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Ghafari M, Banitalebi E, Nabipur A. Hypoadiponectinemia, Type 2 Diabetes, Ethnicity, and Exercise Training: A Meta-Analysis of Iranian Randomized Controlled Clinical Trials. mljgoums 2022; 16 (5) :16-25
URL: http://mlj.goums.ac.ir/article-1-1344-en.html
URL: http://mlj.goums.ac.ir/article-1-1344-en.html
1- Department of Sport Sciences, Shahrekord University, Shahrekord, Iran , Ghafari.mehdi@gmail.com
2- Department of Sport Sciences, Shahrekord University, Shahrekord, Iran
2- Department of Sport Sciences, Shahrekord University, Shahrekord, Iran
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| Abstract (HTML) (2322 Views)
.PNG)
Figure 1- The overview of the search strategy
Effects of training on adiponectin
The meta-analysis showed that adiponectin levels increased significantly in diabetic subjects after physical activity (MD: 0.72 ng/dl, p<0.001,), but the heterogeneity of the study remained significant (I2= 89%). As shown in figure 2, different aerobic training modalities significantly increased adiponectin levels (MD: 0.84 ng/dl, p<0.001,), but neither interval training nor concurrent-resistance training significantly altered adiponectin levels (MD: 0.36 ng/dl; p=0.48).
.PNG)
Figure 2- Effects of physical activity on adiponectin levels (ng/dl). The forest plot shows pooled mean differences with 95% confidence intervals (CI) for 14 effect sizes pooled from 17 trials. The effect sizes were merged due to the different training methods used in studies by Zarei (43) and Hosseini (33).
Subgroup analysis
Subgroup analysis was performed for a training method (Figure 3). Based on the results, heterogeneity remained high and adiponectin levels significantly increased across all subgroups.
.PNG)
Figure 3-Effects of different methods of physical activity on adiponectin levels (ng/dl). The forest plot shows pooled mean differences with 95% confidence intervals (CI) for 14 effect sizes pooled from 17 trials (tree separate effect sizes were pooled for different training modalities from Zarei (43), and two from Hosseini (33)).
Sensitivity analysis
No significant change in the effect size was found, which indicates robustness of the data in the initial analysis (Figure 4).
.PNG)
Figure 4-Sensitivity analysis of the studies. In sensitivity analyses, we recalculated the combined results by excluding one study per iteration
.PNG)
Figure 5- The funnel plot showing study precision against the mean difference effect estimate with 95% confidence interval for adiponectin
DISCUSSION
Full-Text: (428 Views)
INTRODUCTION
Diabetes is associated with abdominal fat accumulation (visceral/hepatic) (1). This, along with secretion of inflammatory adipokines such as leptin, adiponectin, interleukin-6, tumor necrosis factor-α (TNF-α), and resistin are important risk factors for insulin resistance (2). It has been shown that there are significant race-ethnic related differences in the secretory profile of adipocytes and circulating adipokines (3). Adiponectin, the most abundant anti-inflammatory adipocytokine (accounting for 0.01% of total serum protein), is secreted by adipocytes. It is involved in energy hemostasis (4), inflammation, vascular physiology (5), insulin sensitivity, and glucose and lipid metabolism (6). It also has cardioprotective and anti-atherogenic properties (7). In fact, it has been shown that hypoadiponectinemia is associated with severity of atherosclerosis and coronary artery disease in people with type 2 diabetes (8). Evidence indicates racial/ethnic differences in hypoadiponectinemia in different metabolic syndromes (9-11).
As exercise training intervention reduces the risk of developing type 2 diabetes complications (12); therefore, it may be interesting to evaluate effects of exercise on hypoadiponectinemia. Physical activity and exercise training also act as potent facilitators for the maintenance of health outcomes in patients with diabetes (13). Considering the racial-ethnic differences is crucial when recommending lifestyle modifications for patients with diabetes (14). Studies have also reported racial/ethnic differences in cardiac responses to submaximal exercise (15, 16), physical activity, dietary behaviors (17), and leisure-time physical activity levels among individuals with diabetes (18). The magnitude of responses of adiponectin to exercise training may also be influenced by race-ethnic characteristics and adiponectin gene polymorphism (19). For example, individuals with the genotype GT + TT at SNP276 (G/T) have a greater adiponectin response to exercise training compared to those with the GG genotype (20). However, some studies demonstrated that polymorphisms of the adiponectin gene are not associated with the effect of exercise training on adiponectin levels (19, 21). Recently, Sellami et al. illustrated the role of racial differences in anaerobic capacity, hematological parameters, and lactate levels during recovery in women (22). On the one hand, such racial/ethnic differences may affect adiponectin level changes in response to exercise training in metabolic syndrome. For example, Arslanian and colleagues showed that race/ethnicity alone has a significant effect, beyond the intervention effect, on adiponectin levels, insulin sensitivity, and β-cell function (9). In addition, there is no difference in the recommended guidelines for exercise training modalities across different racial groups. It has been shown that African-American individuals are generally more likely to follow exercise training recommendations. Hispanic men also have higher physical activity levels than other racial groups. Furthermore, racial/ethnic heterogeneity was found in responses to weight loss interventions. Caucasian and Hispanic individuals show more interest to lose weight (23).
