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Qiu B, Zhou Y, Tao X, Hou X, Du L, Lv Y, Yu L. The effect of exercise on flow-mediated dilation in people with type 2 diabetes mellitus: a systematic review and meta-analysis of randomized controlled trials. Front Endocrinol (Lausanne) 2024; 15:1347399. [PMID: 38596227 PMCID: PMC11002232 DOI: 10.3389/fendo.2024.1347399] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/30/2023] [Accepted: 03/11/2024] [Indexed: 04/11/2024] Open
Abstract
INTRODUCTION An increasing number of studies have investigated the effect of exercise on flow-mediated dilation (FMD) in people with type 2 diabetes mellitus (T2DM), while the findings were controversial. The primary aim of this systematic review and meta-analysis was to investigate the effect of exercise on FMD in T2DM patients, and the secondary aim was to investigate the optimal type, frequency, session duration, and weekly time of exercise for T2DM patients. METHODS Searches were conducted in PubMed, Cochrane Library, Scopus, Web of Science, Embase and EBSCO databases. The Cochrane risk of bias tool (RoB2) in randomized trial and Physiotherapy Evidence Database (PEDro) scale were used to assess the methodological quality of the included studies. RESULTS From the 3636 search records initially retrieved, 13 studies met the inclusion criteria. Our meta-analysis revealed that exercise had a significant effect on improving FMD in T2DM patients [WMD, 2.18 (95% CI, 1.78-2.58), p < 0.00001, I2 = 38%], with high-intensity interval training (HIIT) being the most effective intervention type [HIIT, 2.62 (1.42-3.82); p < 0.0001; aerobic exercise, 2.20 (1.29-3.11), p < 0.00001; resistance exercise, 1.91 (0.01-3.82), p = 0.05; multicomponent training, 1.49 (0.15-2.83), p = 0.03]. In addition, a higher frequency [> 3 times, 3.06 (1.94-4.19), p < 0.00001; ≤ 3 times, 2.02 (1.59-2.45), p < 0.00001], a shorter session duration [< 60 min, 3.39 (2.07-4.71), p < 0.00001; ≥ 60 min, 1.86 (1.32-2.40), p < 0.00001], and a shorter weekly time [≤ 180 min, 2.40 (1.63-3.17), p < 0.00001; > 180 min, 2.11 (0.82-3.40), p = 0.001] were associated with larger improvements in FMD. CONCLUSION This meta-analysis provides clinicians with evidence to recommended that T2DM patients participate in exercise, especially HIIT, more than 3 times per week for less than 60 min, with a target of 180 min per week being reached by increasing the frequency of exercise. SYSTEMATIC REVIEW REGISTRATION https://www.crd.york.ac.uk/prospero, identifier CRD42023466575.
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Affiliation(s)
- Bopeng Qiu
- Department of Strength and Conditioning Assessment and Monitoring, Beijing Sport University, Beijing, China
| | - Yilun Zhou
- Department of Strength and Conditioning Assessment and Monitoring, Beijing Sport University, Beijing, China
| | - Xifeng Tao
- Department of Strength and Conditioning Assessment and Monitoring, Beijing Sport University, Beijing, China
- School of Physical Education, Xihua University, Chengdu, China
| | - Xiao Hou
- School of Sport Sciences, Beijing Sport University, Beijing, China
| | - Liwen Du
- Department of Strength and Conditioning Assessment and Monitoring, Beijing Sport University, Beijing, China
| | - Yuanyuan Lv
- China Institute of Sport and Health Science, Beijing Sport University, Beijing, China
| | - Laikang Yu
- Department of Strength and Conditioning Assessment and Monitoring, Beijing Sport University, Beijing, China
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Chen S, Zhou K, Shang H, Du M, Wu L, Chen Y. Effects of concurrent aerobic and resistance training on vascular health in type 2 diabetes: a systematic review and meta-analysis. Front Endocrinol (Lausanne) 2023; 14:1216962. [PMID: 37780628 PMCID: PMC10534066 DOI: 10.3389/fendo.2023.1216962] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/04/2023] [Accepted: 08/29/2023] [Indexed: 10/03/2023] Open
Abstract
Objective To determine the impacts of concurrent aerobic and resistance training on vascular structure (IMT) and function (PWV, FMD, NMD) in type 2 diabetes (T2D). Methods The electronic databases PubMed, Web of Science Core Collection, Cochrane Library, Embase, Scopus, CINAHL, and SPORTDiscus were systematically searched for articles on "type 2 diabetes" and "concurrent training" published from inception to August 2, 2022. We included randomized controlled trials that examined the effects of concurrent training versus passive controls on IMT, PWV, FMD and NMD in T2D. Results Ten studies were eligible, including a total of 361 participants. For IMT, concurrent training showed a slight decrease by 0.05 mm (95% CI -0.11 to 0.01, p > 0.05). concurrent training induced an overall significant improvement in FMD by 1.47% (95% CI 0.15 to 2.79, p < 0.05) and PWV by 0.66 m/s (95% CI -0.89 to -0.43, p < 0.01) in type 2 diabetics. However, concurrent training seemed to exaggerate the impaired NMD (WMD = -2.30%, 95% CI -4.02 to -0.58, p < 0.05). Conclusions Concurrent training is an effective method to improve endothelial function and artery stiffness in T2D. However, within 24 weeks concurrent training exacerbates vascular smooth muscle dysfunction. More research is needed to explore whether longer and/or higher-intensity concurrent training interventions could enhance the vascular structure and smooth muscle function in this population. Systematic review registration www.crd.york.ac.uk/PROSPERO/, identifier CRD42022350604.
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Affiliation(s)
- Shengju Chen
- School of Physical Education, Liaoning Normal University, Dalian, China
| | - Kaixiang Zhou
- Sports Health College, Chengdu University of Traditional Chinese Medicine, Chengdu, China
| | - Huayu Shang
- School of Sports Medicine and Health, Chengdu Sport University, Chengdu, China
| | - Mingyang Du
- College of Physical Education, Chongqing University, Chongqing, China
| | - Linfeng Wu
- College of Physical Education, Chongqing University, Chongqing, China
| | - Yu Chen
- College of Physical Education, Chongqing University, Chongqing, China
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Vitez L, Bunc M, Jug B. The Effects of Exercise Training on Exercise Capacity and Vascular Function after Transcatheter Aortic Valve Implantation-A Pilot Study. J Cardiovasc Dev Dis 2023; 10:343. [PMID: 37623356 PMCID: PMC10455217 DOI: 10.3390/jcdd10080343] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/29/2023] [Revised: 08/05/2023] [Accepted: 08/10/2023] [Indexed: 08/26/2023] Open
Abstract
Transcatheter aortic valve implantation (TAVI) improves event-free survival in patients with severe aortic stenosis, but patients' exercise capacity remains poor after the procedure. Therefore, we sought to compare the effects of a supervised center-based exercise training program and unsupervised exercise routine on exercise capacity and vascular function in patients after TAVI. Patients were randomized to either center-based exercise training (12-24 sessions of combined aerobic and low-weight resistance training twice weekly for 8-12 weeks) or an unsupervised home-based exercise routine (initial appraisal with detailed recommendations and monthly follow-up). Exercise capacity (cardiopulmonary testing) and vascular function (ultrasonographic measurement of flow-mediated vasodilation (FMD) and arterial stiffness) were assessed at the baseline and after the study period. We included 23 patients (mean age of 81 years, 61% women), with higher-than-expected drop-out rates (41%) because of the coronavirus-19 pandemic outbreak. Exercise capacity improved over time, irrespective of the intervention group: 0.09 mL/min/kg increase in peak oxygen uptake (95% CI [0.01-0.16]; p = 0.02), 8.2 Watts increase in workload (95% CI [0.6-15.8]; p = 0.034), and 47 s increase in cumulative exercise time (95% CI [5.0-89.6]; p = 0.029). A between-group difference in change over time (treatment effect) was detected only for FMD (4.49%; 95% CI [2.35; 6.63], p < 0.001), but not for other outcome variables. Both supervised and unsupervised exercise training improve exercise capacity and vascular function in patients after TAVI, with supervised exercise training possibly yielding larger improvements in vascular function, as determined by FMD.
