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Effectiveness of Resistance Exercise on Inflammatory Biomarkers in Patients with Type 2 Diabetes Mellitus: A Systematic Review with Meta-Analysis
Rubén Fernández-Rodríguez, Sonia Monedero-Carrasco, Bruno Bizzozero-Peroni, Miriam Garrido-Miguel, Arthur Eumann Mesas, Vicente Martínez-Vizcaíno
Diabetes Metab J. 2023;47(1):118-134.   Published online April 29, 2022
DOI: https://doi.org/10.4093/dmj.2022.0007
  • 10,390 View
  • 321 Download
  • 11 Web of Science
  • 11 Crossref
AbstractAbstract PDFSupplementary MaterialPubReader   ePub   
Background
Type 2 diabetes mellitus (T2DM) is related to increased inflammatory processes. The effects of resistance exercise on inflammatory biomarkers in T2DM are controversial. Our purpose was to determine the effectiveness of resistance exercise on inflammatory biomarkers in patients diagnosed with T2DM.
Methods
We searched four databases until September 2021. We included randomized clinical trials (RCTs) of the effects of resistance exercise on inflammatory biomarkers (C-reactive protein [CRP], tumor necrosis factor alpha, interleukin-6, and interleukin-10) in patients with T2DM. A random effects meta-analysis was conducted to determine the standardized mean difference (SMD) and the raw mean difference (MD) for CRP.
Results
Thirteen RCTs were included in the review, and 11 in the meta-analysis for CRP. Lower CRP levels were observed when resistance exercise was compared with the control groups (SMD=–0.20; 95% confidence interval [CI], –0.37 to –0.02). When conducting the MD meta-analysis, resistance exercise showed a significant decrease in CRP of –0.59 mg/dL (95% CI, –0.88 to –0.30); otherwise, in the control groups, the CRP values increased 0.19 mg/dL (95% CI, 0.17 to 0.21).
Conclusion
Evidence supports resistance exercise as an effective strategy to manage systemic inflammation by decreasing CRP levels in patients with T2DM. The evidence is still inconclusive for other inflammatory biomarkers.

Citations

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Review
Obesity and Metabolic Syndrome
The Effect of Regular Exercise on Insulin Sensitivity in Type 2 Diabetes Mellitus: A Systematic Review and Meta-Analysis
Kimberley L. Way, Daniel A. Hackett, Michael K. Baker, Nathan A. Johnson
Diabetes Metab J. 2016;40(4):253-271.   Published online August 2, 2016
DOI: https://doi.org/10.4093/dmj.2016.40.4.253
  • 11,130 View
  • 239 Download
  • 113 Web of Science
  • 110 Crossref
AbstractAbstract PDFSupplementary MaterialPubReader   

The purpose of this study was to examine the effect of regular exercise training on insulin sensitivity in adults with type 2 diabetes mellitus (T2DM) using the pooled data available from randomised controlled trials. In addition, we sought to determine whether short-term periods of physical inactivity diminish the exercise-induced improvement in insulin sensitivity. Eligible trials included exercise interventions that involved ≥3 exercise sessions, and reported a dynamic measurement of insulin sensitivity. There was a significant pooled effect size (ES) for the effect of exercise on insulin sensitivity (ES, –0.588; 95% confidence interval [CI], –0.816 to –0.359; P<0.001). Of the 14 studies included for meta-analyses, nine studies reported the time of data collection from the last exercise bout. There was a significant improvement in insulin sensitivity in favour of exercise versus control between 48 and 72 hours after exercise (ES, –0.702; 95% CI, –1.392 to –0.012; P=0.046); and this persisted when insulin sensitivity was measured more than 72 hours after the last exercise session (ES, –0.890; 95% CI, –1.675 to –0.105; P=0.026). Regular exercise has a significant benefit on insulin sensitivity in adults with T2DM and this may persist beyond 72 hours after the last exercise session.

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Original Articles
Pathophysiology
The Preventive Effects of 8 Weeks of Resistance Training on Glucose Tolerance and Muscle Fiber Type Composition in Zucker Rats
Ji-yeon Kim, Mi Jung Choi, Byunghun So, Hee-jae Kim, Je Kyung Seong, Wook Song
Diabetes Metab J. 2015;39(5):424-433.   Published online October 22, 2015
DOI: https://doi.org/10.4093/dmj.2015.39.5.424
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AbstractAbstract PDFPubReader   
Background

We investigated the therapeutic effects of resistance training on Zucker rats before and after the onset of diabetes to understand the importance of the timing of exercise intervention. We assessed whether 8 weeks of resistance training ameliorated impaired glucose tolerance and altered muscle fiber type composition in Zucker rats.