Based on a review of existing literature, we hypothesized that there would be significant racial/ethnic differences in response of hypoadiponectinemia to different types of exercise training in Iranians with diabetes. We further hypothesized that racial differences have been overlooked in some systematic reviews and meta-analysis of randomized controlled trials (RCTs) that evaluated effectiveness of different exercise trainings on diabetes risk factors such as adipokines, especially adiponectin. Finally, we hypothesized that racial/ethnic characteristics should be considered when designing exercise training interventions for diabetic patients. The results related to other races may not be generalized to the Iranian population of diabetics. For example, a systematic review and meta-analysis of RCTs showed that aerobic exercise increased adiponectin levels in non-Iranian people with prediabetes and diabetes (24). Another meta-analysis of RCTs showed that aerobic training did not change adiponectin levels in non-Iranian patients with type 2 diabetes (25). The aim of this study was to conduct a systematic review and meta-analysis on RCTs to evaluate effects of different exercise trainings on hypoadiponectinemia in patients with diabetes, to help better application and generalization of data in Iranian diabetics.
Diabetes is associated with abdominal fat accumulation (visceral/hepatic) (1). This, along with secretion of inflammatory adipokines such as leptin, adiponectin, interleukin-6, tumor necrosis factor-α (TNF-α), and resistin are important risk factors for insulin resistance (2). It has been shown that there are significant race-ethnic related differences in the secretory profile of adipocytes and circulating adipokines (3). Adiponectin, the most abundant anti-inflammatory adipocytokine (accounting for 0.01% of total serum protein), is secreted by adipocytes. It is involved in energy hemostasis (4), inflammation, vascular physiology (5), insulin sensitivity, and glucose and lipid metabolism (6). It also has cardioprotective and anti-atherogenic properties (7). In fact, it has been shown that hypoadiponectinemia is associated with severity of atherosclerosis and coronary artery disease in people with type 2 diabetes (8). Evidence indicates racial/ethnic differences in hypoadiponectinemia in different metabolic syndromes (9-11).
As exercise training intervention reduces the risk of developing type 2 diabetes complications (12); therefore, it may be interesting to evaluate effects of exercise on hypoadiponectinemia. Physical activity and exercise training also act as potent facilitators for the maintenance of health outcomes in patients with diabetes (13). Considering the racial-ethnic differences is crucial when recommending lifestyle modifications for patients with diabetes (14). Studies have also reported racial/ethnic differences in cardiac responses to submaximal exercise (15, 16), physical activity, dietary behaviors (17), and leisure-time physical activity levels among individuals with diabetes (18). The magnitude of responses of adiponectin to exercise training may also be influenced by race-ethnic characteristics and adiponectin gene polymorphism (19). For example, individuals with the genotype GT + TT at SNP276 (G/T) have a greater adiponectin response to exercise training compared to those with the GG genotype (20). However, some studies demonstrated that polymorphisms of the adiponectin gene are not associated with the effect of exercise training on adiponectin levels (19, 21). Recently, Sellami et al. illustrated the role of racial differences in anaerobic capacity, hematological parameters, and lactate levels during recovery in women (22). On the one hand, such racial/ethnic differences may affect adiponectin level changes in response to exercise training in metabolic syndrome. For example, Arslanian and colleagues showed that race/ethnicity alone has a significant effect, beyond the intervention effect, on adiponectin levels, insulin sensitivity, and β-cell function (9). In addition, there is no difference in the recommended guidelines for exercise training modalities across different racial groups. It has been shown that African-American individuals are generally more likely to follow exercise training recommendations. Hispanic men also have higher physical activity levels than other racial groups. Furthermore, racial/ethnic heterogeneity was found in responses to weight loss interventions. Caucasian and Hispanic individuals show more interest to lose weight (23).
Based on a review of existing literature, we hypothesized that there would be significant racial/ethnic differences in response of hypoadiponectinemia to different types of exercise training in Iranians with diabetes. We further hypothesized that racial differences have been overlooked in some systematic reviews and meta-analysis of randomized controlled trials (RCTs) that evaluated effectiveness of different exercise trainings on diabetes risk factors such as adipokines, especially adiponectin. Finally, we hypothesized that racial/ethnic characteristics should be considered when designing exercise training interventions for diabetic patients. The results related to other races may not be generalized to the Iranian population of diabetics. For example, a systematic review and meta-analysis of RCTs showed that aerobic exercise increased adiponectin levels in non-Iranian people with prediabetes and diabetes (24). Another meta-analysis of RCTs showed that aerobic training did not change adiponectin levels in non-Iranian patients with type 2 diabetes (25). The aim of this study was to conduct a systematic review and meta-analysis on RCTs to evaluate effects of different exercise trainings on hypoadiponectinemia in patients with diabetes, to help better application and generalization of data in Iranian diabetics.
MATERIALS AND METHODS
Literature searches of the Cochrane Central Register of Controlled Trials were carried out using the following search strategy: [exercise OR training OR physical activity OR Training] AND diabetes AND adiponectin. Next, RCTs were included and compared with each type of supervised exercise (aerobic training, resistance training, or combined training).