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Affiliation(s)
- Luka Vitez
- Department of Cardiology, Division of Internal Medicine, University Medical Centre Ljubljana, 1000 Ljubljana, Slovenia
- Faculty of Medicine, University of Ljubljana, 1000 Ljubljana, Slovenia
| | - Matjaž Bunc
- Department of Cardiology, Division of Internal Medicine, University Medical Centre Ljubljana, 1000 Ljubljana, Slovenia
- Faculty of Medicine, University of Ljubljana, 1000 Ljubljana, Slovenia
| | - Borut Jug
- Faculty of Medicine, University of Ljubljana, 1000 Ljubljana, Slovenia
- Department of Vascular Diseases, Division of Internal Medicine, University Medical Centre Ljubljana, 1000 Ljubljana, Slovenia
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Eseadi C, Amedu AN. Potential impact of music interventions in managing diabetic conditions. World J Clin Cases 2023; 11:2916-2924. [PMID: 37215419 PMCID: PMC10198074 DOI: 10.12998/wjcc.v11.i13.2916] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/29/2022] [Revised: 03/01/2023] [Accepted: 04/04/2023] [Indexed: 04/25/2023] Open
Abstract
Diabetes is one of the most prevalent diseases, characterized by an insufficiency in insulin secretion as well as chronic hyperglycemia and disturbances in carbohydrate, lipid, and protein metabolism. The major aim of this study was to conduct a literature review on the impact of music intervention on the management of diabetic conditions among patients. Available studies on the impact of music interventions on the management of diabetic conditions were reviewed and analysed using descriptive literature review approach. This review showed that music intervention plays a dual role in managing patients' diabetic conditions. First, music intervention is impactful in managing the health condition of diabetic patients through enhancing the patient’s compliance with exercise, improving lower limb blood circulation, and enhancing health parameters that increase autonomous balance among diabetic patients. Second, music therapy is impactful in the management of diabetic conditions through lowering blood sugar, heart rate, glucose levels, and stress among patients. However, with the number of empirical studies available in this regard, the impact of music intervention is still growing, and longer-term studies and randomised controlled trials with robust sample size are recommended to reach a more valid conclusion.
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Affiliation(s)
- Chiedu Eseadi
- Department of Educational Psychology, Faculty of Education, University of Johannesburg, Johannesburg 2006, Gauteng, South Africa
| | - Amos Nnaemeka Amedu
- Social Science Education, University of Nigeria, Nsukka 41001, Enugu State, Nigeria
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Shivgulam ME, Liu H, Schwartz BD, Langley JE, Bray NW, Kimmerly DS, O'Brien MW. Impact of Exercise Training Interventions on Flow-Mediated Dilation in Adults: An Umbrella Review. Sports Med 2023; 53:1161-1174. [PMID: 37017797 DOI: 10.1007/s40279-023-01837-w] [Citation(s) in RCA: 12] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 03/08/2023] [Indexed: 04/06/2023]
Abstract
BACKGROUND Dysfunction of the endothelium is a key precursor of cardiovascular disease. Endothelial function, as assessed via the flow-mediated dilation test, is attenuated with chronic disease (e.g., type 2 diabetes mellitus, hypertension). Exercise training may mitigate this dysfunction and promote better vascular health. OBJECTIVE The main objective of this umbrella review was to determine the impact of exercise training on flow-mediated dilation in healthy adults and those with chronic disease. METHODS Studies were included if they conducted a systematic review and/or meta-analysis on flow-mediated dilation responses to exercise interventions in adults. Sources were searched in January 2022 and included Scopus, EMBASE, MEDLINE, CINAHL, and Academic Search Premier. National Institutes of Health quality assessment tools were used. The results were presented narratively. RESULTS Twenty-seven systematic reviews, including 19 meta-analyses, (total: 5464 unique participants, 2181 reported unique female individuals) met the inclusion criteria. The average overall quality of included reviews was 8.8/11. The quality of studies within each included review varied from low to moderate using a variety of quality assessment scales. Reviews were conducted in healthy adults (n = 9, meta-analyses = 6), as well as those with type 2 diabetes (n = 5, meta-analyses = 4), cardiovascular conditions [i.e., conditions that impact the cardiovascular system, but excluding samples of only type 2 diabetes] (n = 11, meta-analyses = 7), and other chronic conditions (n = 2, meta-analyses = 2). Overall, the included reviews provided evidence that the type of training to optimally improve FMD may vary based on disease condition. Specifically, the evidence suggests that healthy adults benefitted most from higher intensity aerobic training and/or more frequent low-to-moderate resistance training. In addition, adults with type 2 diabetes benefitted most from low-intensity resistance or aerobic exercise training, whereas those with cardiovascular conditions should consider engaging in high-intensity aerobic training to improve endothelial function. CONCLUSIONS This information may help guide the design of specific exercise programs or recommendations for adults with chronic conditions.
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Affiliation(s)
- Madeline E Shivgulam
- Division of Kinesiology, School of Health and Human Performance, Dalhousie University, Halifax, Nova Scotia, Canada
| | - Haoxuan Liu
- Division of Kinesiology, School of Health and Human Performance, Dalhousie University, Halifax, Nova Scotia, Canada
| | - Beverly D Schwartz
- Division of Kinesiology, School of Health and Human Performance, Dalhousie University, Halifax, Nova Scotia, Canada
| | - Jodi E Langley
- Division of Kinesiology, School of Health and Human Performance, Dalhousie University, Halifax, Nova Scotia, Canada
| | - Nick W Bray
- Cumming School of Medicine, Department of Physiology and Pharmacology, University of Calgary, Calgary, Alberta, Canada
| | - Derek S Kimmerly
- Division of Kinesiology, School of Health and Human Performance, Dalhousie University, Halifax, Nova Scotia, Canada
| | - Myles W O'Brien
- Division of Kinesiology, School of Health and Human Performance, Dalhousie University, Halifax, Nova Scotia, Canada.
- School of Physiotherapy (Faculty of Health) and Department of Medicine (Faculty of Medicine), Dalhousie University, Halifax, Nova Scotia, Canada.
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Sabouri M, Amirshaghaghi F, Hesari MM. High-intensity interval training improves the vascular endothelial function comparing moderate-intensity interval training in overweight or obese adults: A meta-analysis. Clin Nutr ESPEN 2023; 53:100-106. [PMID: 36657899 DOI: 10.1016/j.clnesp.2022.11.023] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/30/2022] [Revised: 11/12/2022] [Accepted: 11/30/2022] [Indexed: 12/12/2022]
Abstract
OBJECTIVE Obesity is associated with endothelial dysfunction and cardiovascular diseases. Moderate-intensity continuous training (MICT) is a common method to improve endothelial function and the cardiovascular risk profile in obesity. However, in recent times, high-intensity interval training (HIIT) has become a popular alternative for MICT primarily because of its time efficiency. Therefore, we hypothesized that HIIT is superior to MICT in improving vascular function. We aimed to evaluate this hypothesis by conducting a meta-analysis and quantifying the effect of HIIT on flow-mediated dilation (FMD) in overweight/obese adults. METHODS Databases (Scopus, Web of Science, and PubMed) were searched up to January 2022 for HIIT vs. moderate-intensity interval training (MICT) and HIIT vs. control (CON) studies on endothelial function assessed by flow-mediated dilation (FMD) in overweight and obese adults. From the included studies, standardized mean difference (SMD) and 95% confidence intervals (95% CIs) were calculated. RESULTS 8 studies with 208 participants were included in this meta-analysis. According to the 6 studies, HIIT improved the FMD with an overall change of %2.6 [(95% CI: 0.82 to 4.377), p = 0.004] compared to the MICT in overweight and obese adults. Moreover, based on the 5 studies that compared HIIT and CON, the results showed HIIT significantly increased FMD by 1.83% [(95% CI: 0.478 to 3.187), p = 0.008]. CONCLUSIONS These results showed that exercise training, particularly HIIT, could improve endothelial function in overweight and obese adults.