Methods

Five-week-old male Zucker rats were divided into Zucker lean control (ZLC-Con), non-exercised Zucker diabetic fatty (ZDF-Con), and exercised Zucker diabetic fatty (ZDF-Ex) groups. The ZDF-Ex rats climbed a ladder three times a week for 8 weeks. Intraperitoneal glucose tolerance tests (IPGTT) were performed on the 1st and 8th weeks of training, and grip strength was measured during the last week. We also measured glucose transporter 4 (GLUT4) expression by Western blot and immunofluorescence. Moreover, immunohistochemistry was performed to assess muscle fiber type composition.

Results

Fasting glucose levels and area under the curve responses to IPGTTs gradually increased as diabetes progressed in the ZDF-Con rats but decreased in the ZDF-Ex rats. Grip strength decreased in the ZDF-Con rats. However, resistance training did not improve grip strength in the ZDF-Ex rats. GLUT4 expression in the ZLC-Con and the ZDF-Con rats did not differ, but it increased in the ZDF-Ex rats. The proportions of myosin heavy chain I and II were lower and higher, respectively, in the ZDF-Con rats compared to the ZLC-Con rats. Muscle fiber type composition did not change in the ZDF-Ex rats.

Conclusion

Our results suggest that regular resistance training initiated at the onset of diabetes can improve glucose tolerance and GLUT4 expression without changing muscle morphology in Zucker rats.

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Effects of Resistance Training and Aerobic Exercise on Insulin Sensitivity in Overweight Korean Adolescents: A Controlled Randomized Trial
Sunghwan Suh, In-Kyong Jeong, Mi Yeon Kim, Yeon Soo Kim, Sue Shin, Sun Sin Kim, Jae Hyeon Kim
Diabetes Metab J. 2011;35(4):418-426.   Published online August 31, 2011
DOI: https://doi.org/10.4093/dmj.2011.35.4.418
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AbstractAbstract PDFPubReader   
Background

Data on the impact of resistance training on insulin resistance in overweight or obese children are inconclusive.

Methods

Thirty overweight South Korean adolescents (mean age of 13.10 years) were divided by sex, and then randomly assigned to one of three treatment groups, which were the diet only (DO), diet with aerobic exercise (AE), or diet with resistance training (RT) group. Physiologic and metabolic parameters were assessed at baseline and after 12 weeks of exercise training and diet modification.

Results

Both exercise groups (aerobic and resistance) showed significant improvements in their insulin area under the curve and insulin sensitivity index values when compared to their baseline values while the DO group showed no significant changes in these variables. Age-, sex-, and body mass index (BMI)-adjusted intergroup comparison analyses showed a marked reduction in BMI and a significant reduction in muscle mass in the AE group when compared to the RT group and the DO group, respectively.

Conclusion

A 12-week exercise training program of either resistance or aerobic activity improved insulin sensitivity in overweight adolescents, although it failed to show superiority over a DO program. Aerobic exercise decreased both body weight and BMI, and it was noted that this group also had a significant reduction in muscle mass when compared to the DO group.

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Effects of Aerobic Exercise vs. Resistance Training on Endothelial Function in Women with Type 2 Diabetes Mellitus
Hwi Ryun Kwon, Kyung Wan Min, Hee Jung Ahn, Hee Geum Seok, Jae Hyuk Lee, Gang Seo Park, Kyung Ah Han
Diabetes Metab J. 2011;35(4):364-373.   Published online August 31, 2011
DOI: https://doi.org/10.4093/dmj.2011.35.4.364
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AbstractAbstract PDFPubReader   
Background

There is controversy over whether aerobic or resistance exercise is more effective for improving endothelial function in type 2 diabetes mellitus (T2DM). This study was aimed to investigate the effects of an aerobic and resistance training program on endothelial function, and the influences of glycemic control, body weight changes, and aerobic capacity in T2DM.

Methods

Total 40 overweight women with T2DM were assigned into 3 groups: an aerobic exercise group (AEG, n=13), resistance exercise group (REG, n=12), and control group (CG, n=15), and followed either brisk walking for the AEG or resistance band training for the REG, 60 minutes per day, 5 days per week for 12 weeks with monitoring daily activity using accelerometers. We assessed endothelial function by flow-mediated dilation (FMD), and aerobic capacity by oxygen uptake at anaerobic threshold (AT_VO2) at baseline and following training program.

Results

The mean participants' age was 57.0±6.8 years, and body mass index (BMI) was 27.0±2.3 kg/m2. After intervention, FMD increased by 2.2±1.9% in AEG, which differed from REG and CG (P=0.002), despite of decreased body weight (BW) in both AG and RG (2.8±2.5%, P=0.002; 1.6±2.0%, P=0.017, respectively). A significant increased AT_VO2 and decreased HbA1c were found only in AEG. In all participants, FMD was changed with the significant relations to the AT_VO2 (r=0.348, P=0.035), but not to HbA1c levels or BW.