Inclusion criteria were studies involving 4 weeks of exercise intervention on diabetics and clinical trials on a human population. Exclusion criteria were as follows: having type 2 diabetes, RCTs that did not report enough data to complete meta-analysis, double-release or subgroup analysis of trials, and trials with less than 6 weeks of follow-up.
Two examiners extracted all data separately. For the variables of interest, we extracted baseline and post-intervention mean and standard deviation and sample sizes, for intervention and control groups (26).
Two authors separately evaluated the methodological quality of the trials, and the Cochrane risk-of-bias tool was used to evaluate the risk of bias in each study.
Data analysis was carried out using random effect models (27), and the results were expressed as the weighted mean difference (WMD). The effect size was estimated based on the parameters that existed between the control group and the training group. Heterogeneity was evaluated by using the I2 index (28). The funnel plot and the Egger's test were used to assess publication bias (29). The trim and fill methods were used to estimate the potential impact of unpublished studies on our results (21). All analyses were conducted using the Stata statistical software (version 12.0, Stata, College Station, USA).
Inclusion criteria were studies involving 4 weeks of exercise intervention on diabetics and clinical trials on a human population. Exclusion criteria were as follows: having type 2 diabetes, RCTs that did not report enough data to complete meta-analysis, double-release or subgroup analysis of trials, and trials with less than 6 weeks of follow-up.
Two examiners extracted all data separately. For the variables of interest, we extracted baseline and post-intervention mean and standard deviation and sample sizes, for intervention and control groups (26).
Two authors separately evaluated the methodological quality of the trials, and the Cochrane risk-of-bias tool was used to evaluate the risk of bias in each study.
Data analysis was carried out using random effect models (27), and the results were expressed as the weighted mean difference (WMD). The effect size was estimated based on the parameters that existed between the control group and the training group. Heterogeneity was evaluated by using the I2 index (28). The funnel plot and the Egger's test were used to assess publication bias (29). The trim and fill methods were used to estimate the potential impact of unpublished studies on our results (21). All analyses were conducted using the Stata statistical software (version 12.0, Stata, College Station, USA).
RESULTS
Fourteen studies with 444 individuals (236 men and 128 women) were included in the analysis. Figure 1 provides an overview of the search strategy. The age of the participants ranged between 18 and 60 years. The number of exercise sessions per week ranged between 3 and 5. The duration of interventions ranged between 6 and 12 weeks (Table 1).| Author(s), year of publication, reference number | Age (years, +C22:J38Mean ± SD) |
Medical condition | Training sessions per week | Duration of intervention (weeks) |
| Ilkhani et al. [2017](30) | I: 63.12 ± 1.98, C: 63.12 ± 1.98 | T2D | 5 | 8 |
| Mohamadzadeh salamat [2018] (31) | I: 21.9 ± 1.7, C: 21.8 ± 2 | T2D | 3 | 8 |
| Abolfathi et al. [2015](32) | I: 47.85 ± 4.52, C: 45.25 ± 6.86 | T2D | 3 | 8 |
| Hosseini et al [2018] (33) | I: 28.92 ± 3.6, C: 29.18 ± 4.33 | T2D | 3 | 6 |
| Hosseini et al. [2018](33) | I: 30.27 ± 4.149, C: 29.18 ± 4.33 | T2D | 3 | 6 |
| Begzade et al. [2019] (34) | I: 46.22 ± 7.28, C: 47.38 ± 7.08 | T2D | 3 | 8 |
| Abedi (2016) (35) | I: ±, C: ± | T2D | 3 | 8 |
| Parsian et al. (2013) (36) | I: 45 ± 7, C: 43 ± 8 | T2D | 3 | 12 |
| Moradi et al. [2013](37) | I: 20.9 ± 3.6, C: 21.5 ± 3.2 | T2D | 3 | 12 |
| Atashak et al. [2011] (38) | I: 23.71 ± 3.81, C: 24.38 ± 2.33 | T2D | 3 | 10 |
| Rashidlamir and Saadatnia [2010] (39) | I: 40.06 ± 4.04, C: 37.06 ± 5.1 | T2D | 4 | 8 |
| Ghasemnian et al. [2013](40) | I: ±, C: ± | T2D | 4 | 8 |
| Rashidlamir et al. [2013] (41) | I: 22.54 ± 2.54, C: 22.3 ± 1.56 | T2D | 4 | 8 |
| Shavandi et al. [2011](42) | I: 58.8 ± 6.65, C: 53.5 ± 4.5 | T2D | 3 | 8 |
| Zarei et al. [2015](43) | I: 47.9 ± 3, C: 46.9 ± 1.2 | T2D | 3 | 12 |
| Zarei et al. [2015] (43) | I: 45.8 ± 6.3, C: 46.9 ± 1.2 | T2D | 3 | 12 |
| Zarei et al. [2017](43) | I: 47.5 ± 0.9, C: 46.9 ± 1.2 | T2D | 3 | 12 |
Figure 1- The overview of the search strategy
Effects of training on adiponectin
The meta-analysis showed that adiponectin levels increased significantly in diabetic subjects after physical activity (MD: 0.72 ng/dl, p<0.001,), but the heterogeneity of the study remained significant (I2= 89%). As shown in figure 2, different aerobic training modalities significantly increased adiponectin levels (MD: 0.84 ng/dl, p<0.001,), but neither interval training nor concurrent-resistance training significantly altered adiponectin levels (MD: 0.36 ng/dl; p=0.48).