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Affiliation(s)
- Mostafa Sabouri
- Department of Exercise Physiology & Health Science, University of Tehran, Tehran, Iran; Department of Nutrition and Integrative Physiology, Florida State University, Tallahassee, FL, USA.
| | | | - Mahsa Mahabadi Hesari
- Department of Exercise Physiology & Health Science, University of Tehran, Tehran, Iran
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Cheng Y, Sun Z, Ya X, Zhou L, Wang M, Wang X, Liu Y. Effect of exercise training on arterial stiffness in obese and overweight children: a meta-analysis. Eur J Pediatr 2022; 181:2633-2642. [PMID: 35499629 DOI: 10.1007/s00431-022-04489-6] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/27/2021] [Revised: 04/25/2022] [Accepted: 04/25/2022] [Indexed: 11/03/2022]
Abstract
The aim of this study was to investigate the effect of exercise training on arterial stiffness in obese and overweight children. Three databases were searched up to July 2021 for papers about exercise training and arterial stiffness in obese and overweight children. The quality of each identified study was evaluated. Effect sizes were estimated in terms of the standardized mean difference. Egger's test and sensitivity analysis were used to assess publication bias. In total, 26 studies by 19 researchers were included in the meta-analysis. Flow-mediated dilatation (FMD), pulse wave velocity (PWV), and intima-media thickness (IMT) were improved after exercise training in obese and overweight children. Subgroup analysis showed that exercise only reduced the PWV and IMT in individuals with a BMI < 30. FMD, PWV, and IMT were improved by exercise training in participants aged below 14 years, but only FMD was increased by exercise in participants aged 14 years and above. All types of training significantly improved FMD. Aerobic exercise (AE) and high-intensity intermittent training (HIIT) reduced the PWV of the participants, but were less effective than resistance training (RT) and aerobic plus resistance training. Only HIIT significantly reduced the IMT. Conclusions: Exercise training improved vascular endothelial function and vascular sclerosis in overweight and obese children, especially in those with a BMI < 30 and younger than 14 years. AE had a more favorable effect on arterial stiffness. What is Known: • Exercise training was a good way to lose weight and subsequently promoted vascular function in overweight and obese children. What is New: • Exercise training was more effective on the vascular endothelial function and vascular sclerosis in overweight and obese children with a BMI<30. • Aerobic exercise had a more favorable effect on arterial stiffness, while the improvement was not effective after resistance training and combined training mode.
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Affiliation(s)
- Yue Cheng
- Department of Physical Education, Jiangsu Normal University, Tongshan District, No.101, Shanghai Road, Xuzhou, Jiangsu Province, 221116, China
| | - Zhenjia Sun
- Department of Physical Education, Jiangsu Normal University, Tongshan District, No.101, Shanghai Road, Xuzhou, Jiangsu Province, 221116, China
| | - Xudong Ya
- Department of Physical Education, Jiangsu Normal University, Tongshan District, No.101, Shanghai Road, Xuzhou, Jiangsu Province, 221116, China
| | - Linlin Zhou
- Department of Physical Education, Jiangsu Normal University, Tongshan District, No.101, Shanghai Road, Xuzhou, Jiangsu Province, 221116, China
| | - Mingxia Wang
- Department of Physical Education, Jiangsu Normal University, Tongshan District, No.101, Shanghai Road, Xuzhou, Jiangsu Province, 221116, China
| | - Xingqi Wang
- Biomedical R&d Center, School of Life Science, Jiangsu Normal University, Xuzhou, Jiangsu Province, 221116, China
| | - Yujia Liu
- Department of Physical Education, Jiangsu Normal University, Tongshan District, No.101, Shanghai Road, Xuzhou, Jiangsu Province, 221116, China.
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Manresa-Rocamora A, Ribeiro F, Casanova-Lizón A, Flatt AA, Sarabia JM, Moya-Ramón M. Cardiac Rehabilitation Improves Endothelial Function in Coronary Artery Disease Patients. Int J Sports Med 2022; 43:905-920. [PMID: 35468652 DOI: 10.1055/a-1717-1798] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/18/2022]
Abstract
Exercise-based cardiac rehabilitation may be an effective non-pharmacological intervention for improving endothelial function in coronary artery disease patients. Therefore, this systematic review with meta-analysis aimed to (a) estimate the training-induced effect on endothelial and vascular smooth muscle function, assessed by flow-mediated dilation and nitroglycerin-mediated dilation, respectively, in coronary artery disease patients; and to (b) study the influence of potential trial-level variables (i. e. study and intervention characteristics) on the training-induced effect on endothelial and vascular smooth muscle function. Electronic searches were performed in Pubmed, Scopus, and Embase up to February 2021. Random-effects models of standardised mean change were estimated. Heterogeneity analyses were performed by using the Chi 2 test and I 2 index. Our results showed that exercise-based cardiac rehabilitation significantly enhanced flow-mediated dilation (1.04 [95% confidence interval=0.76 to 1.31]) but did not significantly change nitroglycerin-mediated dilation (0.05 [95% confidence interval=-0.03 to 0.13]). Heterogeneity testing reached statistical significance (p<.001) with high inconsistency for flow-mediated dilation (I 2 =92%). Nevertheless, none of the analysed variables influenced the training-induced effect on flow-mediated dilation. Exercise-based cardiac rehabilitation seems to be an effective therapeutic strategy for improving endothelial-dependent dilation in coronary artery disease patients, which may aid in the prevention of cardiovascular events.