Conclusion

Aerobic exercise appears to be more beneficial than resistance exercise for improving endothelial function in T2DM. In addition, aerobic capacity could be a better predictor of changes in FMD than BW and glycemic control.

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The Effects of Resistance Training on Muscle and Body Fat Mass and Muscle Strength in Type 2 Diabetic Women
Hwi Ryun Kwon, Kyung Ah Han, Yun Hyi Ku, Hee Jung Ahn, Bo-Kyung Koo, Ho Chul Kim, Kyung Wan Min
Korean Diabetes J. 2010;34(2):101-110.   Published online April 30, 2010
DOI: https://doi.org/10.4093/kdj.2010.34.2.101
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AbstractAbstract PDFPubReader   
Background

Our goal was to investigate the effects of low intensity resistance training on body fat, muscle mass and strength, cardiovascular fitness, and insulin sensitivity in type 2 diabetes.

Methods

Twenty-eight overweight women with type 2 diabetes were randomly assigned to a resistance training group (RG, n = 13) or a control group (CG, n = 15). RG performed resistance training using elastic bands, of which strength was equal to 40 to 50% of one repetition maximum (1RM), for three days per week. Each exercise consisted of three sets for 60 minutes. We assessed abdominal fat using computed tomography, muscle mass using dual-energy X-ray absorptiometry, and muscle strength using Keiser's chest and leg press. Insulin sensitivity was measured using the insulin tolerance test, and aerobic capacity was expressed as oxygen uptake at the anaerobic threshold (AT-VO2) before and after the 12-week exercise program.

Results

The age of participants was 56.4 ± 7.1 years, duration of diabetes was 5.9 ± 5.5 years, and BMI was 27.4 ± 2.5 kg/m2, without significant differences between two groups. During intervention, a greater increase in muscle mass and greater decreases in both total fat mass and abdominal fat were observed in RG compared to those of CG (P = 0.015, P = 0.011, P = 0.010, respectively). Increase in 1RM of upper and lower extremities was observed in the RG (P = 0.004, P = 0.040, respectively), without changes in AT-VO2 and insulin resistance in either group.

Conclusion

In conclusion, the low intensity resistance training was effective in increasing muscle mass and strength and reducing total fat mass without change of insulin sensitivity in type 2 diabetic patients.

Citations

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Relationship of Maximal Muscle Strength with Body Mass Index and Aerobics Capacity in Type 2 Diabetic Patients.
Hwi Ryun Kwon, Kyung Ah Han, Yun Hyi Ku, Hee Jung Ahn, Bo Kyung Koo, Kyung Wan Min
Korean Diabetes J. 2009;33(6):511-517.   Published online December 1, 2009
DOI: https://doi.org/10.4093/kdj.2009.33.6.511
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AbstractAbstract PDF
BACKGROUND
Combination fitness regimens (including aerobic and resistance exercises) are effective for improving cardio-respiratory fitness, reducing visceral fat and increasing insulin sensitivity in diabetic patients. The combination exercise intensity that a patient is capable of is limited by his or her aerobic capacity and one repetition maximum (1RM). We investigated the relationships between 1RM, aerobic exercise capacity and body mass index in patients with type 2 diabetes. METHODS: A total of 177 (men: 85, women: 92) diabetic subjects with HbA1c < or = 10% were enrolled. Muscle strength and 1RM were assessed bychest press (upper body) and leg press (lower body). We assessed aerobic capacity by VO2max and muscle mass by bioimpedance analysis. RESULTS: There was no correlation between 1RM and VO2max in type 2 diabetic patients (upper: P = 0.122, lower: P = 0.138 for men, and upper: P = 0.952, lower: P = 0.570 for women). However, 1RM was significantly correlated with muscle mass both in men and women (upper: r = 0.493, P < 0.001, r = 0.315, P = 0.002 lower: r = 0.437 P < 0.001, r = 0.307, P =0.003, respectively). There was also a significant correlation between 1RM and BMI. In obese male subjects with BMI > or = 25 kg/m2, we observed a significant correlation between muscle mass and BMI (r = 0.374, P = 0.032), but this correlation was not observed in women. CONCLUSION: Clinicians treating Korean type 2 diabetic subjects should recommend resistance exercise to their patients. In particular, obese women with diabetes may receive greater benefits by increasing muscle mass through resistance exercises.