Figure 2- Effects of physical activity on adiponectin levels (ng/dl). The forest plot shows pooled mean differences with 95% confidence intervals (CI) for 14 effect sizes pooled from 17 trials. The effect sizes were merged due to the different training methods used in studies by Zarei (43) and Hosseini (33).
Subgroup analysis
Subgroup analysis was performed for a training method (Figure 3). Based on the results, heterogeneity remained high and adiponectin levels significantly increased across all subgroups.
Figure 3-Effects of different methods of physical activity on adiponectin levels (ng/dl). The forest plot shows pooled mean differences with 95% confidence intervals (CI) for 14 effect sizes pooled from 17 trials (tree separate effect sizes were pooled for different training modalities from Zarei (43), and two from Hosseini (33)).
Sensitivity analysis
No significant change in the effect size was found, which indicates robustness of the data in the initial analysis (Figure 4).
Figure 4-Sensitivity analysis of the studies. In sensitivity analyses, we recalculated the combined results by excluding one study per iteration
Figure 5- The funnel plot showing study precision against the mean difference effect estimate with 95% confidence interval for adiponectin
DISCUSSION
To our knowledge, this is the first systematic review and meta-analysis of RCTs to have investigated the effects of different exercise trainings on hypoadiponectinemia among Iranian diabetics. This is important because there is evidence that the benefits of exercise training interventions for people with diabetes may be influenced by racial and ethnic differences (44). In addition, no previous systematic review and meta-analysis has evaluated effects of exercise training on specific domains of adiponectin levels while considering ethnic differences in Iranian people. Since the prevalence of diabetes in Iran is increasing and background conditions such as ethnicity and race may be involved, it is crucial to identify strategies for successful management of diabetes in Iranians. Although numerous non-pharmacological options are available for treatment diabetes, exercise training always forms an integral part of a diabetes management program. A growing body of evidence demonstrates the benefits of exercise training, and adipocytokines might represent a possible explanation when it comes to the mechanisms mediating the beneficial effects of exercise training on impaired glucose metabolism.
Hypoadiponectinemia is closely related to insulin resistance, hyperinsulinemia, impaired glucose metabolism, inflammation, obesity, type 2 diabetes (45-48), and atherosclerosis (49, 50). Increased circulating adiponectin concentrations have been shown to be associated with a reduced risk of diabetes, even among different races (9, 51). It has been reported that exercise training interventions exert greater effects on circulating adiponectin compared with glucose/lipid-lowering medicines (52), anti-hypertensive drugs, anti-atherosclerotic agents, and nutritional interventions (53). Our study illustrated that circulating adiponectin levels increased in response to exercise training in adults Iranians with prediabetes and diabetes. This is in line with results of a previous meta-analysis on overweight and obese individuals of different races (54). A meta-analysis by Becic el al. (24) reported that physical exercise, particularly aerobic exercise, significantly changes adiponectin levels in diabetics; however, this meta-analysis did not include studies on Iranians. In contrast to our results, Hayashino and colleagues (25) did not find any significant changes in circulating adiponectin levels in response to exercise training in individuals with type 2 diabetes; however, this meta-analysis included studies that had been performed on racial groups different from ours.
Our meta-analysis confirms that adiponectin levels significantly increase following exercise training at an adequate duration and intensity in Iranian diabetics. However, caution is needed when comparing the results of our study with others because some studies included aerobic exercise (24, 56) or resistance exercise (57), and combined aerobic-resistance exercise (58). Nevertheless, high heterogeneity was also found in previous racial/ethnic meta-analyses (23). In this regards, racial/ethnic differences may be a reason for the significant differences between our study and other systematic reviews and meta-analysis studies. The present systematic review and meta-analysis of Iranian RCTs provides new empirical evidence on racial/ethnic heterogeneity in diabetes-related risk factors for adults with diabetes.
The present systematic review and meta-analysis of RCTs had both strengths and limitations that should be considered. First, publication bias could not be avoided and excluded. Moreover, some Iranian RCTs included in the present study reported concealed allocation. Furthermore, some Iranian RCTs had small sizes (fewer than 20 subjects for each group), which tend to lead to extreme effects. One of the major strengths of the present systematic review was the evaluation of the effects of exercise training on Iranians with diabetes. This was achieved using a comprehensive search strategy, which included Iranian RTCs and a more homogenous racial population.
CONCLUSION
It has been well-established that exercise training is a feasible and beneficial method for management of diabetes risk factors, including hypoadiponectinemia. However, in terms of minimizing the risk of hypoadiponectinemia, the optimal quality of exercise training and the mechanisms involved in hypoadiponectinemia, diabetes, and ethnicity/race are relatively unclear. Furthermore, this benefit may be more substantial when accompanied by racial considerations. It is recommended to conduct large RCTs focusing on the effects of different exercise modalities on diabetes-related risk factors. In addition, we suggest considering ethnic diversities when recommending exercise training regimens for decreasing diabetes-related risk factors. However, RCT articles with larger sample sizes and different racial subgroups of diabetic patients are needed to confirm the effect of exercise.