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Affiliation(s)
- Agustín Manresa-Rocamora
- Sports Research Centre, Department of Sport Sciences, Miguel Hernández University of Elche, 03202 Elche, Spain.,Institute for Health and Biomedical Research (ISABIAL Foundation), Miguel Hernandez University, 03550 Alicante, Spain
| | - Fernando Ribeiro
- School of Health Sciences and Institute of Biomedicine- iBiMED, Universidade de Aveiro, Aveiro, Portugal
| | - Antonio Casanova-Lizón
- Sports Research Centre, Department of Sport Sciences, Miguel Hernández University of Elche, 03202 Elche, Spain
| | - Andrew A Flatt
- Health Sciences and Kinesiology, Georgia Southern University - Armstrong Campus, Savannah, United States
| | - José Manuel Sarabia
- Sports Research Centre, Department of Sport Sciences, Miguel Hernández University of Elche, 03202 Elche, Spain.,Institute for Health and Biomedical Research (ISABIAL Foundation), Miguel Hernandez University, 03550 Alicante, Spain
| | - Manuel Moya-Ramón
- Sports Research Centre, Department of Sport Sciences, Miguel Hernández University of Elche, 03202 Elche, Spain.,Institute for Health and Biomedical Research (ISABIAL Foundation), Miguel Hernandez University, 03550 Alicante, Spain
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Brousseau-Foley M, Blanchette V, Trudeau F, Houle J. Physical Activity Participation in People With an Active Diabetic Foot Ulceration: A Scoping Review. Can J Diabetes 2022; 46:313-327. [PMID: 35568433 DOI: 10.1016/j.jcjd.2021.07.002] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/11/2020] [Revised: 02/22/2021] [Accepted: 07/05/2021] [Indexed: 11/25/2022]
Abstract
BACKGROUND Being physically active on a regular basis has a favourable impact on diabetes-related complications. With the exception of evidence advising individuals with an active diabetic foot ulceration (DFU) to avoid weight-bearing activity, no physical activity (PA) recommendations are currently provided for this population. OBJECTIVE The aim of this scoping review was to examine and map the existing research evidence of PA participation for individuals with an active DFU. DESIGN A scoping review using the Arksey and O'Malley framework was conducted in electronic databases and grey literature from inception to June 2020 to identify publications that investigated individuals with type 1 or type 2 diabetes and an active DFU at enrolment in relation to a PA intervention. Reported outcomes had to inform on effects of PA on any health or wound parameters. RESULTS Nineteen articles from 17 distinct studies met inclusion criteria. Fourteen of the included studies were published in the last 10 years. Types of exercises and materials used, duration of studies, offloading considerations and provision of wound care varied greatly between studies. Included studies are heterogenous in methodological designs and aims, and reporting was often lacking important components of wound care and PA interventions. A discussion based on descriptive statistics and narrative analysis is provided. CONCLUSIONS It is not possible from this scoping review to determine what would be the ideal components of a PA program for this specific population. Conclusions are limited by the quality and design of the included studies. No articles evaluated quality of life, mortality or cardiorespiratory capacity, nor were adverse effects routinely reported.
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Affiliation(s)
- Magali Brousseau-Foley
- Department of Human Kinetics, Université du Québec à Trois-Rivières, Trois-Rivières, Québec, Canada; Centre intégré universitaire de santé et de services sociaux de la Mauricie et du Centre-du-Québec, affiliated with Université de Montréal, Faculty of Medicine, Trois-Rivières, Québec, Canada.
| | - Virginie Blanchette
- Department of Human Kinetics, Université du Québec à Trois-Rivières, Trois-Rivières, Québec, Canada
| | - François Trudeau
- Department of Human Kinetics, Université du Québec à Trois-Rivières, Trois-Rivières, Québec, Canada
| | - Julie Houle
- Department of Nursing, Université du Québec à Trois-Rivières, Trois-Rivières, Québec, Canada
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Hovsepian V, Marandi SM, Esfarjani F, Zavar R, Sadeghi M. The Effect of All Extremity High Intensity Interval Training on Athero-Protective Factors and Endothelial Function in Overweight and Obese Women. Int J Prev Med 2021; 12:141. [PMID: 34912517 PMCID: PMC8631139 DOI: 10.4103/ijpvm.ijpvm_248_19] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/10/2019] [Accepted: 01/23/2020] [Indexed: 12/29/2022] Open
Abstract
Context: Obesity is associated with endothelial dysfunction and cardiovascular diseases. Adiponectin and fibroblast growth factor 21 (FGF21) as hormones are highly contributive in cardiovascular system, while they are disrupted through obesity. Weight-bearing high intensity interval training (HIIT) as an effective procedure in preventing obesity-related complications in adults with obesity may be limited due to the subjects' muscular weakness and complications interfering walking. Aims: The purpose of this study was to assess the effectiveness of non-weight bearing all extremity HIIT (all ex. HIIT) on FGF21, adiponectin, nitric oxide (NO), and flow mediated dilation (FMD) in overweight and obese women. Methods: Thirty healthy overweight and obese sedentary university female students within 20.53 ± 1.50 age range and BMI ≥27 kg.m-2 were assigned in two experimental and control groups. All ex. HIIT consisted of 4 × 4 min at 85–90% max HR with an interspersed with 3 × 3 min recovery per round at 70% max HR by upper and lower ergometers in a simultaneous manner on 10 weeks of four sessions of 40 min each. FGF21, adiponectin, NO, FMD, weight, waist and maximal oxygen uptake (VO2max) were measured in pre and post-tests. Paired sample t-test and analysis of covariance are applied for statistical analysis. Results: Results indicated a significant increase in adiponectin (P ≤ 0.01) and FMD (P ≤ 0.001), while there existed no changes in FGF21 at (P ≥ 0.10) and NO (P ≥ 0.84). The weight and waist decreased at (P ≤ 0.001), and the VO2max increased at (P ≤ 0.001). Conclusions: All ex. HIIT may be a safe alternative for overweigh and obese women who have complications with weight-bearing exercises, and may increase adiponectin, and improve the FMD, aerobic fitness, and body composition.
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Affiliation(s)
- Volga Hovsepian
- Department of Exercise Physiology, Faculty of Physical Education and Sport Sciences, University of Isfahan, Isfahan, Iran
| | - Sayad M Marandi
- Department of Exercise Physiology, Faculty of Physical Education and Sport Sciences, University of Isfahan, Isfahan, Iran
| | - Fahimeh Esfarjani
- Department of Exercise Physiology, Faculty of Physical Education and Sport Sciences, University of Isfahan, Isfahan, Iran
| | - Reihaneh Zavar
- Heart Failure Research Centre, Cardiovascular Research Institute Isfahan University of Medical Sciences, Isfahan, Iran
| | - Masoumeh Sadeghi
- Cardiac Rehabilitation Research Center, Cardiovascular Research Institute, Isfahan Iran, University of Medical Sciences, Isfahan, Iran
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Liu Y, Sun Z, Chen T, Yang C. Does exercise training improve the function of vascular smooth muscle? A systematic review and meta-analysis. Res Sports Med 2021; 30:577-592. [PMID: 33870820 DOI: 10.1080/15438627.2021.1917408] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/21/2022]
Abstract
We aimed to determine the effects of exercise training on the function of vascular smooth muscle cells. PubMed and Web of Science about the effects of exercise training on vascular smooth muscle cells were searched up to August 2020. The effect sizes were estimated in terms of the standardized mean difference. The number of studies included was thirty-five overall. Exercise training had positive effects on vascular smooth muscle cells function in participants older than 40. Effect sizes for HIGH intensity and MIX were positive but small, and also when training duration was longer than 12 weeks. We concluded that vascular smooth muscle cells response can be promoted by exercise training. Vigorous aerobic exercise and mixture training modality were the best ways to promote the dilation response of vascular smooth muscle cells. Additionally, the significant improvement induced by exercise training only occurred when training lasted for longer than 12 weeks.
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Affiliation(s)
- Yujia Liu
- Institute of Physical Education, Jiangsu Normal University, Xuzhou, Jiangsu, China
| | - Zhenjia Sun
- Institute of Physical Education, Jiangsu Normal University, Xuzhou, Jiangsu, China
| | - Tong Chen
- Institute of Physical Education, Jiangsu Normal University, Xuzhou, Jiangsu, China
| | - Chen Yang
- School of Sports and Health, Nanjing Sport Institute, Nanjing, Jiangsu, China
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12
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Takeda Y, Matoba K, Sekiguchi K, Nagai Y, Yokota T, Utsunomiya K, Nishimura R. Endothelial Dysfunction in Diabetes. Biomedicines 2020; 8:E182. [PMID: 32610588 PMCID: PMC7400447 DOI: 10.3390/biomedicines8070182] [Citation(s) in RCA: 43] [Impact Index Per Article: 8.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/25/2020] [Revised: 06/25/2020] [Accepted: 06/26/2020] [Indexed: 12/14/2022] Open
Abstract
Diabetes is a worldwide health issue closely associated with cardiovascular events. Given the pandemic of obesity, the identification of the basic underpinnings of vascular disease is strongly needed. Emerging evidence has suggested that endothelial dysfunction is a critical step in the progression of atherosclerosis. However, how diabetes affects the endothelium is poorly understood. Experimental and clinical studies have illuminated the tight link between insulin resistance and endothelial dysfunction. In addition, macrophage polarization from M2 towards M1 contributes to the process of endothelial damage. The possibility that novel classes of anti-hyperglycemic agents exert beneficial effects on the endothelial function and macrophage polarization has been raised. In this review, we discuss the current status of knowledge regarding the pathological significance of insulin signaling in endothelium. Finally, we summarize recent therapeutic strategies against endothelial dysfunction with an emphasis on macrophage polarity.
