 60 min/session 5 sessions/week | 3 weeks | diet control | TNF-α |
5 | Abd El-Kader SM et al. [19] <Saudi Arabia> | 2013 | 44.1 ± 5.9 (33.2 ± 2.8) | 43.6 ± 6.2 (34.5 ± 1.5) | 40 (17/23) 40 (19/21) | AT | 60 min/session 3 sessions/week | 12 weeks | None | TNF-α, IL-6 |
6 | Kadoglou NP et al. [20] <Greece> | 2013 | 57.9 ± 7.2 (32.1 ± 2.95) | 57.4 ± 5.7 (32.24 ± 3.16) | AT:21 (6/15) 24 (7/17) RT:23 (7/16) CT:22 (5/17) | AT, RT, CT | 60 min/session 4 sessions/week | 24 weeks | Metformin etc. | CRP |
7 | Kim KB et al. [21] <Korea> | 2014 | 52.5 ± 1.8 (26.41 ± 2.42) | 51 ± 1.38 (25.92 ± 2.97) | 8 (0/8) AT:8 (0/8) CT:8 (0/8) | AT, CT | 60 min/session 3 sessions/week | 12 weeks | None | CRP, IL-6 |
8 | Mavros Y et al. [22] <Australia> | 2014 | 69.2 ± 6.3 (31.1 ± 4.8) | 67.2 ± 4.9 (31.1 ± 4.8) | 47 (24/23) 41 (22/19) | RT | 60 min/session 3 sessions/week | 12 months | Diet control and medication | CRP |
9 | Abd El-Kader SM et al. [23] <Saudi Arabia> | 2015 | 43.6± 6.2 (31.65 ± 5.53) | 44.1 ± 5.9 (30.87 ± 5.76) | 25 (un) 25 (un) | AT | 60 min/session 3 sessions/week | 12 weeks | None | TNF-α, IL-6 |
10 | Annibalini G et al. [24] <Italy> | 2017 | 60 ± 6.8 (29.0 ± 3.8) | 57 ± 9.1 (28.3 ± 1.5) | 8 (8/0) 8 (8/0) | CT | 90 min/session 3 sessions/week | 16 weeks | Glucose-lowering drugs | TNF-α, CRP, IL-6 |
11 | Mallarda AR et al. [25] < Australia > | 2017 | 54.9 ± 5.3 (29.6 ± 3.6) | 58.6 ± 5.0 (30.2 ± 2.7) | 18 (12/6) 20 (12/8) | HIIT | 70 min/session 3 sessions/week | 12 weeks | None | TNF-α, IL-6, IL-10 |
12 | Miller EG et al. [26] <Australia> | 2017 | 66.9 ± 5.3 (32.5 ± 3.8) | 66.9 ± 5.3 (31.5 ± 10.9) | 18 (8/10) 18 (11/7) | RT | 60 min/session 3 sessions/week | 12 months | None | IL-10 |
13 | Martins FM et al. [27] <Brazil> | 2018 | 65 ± 6.3 (29.2 ± 7.1) | 64.3 ± 6.7 (27.0 ± 6.2) | 8 (0/8) 8 (0/8) | HIIT, CT | 60 min/session 3 sessions/week | 12 weeks | None | CRP, IL-6 |
14 | Dadrass A et al. [28] <Iran> | 2019 | 53.2 ± 8.1 (27.7 ± 3.55) | 53.75 ± 8 (27.94 ± 4.43) | 12 (un) 12 (un) | RT | 60 min/session 3 sessions/week | 12 weeks | VitaminD | TNFα, CRP, IL-6 |
15 | Rech A et al. [29] <Brazil> | 2019 | 68 ± 6.5 (28.3 ± 3.1) | 70.5 ± 7.4 (28.46 ± 3.2) | 21 (10/11) 17 (10/7) | AT, RT | 60 min/session 3 sessions/week | 12 weeks | None | TNF-α, CRP, IL-6I L-10 |
16 | Abd El-Kader SM et al. [30] <Saudi Arabia> | 2020 | 42.2 ± 4.9 (30.58 ± 2.76) | 41.5 ± 5.2 (31.16 ± 2.89) | 50 (32/18) 50 (34/16) | AT | 60 min/session 3 sessions/week | 12 weeks | Diet control | TNF-α, IL-6 |
17 | Magalhães, J.P. et al. [31] <Portugal> | 2020 | 59 ± 8.1 (30.7 ± 5.0) | 58.9 ± 7.5 (31.1 ± 5.0) | 27 (14/13) 13 (9/4) | HIIT | 90 min/session 3 sessions/week | 12 months | Dietary counselling | TNF-α, CRP, IL-6 |
18 | Su X et al. [32] <China> | 2022 | 63.6 ± 2.6 (25.67 ± 0.96) | 64 ± 1.9 (24.9 ± 0.67) | 13 (0/13) 14 (0/14) | CT | 60 min/session 3 sessions/week | 12 weeks | hypoglycemic drugs | TNF-α, CRP, IL-6 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yang, W.; Jiao, H.; Xue, Y.; Wang, L.; Zhang, Y.; Wang, B.; Teng, Z.; Li, J.; Zhao, H.; Liu, C. A Meta-Analysis of the Influence on Inflammatory Factors in Type 2 Diabetes among Middle-Aged and Elderly Patients by Various Exercise Modalities. Int. J. Environ. Res. Public Health 2023, 20, 1783. https://doi.org/10.3390/ijerph20031783
Yang W, Jiao H, Xue Y, Wang L, Zhang Y, Wang B, Teng Z, Li J, Zhao H, Liu C. A Meta-Analysis of the Influence on Inflammatory Factors in Type 2 Diabetes among Middle-Aged and Elderly Patients by Various Exercise Modalities. International Journal of Environmental Research and Public Health. 2023; 20(3):1783. https://doi.org/10.3390/ijerph20031783
Chicago/Turabian StyleYang, Weijun, Haotian Jiao, Yizhang Xue, Lishuo Wang, Ye Zhang, Boqian Wang, Ziyi Teng, Junyan Li, Haotian Zhao, and Chang Liu. 2023. "A Meta-Analysis of the Influence on Inflammatory Factors in Type 2 Diabetes among Middle-Aged and Elderly Patients by Various Exercise Modalities" International Journal of Environmental Research and Public Health 20, no. 3: 1783. https://doi.org/10.3390/ijerph20031783