ACKNOWLEDGEMENTS
The authors gratefully acknowledge the Research Deputy of Shahrekord University for supporting this study.
DECLARATIONS
FUNDING
The authors received no financial support for the research, authorship, and/or publication of this article.
Ethics approvals and consent to participate
Not applicable.
CONFLICT OF INTEREST
The authors declare that there is no conflict of interest regarding publication of this article.
The present systematic review and meta-analysis of RCTs had both strengths and limitations that should be considered. First, publication bias could not be avoided and excluded. Moreover, some Iranian RCTs included in the present study reported concealed allocation. Furthermore, some Iranian RCTs had small sizes (fewer than 20 subjects for each group), which tend to lead to extreme effects. One of the major strengths of the present systematic review was the evaluation of the effects of exercise training on Iranians with diabetes. This was achieved using a comprehensive search strategy, which included Iranian RTCs and a more homogenous racial population.
CONCLUSION
It has been well-established that exercise training is a feasible and beneficial method for management of diabetes risk factors, including hypoadiponectinemia. However, in terms of minimizing the risk of hypoadiponectinemia, the optimal quality of exercise training and the mechanisms involved in hypoadiponectinemia, diabetes, and ethnicity/race are relatively unclear. Furthermore, this benefit may be more substantial when accompanied by racial considerations. It is recommended to conduct large RCTs focusing on the effects of different exercise modalities on diabetes-related risk factors. In addition, we suggest considering ethnic diversities when recommending exercise training regimens for decreasing diabetes-related risk factors. However, RCT articles with larger sample sizes and different racial subgroups of diabetic patients are needed to confirm the effect of exercise.
ACKNOWLEDGEMENTS
The authors gratefully acknowledge the Research Deputy of Shahrekord University for supporting this study.
DECLARATIONS
FUNDING
The authors received no financial support for the research, authorship, and/or publication of this article.
Ethics approvals and consent to participate
Not applicable.
CONFLICT OF INTEREST
The authors declare that there is no conflict of interest regarding publication of this article.
Research Article: Systematic Review |
Subject:
Sport Physiology
Received: 2020/11/14 | Accepted: 2021/10/10 | Published: 2022/09/6 | ePublished: 2022/09/6
Received: 2020/11/14 | Accepted: 2021/10/10 | Published: 2022/09/6 | ePublished: 2022/09/6
References
1. Ghafari M, Banitalebi E, Faramarzi M. The relationship between the expression of PLIN3 and PLIN5 protein flowing endurance training in streptozotocin rats.J Shahrekord Univ Med Sci. 2019; 21(4): 194-9. [View at Publisher] [DOI:10.34172/jsums.2019.34] [Google Scholar]
2. Freitas Lima LC, Braga VdA, do Socorro de França Silva M, Cruz JdC, Sousa Santos SH, de Oliveira Monteiro MM, et al. diabetes and atherosclerosis: an inflammatory association. Frontiers in physiology. Adipokines. 2015; 6: 304. [View at Publisher] [DOI:10.3389/fphys.2015.00304] [PubMed] [Google Scholar]
3. Khan UI, Wang D, Sowers MR, Mancuso P, Everson-Rose SA, Scherer PE, et al. Race-ethnic differences in adipokine levels: the Study of Women's Health Across the Nation (SWAN). Metabolism. 2012;61(9):1261-9. [View at Publisher] [DOI:10.1016/j.metabol.2012.02.005] [PubMed] [Google Scholar]
4. Lee B, Shao J. Adiponectin and energy homeostasis. Reviews in Endocrine and Metabolic Disorders. 2014; 15(2): 149-56. [View at Publisher] [DOI:10.1007/s11154-013-9283-3] [PubMed] [Google Scholar]
5. Vaiopoulos AG, Marinou K, Christodoulides C, Koutsilieris M. The role of adiponectin in human vascular physiology. International journal of cardiology. 2012; 155(2): 188-93. [View at Publisher] [DOI:10.1016/j.ijcard.2011.07.047] [PubMed] [Google Scholar]
6. Tschritter O, Fritsche A, Thamer C, Haap M, Shirkavand F, Rahe S, et al. Plasma adiponectin concentrations predict insulin sensitivity of both glucose and lipid metabolism. Diabetes. 2003;52(2):239-43. [View at Publisher] [DOI:10.2337/diabetes.52.2.239] [Google Scholar]
7. Ohashi K, Ouchi N, Matsuzawa Y. Anti-inflammatory and anti-atherogenic properties of adiponectin. Biochimie. 2012;94(10):2137-42. [View at Publisher] [DOI:10.1016/j.biochi.2012.06.008] [PubMed] [Google Scholar]
8. Baldasseroni S, Antenore A, Di Serio C, Orso F, Lonetto G, Bartoli N, et al. diabetes and ischemic heart failure: a challenging relationship. Cardiovascular diabetology. Adiponectin. 2012; 11(1): 151. [View at Publisher] [DOI:10.1186/1475-2840-11-151] [PubMed] [Google Scholar]