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Affiliation(s)
- Yusuke Takeda
- Division of Diabetes, Metabolism, and Endocrinology, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo 105-8461, Japan; (Y.T.); (K.S.); (Y.N.); (T.Y.); (R.N.)
| | - Keiichiro Matoba
- Division of Diabetes, Metabolism, and Endocrinology, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo 105-8461, Japan; (Y.T.); (K.S.); (Y.N.); (T.Y.); (R.N.)
| | - Kensuke Sekiguchi
- Division of Diabetes, Metabolism, and Endocrinology, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo 105-8461, Japan; (Y.T.); (K.S.); (Y.N.); (T.Y.); (R.N.)
| | - Yosuke Nagai
- Division of Diabetes, Metabolism, and Endocrinology, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo 105-8461, Japan; (Y.T.); (K.S.); (Y.N.); (T.Y.); (R.N.)
| | - Tamotsu Yokota
- Division of Diabetes, Metabolism, and Endocrinology, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo 105-8461, Japan; (Y.T.); (K.S.); (Y.N.); (T.Y.); (R.N.)
| | - Kazunori Utsunomiya
- Center for Preventive Medicine, The Jikei University School of Medicine, Tokyo 105-8461, Japan;
| | - Rimei Nishimura
- Division of Diabetes, Metabolism, and Endocrinology, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo 105-8461, Japan; (Y.T.); (K.S.); (Y.N.); (T.Y.); (R.N.)
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13
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Gajanand T, Keating SE, Brown WJ, Hordern MD, Fassett RG, Coombes JS. Comparing the Efficacy of Supervised and Unsupervised Exercise Training on Glycaemic Control in Type 2 Diabetes: A Systematic Review. Curr Diabetes Rev 2020; 16:570-579. [PMID: 30747073 DOI: 10.2174/1573399815666190212120404] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/24/2018] [Revised: 01/19/2019] [Accepted: 02/08/2019] [Indexed: 01/30/2023]
Abstract
BACKGROUND Exercise training is vital for glycaemic control in patients with type 2 diabetes mellitus (T2D). While the positive effects of supervised exercise training are well established, unsupervised training may offer an alternative and more sustainable means of realising the benefits of exercise away from a resource-heavy supervised setting. OBJECTIVE To evaluate the available literature and compare the efficacy of supervised and unsupervised exercise training programs on glycemic control in patients with T2D. METHODS CINAHL, MEDLINE, PubMed, and EMBASE, searched from inception to 20 July 2018. Only studies that included both supervised and unsupervised training were included. RESULTS Four studies, involving 115 participants, were included. One compared supervised with unsupervised exercise training and three investigated the efficacy of unsupervised training following supervised training. While supervised training is effective for improving glycaemic control in patients with T2D, unsupervised training may not maintain these changes. Included studies lacked detail relating to the supervised and unsupervised training programs. CONCLUSIONS Given that exercise is a critical component for maintenance of glycaemic control in patients with T2D, and because unsupervised training has been shown to be effective in improving clinical outcomes in other disease populations, further research is warranted to compare supervised and unsupervised exercise training in patients with T2D. It is important that future studies report standardised and detailed descriptions of key elements that form the basis of supervised and unsupervised exercise training groups.
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Affiliation(s)
- Trishan Gajanand
- School of Human Movement and Nutrition Sciences, University of Queensland, Brisbane, Queensland, Australia
| | - Shelley E Keating
- School of Human Movement and Nutrition Sciences, University of Queensland, Brisbane, Queensland, Australia
| | - Wendy J Brown
- School of Human Movement and Nutrition Sciences, University of Queensland, Brisbane, Queensland, Australia
| | - Matthew D Hordern
- School of Human Movement and Nutrition Sciences, University of Queensland, Brisbane, Queensland, Australia
| | - Robert G Fassett
- School of Human Movement and Nutrition Sciences, University of Queensland, Brisbane, Queensland, Australia
| | - Jeff S Coombes
- School of Human Movement and Nutrition Sciences, University of Queensland, Brisbane, Queensland, Australia
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14
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Effect of Exercise on Risk Factors of Diabetic Foot Ulcers: A Systematic Review and Meta-Analysis. Am J Phys Med Rehabil 2019; 98:103-116. [PMID: 30020090 DOI: 10.1097/phm.0000000000001002] [Citation(s) in RCA: 40] [Impact Index Per Article: 6.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/21/2022]
Abstract
The objectives of this study were to examine the effectiveness of different types of exercise on risk factors of diabetic foot ulcers, including glycated hemoglobin, peripheral arterial disease, and diabetic peripheral neuropathy, in people with type 2 diabetes mellitus. PubMed, Web of Science, Cochrane Library, Scopus, and CINAHL were searched from inception to January 2018 for relevant articles. Eligible studies were randomized controlled trials that examined effects of exercise on the selected risk factors. Twenty randomized controlled trials with 1357 participants were included in the meta-analyses. The differences in postintervention values of glycated hemoglobin and ankle brachial index between exercise and control groups were synthesized, yielding mean differences of -0.45% (P < 0.00001) and 0.03 (P = 0.002), respectively; the differences in within-group changes in glycated hemoglobin were synthesized, yielding mean differences of -0.19% (P = 0.1), -0.25% (P = 0.0006), and -0.64% (P = 0.006) for aerobic versus resistance, combined versus aerobic, and combined versus resistance exercise, respectively. Exercise has a significant effect on reducing glycated hemoglobin, whereas combined exercise is more effective compared with aerobic or resistance exercise alone. Exercise also improves ankle brachial index. However, evidence regarding the association between exercise and peripheral neuropathy and risks of diabetic foot ulcers in people with type 2 diabetes mellitus remains insufficient.
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15
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Dos Santos Araujo JE, Nunes Macedo F, Sales Barreto A, Viana Dos Santos MR, Antoniolli AR, Quintans-Junior LJ. Effects of Resistance and Combined training on Vascular Function in Type 2 Diabetes: A Systematic Review of Randomized Controlled Trials. Rev Diabet Stud 2019; 15:16-25. [PMID: 31132077 DOI: 10.1900/rds.2019.15.16] [Citation(s) in RCA: 12] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/09/2023] Open
Abstract
BACKGROUND Cardiovascular disease (CVD) is the main cause of mortality in type 2 diabetes (T2D). Exercise can reduce the risk factors associated with CVD in T2D patients. However, research evaluating its beneficial effects in these patients has used different measurement protocols and types of exercise, complicating comparison. AIM To assess the effects of resistance training (RT) and combined training (CT) on the vascular function of T2D patients. METHODS A database search (MEDLINE, Scopus, and Web of Science) was performed to identify relevant articles that were published up to August 2017. Only original studies evaluating the effects of RT or CT interventions on vascular function in T2D patients were included. The articles were reviewed independently by at least three reviewers. The Cochrane guidelines were used to assess the methodological quality of the studies. Fourteen studies were finally included. Two studies only used RT and twelve studies used CT as intervention strategy. RESULTS AND CONCLUSIONS The results show that resistance training is a useful means for primary treatment of vascular diseases and maintenance of vascular function in T2D patients. However, more studies are necessary to gain full knowledge of the beneficial effects and to identify tailored exercise plans to optimize these benefits. The information provided in this review may help to improve current treatment of vascular diseases in T2D patients and to design future studies.