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  • Evaluation of Muscle Strength and Endurance in Postmenopausal Women: A Cross-sectional Study
    Arati V Mahishale, Manali P Kulkarni
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  • The Correlations between Extremity Circumferences with Total and Regional Amounts of Skeletal Muscle and Muscle Strength in Obese Women with Type 2 Diabetes
    Hwi Ryun Kwon, Kyung Ah Han, Hee Jung Ahn, Jae Hyuk Lee, Gang Seo Park, Kyung Wan Min
    Diabetes & Metabolism Journal.2011; 35(4): 374.     CrossRef
  • The Effects of Aerobic/Resistance Exercise on Body Fat Mass, Muscle Strength and Endothelial Function in Korean Type 2 Diabetes mellitus Patients
    Kyung Wan Min
    Journal of Korean Diabetes.2011; 12(1): 6.     CrossRef
  • The Effects of Resistance Training on Muscle and Body Fat Mass and Muscle Strength in Type 2 Diabetic Women
    Hwi Ryun Kwon, Kyung Ah Han, Yun Hyi Ku, Hee Jung Ahn, Bo-Kyung Koo, Ho Chul Kim, Kyung Wan Min
    Korean Diabetes Journal.2010; 34(2): 101.     CrossRef
Maximal Muscle Strength Deteriorates with Age in Subjects with Type 2 Diabetes Mellitus.
Hwi Ryun Kwon, Yun Hyi Ku, Hee Jung Ahn, Ji Yun Jeong, Sang Ryol Ryu, Bo Kyung Koo, Kyung Ah Han, Kyung Wan Min
Korean Diabetes J. 2009;33(5):412-420.   Published online October 1, 2009
DOI: https://doi.org/10.4093/kdj.2009.33.5.412
  • 2,523 View
  • 24 Download
  • 5 Crossref
AbstractAbstract PDF
BACKGROUND
It is difficult to improve muscle strength with only aerobic exercise training in type 2 diabetes patients. Resistance training is effective for improving muscle mass, muscle strength and insulin sensitivity. One repetition maxima (1RM), or the maximum amount of weight a subject can lift in a single repetition, may be a useful unit for evaluating the results of resistance training in type 2 diabetic patients. This study was aimed to assess baseline values for 1RM in a sample of Korean type 2 diabetes mellitus patients that are scaled for intensity and load of exercise, and to assess the relationship of 1RM to age. METHODS: A total of 266 (male: 95, female: 171) Korean patients with type 2 diabetes mellitus were included in the study sample. Maximal muscle strength was assessed by measuring 1RM for each subject (KEISER, Fresno, CA, USA). Two different exercises were used to measure 1RM: the chest press for the upper extremities, and the leg press for the lower extremities. RESULTS: Both upper and lower values of 1RM decreased with age in men and women; upper 1RM: r = -0.454, P<0.001 in men, r = -0.480, P< 0.001 in women, lower 1RM: r = -0.569, P<0.001 in men, and r = -0.452, P<0.001 in women. Values of 1RM significantly decreased in men only after the age of 70. In women, values of 1RM continuously decreased after the age of 60. CONCLUSION: The maximal muscle strength of individuals with type 2 diabetes decreases with age. We believe that resistance training is especially beneficial for type 2 diabetes mellitus patients after the sixth decade of life.

Citations

Citations to this article as recorded by  
  • The Effects of Floor-seated Exercise Program on Physical Fitness, Depression, and Sleep in Older Adults: A Cluster Randomized Controlled Trial
    Min-Jung Choi, Kyeong-Yae Sohng
    International Journal of Gerontology.2018; 12(2): 116.     CrossRef
  • The Effects of Aerobic/Resistance Exercise on Body Fat Mass, Muscle Strength and Endothelial Function in Korean Type 2 Diabetes mellitus Patients
    Kyung Wan Min
    Journal of Korean Diabetes.2011; 12(1): 6.     CrossRef
  • The Correlations between Extremity Circumferences with Total and Regional Amounts of Skeletal Muscle and Muscle Strength in Obese Women with Type 2 Diabetes
    Hwi Ryun Kwon, Kyung Ah Han, Hee Jung Ahn, Jae Hyuk Lee, Gang Seo Park, Kyung Wan Min
    Diabetes & Metabolism Journal.2011; 35(4): 374.     CrossRef
  • The Effects of Resistance Training on Muscle and Body Fat Mass and Muscle Strength in Type 2 Diabetic Women
    Hwi Ryun Kwon, Kyung Ah Han, Yun Hyi Ku, Hee Jung Ahn, Bo-Kyung Koo, Ho Chul Kim, Kyung Wan Min
    Korean Diabetes Journal.2010; 34(2): 101.     CrossRef
  • Relationship of Maximal Muscle Strength with Body Mass Index and Aerobics Capacity in Type 2 Diabetic Patients
    Hwi Ryun Kwon, Kyung Ah Han, Yun Hyi Ku, Hee Jung Ahn, Bo Kyung Koo, Kyung Wan Min
    Korean Diabetes Journal.2009; 33(6): 511.     CrossRef

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