9. Arslanian S, Bacha F, Caprio S, Goland R, Haymond MW, Levitsky L, et al. Adiponectin, insulin sensitivity, β-cell function, and racial/ethnic disparity in treatment failure rates in TODAY. Diabetes care. 2017;40(1):85-93. [View at Publisher] [DOI:10.2337/dc16-0455] [PubMed] [Google Scholar]
10. Hasson BR, Apovian C, Istfan N. Racial/ethnic differences in insulin resistance and beta cell function: relationship to racial disparities in type 2 diabetes among African Americans versus Caucasians. Current obesity reports. 2015;4(2):241-9. [View at Publisher] [DOI:10.1007/s13679-015-0150-2] [PubMed] [Google Scholar]
11. Morimoto Y, Conroy SM, Ollberding NJ, Kim Y, Lim U, Cooney RV, et al. Ethnic differences in serum adipokine and C-reactive protein levels: the multiethnic cohort. International journal of obesity. 2014; 38(11): 1416-22. [View at Publisher] [DOI:10.1038/ijo.2014.25] [PubMed] [Google Scholar]
12. Ghafari M, Faramarzi M, Hemati ZJAd. Effect Of Endurance Training With Different Intensities on HBA1C in Type 2 diabetes. Armaghane Danesh. 2020; 25(4): 503-514. [View at Publisher]
13. Colberg SR, Sigal RJ, Yardley JE, Riddell MC, Dunstan DW, Dempsey PC, et al. Physical activity/exercise and diabetes: a position statement of the American Diabetes Association. Diabetes care. 2016; 39(11): 2065-79. [View at Publisher] [DOI:10.2337/dc16-1728] [PubMed] [Google Scholar]
14. Bacon E. Racial/ethnic differences in treatment recommendations: lifestyle changes and medication prescriptions for high cholesterol. Ethnicity & health.25(2):273-88. [View at Publisher] [DOI:10.1080/13557858.2017.1398315] [PubMed] [Google Scholar]
15. Foulds HJA, Bredin SSD, Warburton DER. Ethnic differences in the cardiac responses to aerobic exercise. Ethnicity & health.24(2):168-81. [View at Publisher] [DOI:10.1080/13557858.2017.1315377] [PubMed] [Google Scholar]
16. Ghafari M, Faramarzi M, banitalebi E. Comparison Effect of Continuous and Interval Training on Glycemic Factors in Type 2 Diabetic Patients: A Systematic Review and Meta-Analysis of Internal Articles. Sport Physiology. 2021; 13(51): 17-42. [View at Publisher] [DOI] [Google Scholar]
17. Nwasuruba C, Khan M, Egede LE. Racial/ethnic differences in multiple self-care behaviors in adults with diabetes. Journal of general internal medicine. 2007; 22(1): 115-20. [View at Publisher] [DOI:10.1007/s11606-007-0120-9] [PubMed] [Google Scholar]
18. Egede LE, Poston ME. Racial/ethnic differences in leisure-time physical activity levels among individuals with diabetes. Diabetes care. 2004; 27(10): 2493-4. [View at Publisher] [DOI:10.2337/diacare.27.10.2493] [Google Scholar]
19. Lee K-Y, Kang H-S, Shin Y-A. Exercise improves adiponectin concentrations irrespective of the adiponectin gene polymorphisms SNP45 and the SNP276 in obese Korean women. Gene. 2013; 516(2): 271-6. [View at Publisher] [DOI:10.1016/j.gene.2012.12.028] [PubMed] [Google Scholar]
20. Huang H, Iida KT, Murakami H, Saito Y, Otsuki T, Iemitsu M, et al. Influence of adiponectin gene polymorphism SNP276 (G/T) on adiponectin in response to exercise training. Endocrine journal. 2007;54(6):879-86. [View at Publisher] [DOI:10.1507/endocrj.K06-146] [PubMed] [Google Scholar]
21. Hulver MW, Zheng D, Tanner CJ, Houmard JA, Kraus WE, Slentz CA, et al. Adiponectin is not altered with exercise training despite enhanced insulin action. American Journal of Physiology-Endocrinology And Metabolism. 2002; 283(4): E861-E5. [View at Publisher] [DOI:10.1152/ajpendo.00150.2002] [Google Scholar]
22. Sellami M, Chamari K, Zagatto AM, Kebsi W, Chaouachi A, Zouhal H. Racial differences in hemoglobin and plasma volume variation: implications for muscle performance and recovery. Ethnicity & health. 2019; 24(2):182-93. [View at Publisher] [DOI:10.1080/13557858.2017.1315375] [PubMed] [Google Scholar]
23. Gavin JR, Fox KM, Grandy S. Race/Ethnicity and gender differences in health intentions and behaviors regarding exercise and diet for adults with type 2 diabetes: A cross-sectional analysis. BMC public health. 2011;11(1):533. [View at Publisher] [DOI:10.1186/1471-2458-11-533] [PubMed] [Google Scholar]
24. Becic T, Studenik C, Hoffmann G. Exercise increases adiponectin and reduces leptin levels in prediabetic and diabetic individuals: systematic review and meta-analysis of randomized controlled trials. Medical Sciences. 2018; 6(4): 97. [View at Publisher] [DOI:10.3390/medsci6040097] [PubMed] [Google Scholar]