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Affiliation(s)
- João E Dos Santos Araujo
- Laboratory of Cardiovascular Pharmacology, Department of Physiology, Federal University of Sergipe, Sergipe, Brazil
| | - Fabrício Nunes Macedo
- Laboratory of Cardiovascular Pharmacology, Department of Physiology, Federal University of Sergipe, Sergipe, Brazil
| | - André Sales Barreto
- Laboratory of Cardiovascular Pharmacology, Department of Physiology, Federal University of Sergipe, Sergipe, Brazil
| | - Márcio R Viana Dos Santos
- Laboratory of Cardiovascular Pharmacology, Department of Physiology, Federal University of Sergipe, Sergipe, Brazil
| | - Angelo R Antoniolli
- Laboratory of Neurosciences and Pharmacological Trials, Department of Physiology, Federal University of Sergipe, Sergipe, Brazi
| | - Lucindo J Quintans-Junior
- Laboratory of Neurosciences and Pharmacological Trials, Department of Physiology, Federal University of Sergipe, Sergipe, Brazil
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16
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Kemps H, Kränkel N, Dörr M, Moholdt T, Wilhelm M, Paneni F, Serratosa L, Ekker Solberg E, Hansen D, Halle M, Guazzi M. Exercise training for patients with type 2 diabetes and cardiovascular disease: What to pursue and how to do it. A Position Paper of the European Association of Preventive Cardiology (EAPC). Eur J Prev Cardiol 2019; 26:709-727. [PMID: 30642190 DOI: 10.1177/2047487318820420] [Citation(s) in RCA: 68] [Impact Index Per Article: 11.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/11/2022]
Abstract
Patients with type 2 diabetes mellitus suffer from dysregulation of a plethora of cardiovascular and metabolic functions, including dysglycaemia, dyslipidaemia, arterial hypertension, obesity and a reduced cardiorespiratory fitness. Exercise training has the potential to improve many of these functions, such as insulin sensitivity, lipid profile, vascular reactivity and cardiorespiratory fitness, particularly in type 2 diabetes mellitus patients with cardiovascular comorbidities, such as patients that suffered from an acute myocardial infarction, or after a coronary intervention such as percutaneous coronary intervention or coronary artery bypass grafting. The present position paper aims to provide recommendations for prescription of exercise training in patients with both type 2 diabetes mellitus and cardiovascular disease. The first part discusses the relevance and practical applicability of treatment targets that may be pursued, and failure to respond to these targets. The second part provides recommendations on the contents and methods to prescribe exercise training tailored to these treatment targets as well as to an optimal preparation and dealing with barriers and risks specific to type 2 diabetes mellitus and cardiac comorbidity.
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Affiliation(s)
- Hareld Kemps
- 1 Department of Cardiology, Máxima Medical Centre, Veldhoven, The Netherlands
| | - Nicolle Kränkel
- 2 Charité - Universitätsmedizin Berlin, Klinik für Kardiologie, Campus Benjamin Steglitz, Germany.,3 DZHK (German Centre for Cardiovascular Research), partner site Berlin, Germany
| | - Marcus Dörr
- 4 University Medicine Greifswald, Department of Internal Medicine B, Germany.,5 DZHK (German Centre for Cardiovascular Research), partner site Greifswald, Germany
| | - Trine Moholdt
- 6 Department of Circulation and Medical Imaging, Norwegian University of Science and Technology Trondheim, Norway.,7 St Olav's Hospital, Trondheim, Norway
| | - Matthias Wilhelm
- 8 Department of Cardiology, Bern University Hospital and University of Bern, Switzerland
| | - Francesco Paneni
- 9 Centre for Molecular Cardiology and Cardiology, Zurich University Hospital, University of Zurich, Switzerland
| | - Luis Serratosa
- 10 Hospital Universitario Quironsalud, Madrid, Spain.,11 Ripoll & De Prado Sport Clinic, FIFA Medical Centre of Excellence, Murcia, Spain
| | | | - Dominique Hansen
- 13 Hasselt University, Faculty of Rehabilitation Sciences, Diepenbeek, Belgium.,14 Heart Centre Hasselt, Jessa Hospital, Belgium
| | - Martin Halle
- 15 Technical University Munich, Department of Prevention, Rehabilitation and Sports Medicine, Germany.,16 DZHK (German Centre for Cardiovascular Research), partner site Munich, Germany
| | - Marco Guazzi
- 17 University Cardiology Department and Heart Failure Unit and Cardiopulmonary Laboratory, Cardiology, I.R.C.C.S., Milan, Italy.,18 Policlinico San Donato University Hospital, Milan, Italy
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17
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Byrne H, Caulfield B, De Vito G. Effects of Self-directed Exercise Programmes on Individuals with Type 2 Diabetes Mellitus: A Systematic Review Evaluating Their Effect on HbA 1c and Other Metabolic Outcomes, Physical Characteristics, Cardiorespiratory Fitness and Functional Outcomes. Sports Med 2018; 47:717-733. [PMID: 27459860 DOI: 10.1007/s40279-016-0593-y] [Citation(s) in RCA: 24] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/21/2023]
Abstract
BACKGROUND Type two diabetes mellitus (T2DM) is caused and progressed by an individual's lifestyle and, therefore, its optimal day-to-day management may involve the patient taking responsibility for this, including fulfilling a planned and prescribed exercise regime used as part of the treatment. A prescription of exercise designed to meet a patient's individual needs with minimal supervision from healthcare practitioners would facilitate this. However, the optimal prescription of exercise in the population remains unclear. OBJECTIVE This review examines the effects planned self-directed exercise has on glycosylated haemoglobin and other outcomes in individuals with T2DM and aims to identify the most suitable forms of planned self-directed exercise for individuals with T2DM that can be carried out independently. METHODS A search of the electronic databases PubMed, SPORTDiscus, CINAHL, EMBASE, Cochrane (Trials) and ClinicalTrials.gov was conducted along with reference lists of previous reviews. Randomised controlled trials published in English between January 1990 and February 2015 examining participants diagnosed with T2DM only were included. Studies were critically appraised using the PEDro (Physiotherapy Evidence Database) scale and data were presented on standardised tables. RESULTS Twenty-eight articles that used five element gymnastics, a games console exercise intervention (Wii fit plus) or aerobic, resistance or combined training were included. CONCLUSION This review comprehensively summarised the effects planned self-directed exercise interventions had on individuals with T2DM. The review found that self-directed exercise was found to be beneficial for individuals with T2DM for improving glycosylated haemoglobin, physical characteristics, cardiorespiratory fitness, functional measures and other metabolic outcomes.
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Affiliation(s)
- Hugh Byrne
- The Insight Centre for Data Analytics, O'Brien Centre for Science, University College Dublin, Science Centre East, Belfield, Dublin 4, Ireland. .,UCD School of Public Health, Physiotherapy and Sports Science, Belfield, Dublin, Ireland.
| | - Brian Caulfield
- The Insight Centre for Data Analytics, O'Brien Centre for Science, University College Dublin, Science Centre East, Belfield, Dublin 4, Ireland.,UCD School of Public Health, Physiotherapy and Sports Science, Belfield, Dublin, Ireland
| | - Giuseppe De Vito
- The Insight Centre for Data Analytics, O'Brien Centre for Science, University College Dublin, Science Centre East, Belfield, Dublin 4, Ireland.,UCD School of Public Health, Physiotherapy and Sports Science, Belfield, Dublin, Ireland
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18
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Qiu S, Cai X, Yin H, Sun Z, Zügel M, Steinacker JM, Schumann U. Exercise training and endothelial function in patients with type 2 diabetes: a meta-analysis. Cardiovasc Diabetol 2018; 17:64. [PMID: 29720185 PMCID: PMC5930739 DOI: 10.1186/s12933-018-0711-2] [Citation(s) in RCA: 109] [Impact Index Per Article: 15.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/07/2018] [Accepted: 04/25/2018] [Indexed: 12/22/2022] Open
Abstract
BACKGROUND AND AIMS Exercise training is considered a cornerstone in the management of type 2 diabetes, which is associated with impaired endothelial function. However, the association of exercise training with endothelial function in type 2 diabetes patients has not been fully understood. This meta-analysis aimed to investigate their associations with focus on exercise types. METHODS Databases were searched up to January 2018 for studies evaluating the influences of exercise training with durations ≥ 8 weeks on endothelial function assessed by flow-mediated dilation (FMD) among type 2 diabetes patients or between type 2 diabetics and non-diabetics. Data were pooled using random-effects models to obtain the weighted mean differences (WMDs) and 95% confidence intervals (CIs). RESULTS Sixteen databases were included. Exercise training resulted in an overall improvement in FMD by 1.77% (95% CI 0.94-2.59%) in type 2 diabetes patients. Specifically, both aerobic and combined aerobic and resistance exercise increased FMD by 1.21% (95% CI 0.23-2.19%) and 2.49% (95% CI 1.17-3.81%), respectively; but resistance exercise only showed a trend. High-intensity interval aerobic exercise did not significantly improve FMD over moderate-intensity continuous exercise. Notably, the improvement in FMD among type 2 diabetes patients was smaller compared with non-diabetics in response to exercise training (WMD - 0.72%, 95% CI - 1.36 to - 0.08%) or specifically to aerobic exercise (WMD - 0.65%, 95% CI - 1.31 to 0.01%). CONCLUSIONS Exercise training, in particular aerobic and combined exercise, improves endothelial function in type 2 diabetes patients, but such an improvement appears to be weakened compared with non-diabetics. Trial registration PROSPERO CRD42018087376.
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Affiliation(s)
- Shanhu Qiu
- Department of Endocrinology, Zhongda Hospital, Institute of Diabetes, School of Medicine, Southeast University, Nanjing, People's Republic of China
| | - Xue Cai
- Department of Endocrinology, Zhongda Hospital, Institute of Diabetes, School of Medicine, Southeast University, Nanjing, People's Republic of China
| | - Han Yin
- Department of Endocrinology, Zhongda Hospital, Institute of Diabetes, School of Medicine, Southeast University, Nanjing, People's Republic of China
| | - Zilin Sun
- Department of Endocrinology, Zhongda Hospital, Institute of Diabetes, School of Medicine, Southeast University, Nanjing, People's Republic of China.
| | - Martina Zügel
- Division of Sports and Rehabilitation Medicine, Ulm University Medical Center, Ulm, Germany
| | | | - Uwe Schumann
- Division of Sports and Rehabilitation Medicine, Ulm University Medical Center, Ulm, Germany
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19
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Rahbar S, Naimi SS, RezaSoltani A, Rahimi A, Baghban AA, Noori A, Rashedi V. Changes in vascular structure in diabetic patients after 8 weeks aerobic physical exercise: a randomized controlled trial. Int J Diabetes Dev Ctries 2018; 38:202-208. [DOI: 10.1007/s13410-017-0579-9] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/27/2022] Open
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20
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Novaković M, Prokšelj K, Rajkovič U, Vižintin Cuderman T, Janša Trontelj K, Fras Z, Jug B. Exercise training in adults with repaired tetralogy of Fallot: A randomized controlled pilot study of continuous versus interval training. Int J Cardiol 2018; 255:37-44. [DOI: 10.1016/j.ijcard.2017.12.105] [Citation(s) in RCA: 19] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/11/2017] [Revised: 10/28/2017] [Accepted: 12/27/2017] [Indexed: 01/28/2023]
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21
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Wijkman MO, Sandberg K, Kleist M, Falk L, Enthoven P. The exaggerated blood pressure response to exercise in the sub-acute phase after stroke is not affected by aerobic exercise. J Clin Hypertens (Greenwich) 2018; 20:56-64. [DOI: 10.1111/jch.13157] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/30/2017] [Revised: 09/03/2017] [Accepted: 09/22/2017] [Indexed: 11/28/2022]
Affiliation(s)
- Magnus O. Wijkman
- Departments of Internal Medicine and Medical and Health Sciences; Linkopings Universitet; Norrkoping Sweden
| | - Klas Sandberg
- Departments of Internal Medicine and Medical and Health Sciences; Linkopings Universitet; Norrkoping Sweden
- Departments of Rehabilitation and Medical and Health Sciences; Linkopings Universitet; Norrkoping Sweden
| | - Marie Kleist
- Departments of Rehabilitation and Medical and Health Sciences; Linkopings Universitet; Norrkoping Sweden
| | - Lars Falk
- Research and Development Unit of Local Health Care; Department of Medical and Health Sciences; Linkopings Universitet; Linkoping Sweden
- Department of Clinical and Experimental Medicine; Linkopings Universitet; Linkoping Sweden
- Department of Dermatology and Venereology; Linkopings Universitet; Linkoping Sweden
| | - Paul Enthoven
- Research and Development Unit of Local Health Care; Department of Medical and Health Sciences; Linkopings Universitet; Linkoping Sweden
- Department of Medical and Health Sciences; Linkopings Universitet; Linkoping Sweden
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22
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Lee JH, Lee R, Hwang MH, Hamilton MT, Park Y. The effects of exercise on vascular endothelial function in type 2 diabetes: a systematic review and meta-analysis. Diabetol Metab Syndr 2018; 10:15. [PMID: 29541164 PMCID: PMC5840787 DOI: 10.1186/s13098-018-0316-7] [Citation(s) in RCA: 44] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/22/2023] Open
Abstract
BACKGROUND Vascular endothelial dysfunction induced by hyperglycemia and elevated insulin resistance is a potent risk factor for cardiovascular disease and likely contributes to multiple chronic disease complications associated with aging. The aim of this study was to systematically review and quantify the effects of exercise on endothelial function (EF) in type 2 diabetes (T2D). METHODS Five electronic databases were searched (until June 2017) for studies that met the following criteria: (i) randomized controlled trials; (ii) T2D aged ≥ 18 years; (iii) measured EF by brachial artery flow-mediated dilation (FMD); (iv) structured and supervised exercise intervention for ≥ 8 weeks. RESULTS Thirteen cohorts, selected from eight studies (306 patients, average age 59 years), met the inclusion criteria. Exercise training significantly increased FMD (mean ES = 0.41, 95% CI 0.21-0.62, P < 0.001). Low to moderate intensity subgroups and aerobic exercise (AE) subgroups significantly increased FMD more than moderate to high intensity subgroups and combined AE and resistance exercise subgroups respectively (P < 0.01, P < 0.05). The Grading of Recommendations Assessment, Development and Evaluation (GRADE) assessments reported that quality of evidence for all outcomes was moderate except shear rate showing low. Egger's test showed no significant publication bias for all outcomes. CONCLUSION Our results suggest that in patients with T2D, lower intensity exercise has physiological meaningful effects on EF, in support of the emerging concept that the lower efforts of exercise are not necessarily less cardioprotective than higher intensity training.