25. Hayashino Y, Jackson JL, Hirata T, Fukumori N, Nakamura F, Fukuhara S, et al. Effects of exercise on C-reactive protein, inflammatory cytokine and adipokine in patients with type 2 diabetes: a meta-analysis of randomized controlled trials. Metabolism. 2014;63(3):431-40. [View at Publisher] [DOI:10.1016/j.metabol.2013.08.018] [PubMed] [Google Scholar]
26. Sutton AJ, Higgins JP. Recent developments in meta‐analysis. Statistics in medicine. 2008;27(5):625-50. [View at Publisher] [DOI:10.1002/sim.2934] [PubMed] [Google Scholar]
27. Harbord RM, Higgins JP. Meta-regression in Stata. The Stata Journal. 2008; 8(4): 493-519. [View at Publisher] [DOI:10.1177/1536867X0800800403] [Google Scholar]
28. Schünemann HJ, Oxman AD, Higgins JP, Vist GE, Glasziou P, Guyatt GH. Presenting results and 'Summary of findings' tables. Cochrane handbook for systematic reviews of interventions. 2008;5:0. [View at Publisher] [DOI] [Google Scholar]
29. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. Bmj. 2003;327(7414):557-60. [View at Publisher] [DOI:10.1136/bmj.327.7414.557] [PubMed] [Google Scholar]
30. Ilkhani B, Hejazi K, Jafari A. The effects of aerobic interval exercise on Adiponectin, Hemoglobin A1c and insulin resistance index in Elderly Men with Type 2 Diabetes %J nursing of the vulnerable journal. 2017;4(10):1-12. [View at Publisher]
31. Mohamadzadeh salamat K. The effect of continues and progressive resistance training on serum adiponectin and vaspin concentration and insulin resistance in overweight men. Iranian Journal of Diabetes and Metabolism. 2018;17(6):317-24. [View at Publisher]
32. abolfathi F, ranjbar R, shakerian S, yazdan panah L. The Effect of Eight Weeks Aerobic Interval Training on Adiponectin Serum Levels, Lipid Profile and HS-CRP in Women With Type II diabetes. Iranian Journal of Endocrinology and Metabolism. 2015; 17 (4) :316-324 [View at Publisher] [Google Scholar]
33. Hosseini SA, Kazemi N, Nouri R, Kasraian M. The Effect of Aqua and Resistance Trainings on Lipid Profile, Adiponectin, Insulin, and Glucose in Women with Gestational Diabetes Mellitus. The Iranian Journal of Obstetrics, Gynecology and Infertility. 2018;21(4):8-18. [View at Publisher] [Google Scholar]
34. Begzade M, Hossainpppr S, Safi-Khani H. The effect of aerobic training with cinnamon on insulin resistance index and plasma glucose, visfatin and adiponectin levels in men with excess type II diabetes. Journal of Applied Exercise Physiology. 2019;14(28):173-8. [View at Publisher] [Google Scholar]
35. Abedi B. The Effect of 8 Weeks of High-Intensity Interval Training (HIIT) on Serum Adiponectin Levels and Insulin Resistance of Women with Type 2 Diabetes. Journal of Sport Biosciences. 2016 Oct 22;8(3):411-25. [View at Publisher] [Google Scholar]
36. Parsian H, Eizadi M, Khorshidi D, Khanali F. The effect of long-term aerobic exercise on serum adiponectin and insulin sensitivity in type 2 diabetic patients. Journal of Jahrom University of Medical Sciences. 2013;11(1):41-8. [View at Publisher] [DOI:10.29252/jmj.11.1.6] [Google Scholar]
37. Moradi F, AminiAghdam S, Abdi J, Matinhomaee H. Effect of strength training on serum levels of adiponectin, testosterone, and cortisol in sedentary lean men. Journal of Birjand University of Medical Sciences. 2013;20(2):125-35. [View at Publisher] [Google Scholar]
38. Atashak S, Jafari A, Azarbayjani MA. The Influences of long-term resistance training on Adiponectin and lipid profiles levels in obese men. Razi Journal of Medical Sciences. 2011; 18(86): 1-11. [View at Publisher] [Google Scholar]
39. Rashidlamir A, Saadatnia A. The effects of an eight-week aerobic training program on plasma adipokine concentrations in middle-aged men. Tehran University Medical Journal. 2011;69(2): 2011; 69(2): 118-124. [View at Publisher] [Google Scholar]
40. Ghasemnian A, Ghaeini A, Kordi M, Hedayati M, Rami M, Ghorbanian B. Effect of interval endurance training program on plasma eotaxin, adiponectin levels, insulin resistance, serum lipid profile and body composition in overweight and obese adolescents. URMIA MEDICAL JOURNAL. 2013; 24(6): 430-40. [View at Publisher] [Google Scholar]
41. Rashidlamir A, Gholamian S, Ebrahimi Atri A, Seyyedalhoseyni M, Hesar Kooshki M. Effect of regular aerobic exercise on plasma levels of resistin and adiponectin in active young females. Journal of Mazandaran University of Medical Sciences. 2013; 23(101): 67-76. [View at Publisher] [Google Scholar]
42. Shavandi N, Saremi A, Ghorbani A, Parastesh M. Effects of aerobic training on resistin, adiponectin and insulin resistance index in type 2 diabetic men. 2011. [Google Scholar]
43. M Z, MRH N, AH T, S A. he effect of three different intensified aerobic resistance training programs on the levels of adiponectin. Sport Physiol 2015;12(4):1-12.
44. Vaccaro JA, Huffman FG. Sex and race/ethnicity differences in following dietary and exercise recommendations for US representative sample of adults with type 2 diabetes. American journal of men's health. 2017;11(2):380-91. [View at Publisher] [DOI:10.1177/1557988316681126] [PubMed] [Google Scholar]
45. KIYA M, TAMURA Y, TAKENO K, SOMEYA Y, KAKEHI S, SATO M, et al. 1704-P: Coexistence of Hypoadiponectinemia and Impaired Adipose Tissue Insulin Sensitivity Increases the Risk of Metabolic Abnormality Due to Muscle Insulin Resistance in Nonobese Japanese Men. Am Diabetes Assoc; 2020. [View at Publisher] [DOI:10.2337/db20-1704-P] [Google Scholar]
46. Weyer C, Funahashi T, Tanaka S, Hotta K, Matsuzawa Y, Pratley RE, et al. Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. The Journal of Clinical Endocrinology & Metabolism. 2001;86(5):1930-5. [View at Publisher] [DOI:10.1210/jcem.86.5.7463] [Google Scholar]
47. Prakash J, Mittal B, Awasthi S, Agarwal C, Srivastava N. Hypoadiponectinemia in obesity: association with insulin resistance. Indian Journal of Clinical Biochemistry. 2013;28(2):158-63. [View at Publisher] [DOI:10.1007/s12291-012-0246-3] [PubMed] [Google Scholar]
48. Mohammadzadeh G, Zarghami N. Hypoadiponectinemia in obese subjects with type II diabetes: A close association with central obesity indices. Journal of research in medical sciences: the official journal of Isfahan University of Medical Sciences. 2011;16(6):713. [PubMed] [Google Scholar]
49. Hui E, Xu A, Chow W-S, Lee PC, Fong CH, Cheung SC, et al. Hypoadiponectinemia as an independent predictor for the progression of carotid atherosclerosis: a 5-year prospective study. Metabolic syndrome and related disorders. 2014;12(10):517-22. [View at Publisher] [DOI:10.1089/met.2014.0024] [PubMed] [Google Scholar]
50. Pilz S, Sargsyan K, Mangge H. Hypoadiponectinemia as a risk factor for atherosclerosis? Stroke. 2006;37(7):1642-. [View at Publisher] [DOI:10.1161/01.STR.0000227260.24490.56] [Google Scholar]
51. Mather KJ, Funahashi T, Matsuzawa Y, Edelstein S, Bray GA, Kahn SE, et al. Adiponectin, change in adiponectin, and progression to diabetes in the Diabetes Prevention Program. Diabetes. 2008;57(4):980-6. [View at Publisher] [DOI:10.2337/db07-1419] [PubMed] [Google Scholar]
52. Achari AE, Jain SK. Adiponectin, a therapeutic target for obesity, diabetes, and endothelial dysfunction. International Journal of Molecular Sciences. 2017;18(6):1321. [View at Publisher] [DOI:10.3390/ijms18061321] [PubMed] [Google Scholar]
53. Yanai H, Yoshida H. Beneficial effects of adiponectin on glucose and lipid metabolism and atherosclerotic progression: mechanisms and perspectives. International Journal of Molecular Sciences. 2019;20(5):1190. [View at Publisher] [DOI:10.3390/ijms20051190] [Google Scholar]
54. Yu N, Ruan Y, Gao X, Sun J. Systematic review and meta-analysis of randomized, controlled trials on the effect of exercise on serum leptin and adiponectin in overweight and obese individuals. Hormone and Metabolic Research. 2017;49(03):164-73. [View at Publisher] [DOI:10.1055/s-0042-121605] [PubMed] [Google Scholar]
55. Asad MR, Ferdosi MH, Yoosefi Z. The effects of three training methods endurance, resistance and concurrent on adiponectin resting levels in overweighed untrained men. Procedia-Social and Behavioral Sciences. 2012;46:440-4. [View at Publisher] [DOI:10.1016/j.sbspro.2012.05.138] [PubMed] [Google Scholar]
56. Lin H, Hu M, Yan Y, Zhang H. The effect of exercise on adiponectin and leptin levels in overweight or obese subjects: a meta-analysis of randomized controlled trials. Sport Sciences for Health. 2017;13(2):303-14. [View at Publisher] [DOI:10.1007/s11332-017-0358-5] [Google Scholar]
57. Sirico F, Bianco A, D'Alicandro G, Castaldo C, Montagnani S, Spera R, et al. Effects of physical exercise on adiponectin, leptin, and inflammatory markers in childhood obesity: systematic review and meta-analysis. Childhood Obesity. 2018;14(4):207-17. [View at Publisher] [DOI:10.1089/chi.2017.0269] [PubMed] [Google Scholar]
58. Costa RR, Buttelli ACK, Vieira AF, Coconcelli L, de Lima Magalhães R, Delevatti RS, et al. Effect of strength training on lipid and inflammatory outcomes: systematic review with meta-analysis and meta-regression. Journal of Physical Activity and Health. 2019;16(6):477-91. [View at Publisher] [DOI:10.1123/jpah.2018-0317] [PubMed] [Google Scholar]
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