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Affiliation(s)
- Jung-Hoon Lee
- Laboratory of Human Physiology, Korea National Sport University, Seoul, Republic of Korea
| | - Ruda Lee
- Exercise & Cardiovascular Physiology Laboratory, Division of Health and Exercise Science, Incheon National University, Incheon, Republic of Korea
- Sport Science Institute, Incheon National University, Incheon, Republic of Korea
| | - Moon-Hyon Hwang
- Exercise & Cardiovascular Physiology Laboratory, Division of Health and Exercise Science, Incheon National University, Incheon, Republic of Korea
- Sport Science Institute, Incheon National University, Incheon, Republic of Korea
| | - Marc T. Hamilton
- Texas Obesity Research Center from the Division of Research, and Department of Health and Human Performance, University of Houston, Houston, TX USA
| | - Yoonjung Park
- Laboratory of Integrated Physiology, Department of Health and Human Performance, University of Houston, 3875 Holman St, Houston, TX 77204-6015 USA
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Abstract
PURPOSE Flow-mediated dilation, a barometer of cardiovascular (CV) health, is reported to increase with exercise training (ET); however, the potential moderating factors of ET are not clear to date. The purpose of this study was to determine the effect of ET assessed by brachial artery flow-mediated dilation (BAFMD). METHODS Authors searched PubMed between January 1999 and December 2013, bibliographies, and reviews to identify studies examining ET and BAFMD. Two independent reviewers extracted quality, descriptive, exercise, and outcome data of eligible studies. Data were presented as weighted effect sizes (ESs) and 95% confidence limits. RESULTS Analysis included 66 studies reporting BAFMD data (1865 ET and 635 control subjects). Overall, ET had significant improvements in BAFMD compared with controls (P < .0001). Exercise training at higher ET intensities resulted in a greater increase in BAFMD (9.29; 95% CI, 5.09-13.47) than lower ET intensities (3.63; 95% CI, -0.56 to 7.83) or control (-0.42; 95% CI, -2.06 to 1.21). Subjects whose ET duration was ≥150 min/wk (11.33; 95% CI, 7.15-15.51) had a significant improvement in BAFMD compared with those with <150 min/wk (4.79; 95% CI, 3.08-6.51) or control (-0.30; 95% CI, -1.99 to 1.39). Age (P = .11) and baseline artery diameter (P = .31) did not modify the BAFMD response to ET. CONCLUSION Exercise training contributes to a significant increase in BAFMD. These results provide indirect evidence that ET alters a well-known factor associated with the primary and secondary prevention of CV diseases. Exercise training interventions, including greater intensity and duration, may optimize the increase in BAFMD.
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The Impact of Burst Exercise on Cardiometabolic Status of Patients Newly Diagnosed With Type 2 Diabetes. Can J Cardiol 2017; 33:1645-1651. [PMID: 29173604 DOI: 10.1016/j.cjca.2017.09.019] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/25/2017] [Revised: 08/31/2017] [Accepted: 09/19/2017] [Indexed: 01/19/2023] Open
Abstract
BACKGROUND The impact of burst high-intensity exercise on physiological, cardiometabolic, and biochemical variables compared with traditional moderate-intensity continuous exercise training (MICT) has yet to be assessed in patients with type 2 diabetes (T2D). We compared the impact of multiple short-duration, high-intensity burst exercise sessions to MICT on cardiometabolic variables in patients with T2D. METHODS Forty newly diagnosed patients with T2D not receiving lipid lowering or hypoglycemic medications were randomized to 40 minutes of MICT (60% of maximal heart rate) 5 days per week or 3 continuous bursts of 12 minutes of high-intensity exercise (85% of maximal heart rate) 5 days per week for 3 months. Body mass index, hemoglobin A1C (HbA1C), and lipid profile were assessed before and after 3 months of exercise training. RESULTS Burst exercise resulted in greater body mass index reduction than did MICT (-2.1 ± 1.2 kg/m2 vs -0.7 ± 0.7 kg/m2, respectively; P < 0.05). There was a greater reduction at 3 months (P < 0.05) in HbA1C levels in the burst exercise group (8.14% ± 0.49% to 7.32% ± 0.39%) compared with the MICT group (8.18% ± 0.35% to 7.94% ± 0.41%). Compared with MICT, burst exercise was associated with a greater reduction in low-density lipoprotein cholesterol (-11 vs -4%; P < 0.05) and a greater increase in high-density lipoprotein cholesterol (22% vs 3%; all P < 0.05). After 3 months, patients in the burst exercise group attained greater exercise time on the treadmill (exercise capacity) than did those prescribed MICT (6.87 ± 1.44 minutes vs 5.40 ± 1.96 minutes; P < 0.001). CONCLUSIONS Findings from the current study support better cardiometabolic benefits of burst exercise compared with MICT over 3 months in patients with newly diagnosed T2D.
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The influence of prenatal exercise and pre-eclampsia on maternal vascular function. Clin Sci (Lond) 2017; 131:2223-2240. [PMID: 28798074 DOI: 10.1042/cs20171036] [Citation(s) in RCA: 27] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/10/2017] [Revised: 07/03/2017] [Accepted: 07/06/2017] [Indexed: 01/10/2023]
Abstract
During healthy pregnancy, the cardiovascular system undergoes diverse adaptations to support adequate transfer of oxygen and nutrients from mother to fetus. In order to accommodate the large expansion of blood volume and associated cardiac output, the structure, mechanics, and function of the arteries are altered. Specifically, in healthy pregnancy there is a remodeling of arteries (increased angiogenesis and vasodilation), a generalized reduction in arterial stiffness (increased compliance), and an enhanced endothelial function. The development of pregnancy complications, specifically pre-eclampsia, is associated with poor placentation (decreased angiogenesis), increased arterial stiffness, and vascular dysfunction (reduced endothelial function). Many of the positive adaptations that occur in healthy pregnancy are enhanced in response to chronic exercise. Specifically, placental angiogenesis and endothelial function have been shown to improve to a greater extent in women who are active during their pregnancy compared with those who are not. Prenatal exercise may be important in helping to reduce the risk of vascular dysfunction in pregnancy. However, our knowledge of the vascular adaptations resulting from maternal exercise is limited. This review highlights maternal vascular adaptations occurring during healthy pregnancy, and contrasts the vascular maladaptation associated with pre-eclampsia. Finally, we discuss the role of prenatal exercise on vascular function in the potential prevention of vascular complications associated with pre-eclampsia.
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Physical Exercise on Inflammatory Markers in Type 2 Diabetes Patients: A Systematic Review of Randomized Controlled Trials. OXIDATIVE MEDICINE AND CELLULAR LONGEVITY 2017; 2017:8523728. [PMID: 28400914 PMCID: PMC5376457 DOI: 10.1155/2017/8523728] [Citation(s) in RCA: 27] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 10/15/2016] [Revised: 12/07/2016] [Accepted: 02/23/2017] [Indexed: 01/26/2023]
Abstract
Background. Type 2 diabetes mellitus (T2DM) is a serious disease associated with high morbidity and mortality. Scientific findings showed that physical exercise is an option for treatment of these patients. This study's objective is to investigate the effects of supervised aerobic and/or resistance physical training on inflammatory markers in subjects with T2DM. Methods. A systematic review was conducted on four databases, MEDLINE, CENTRAL, LILACS, and Scopus, and manual search from 21 to 30 November 2016. Randomized clinical trials involving individuals diagnosed with T2DM, who have undergone supervised training protocols, were selected in this study. Results. Eleven studies were included. Studies that evaluated control group versus aerobic exercise reported controversial results about the effectiveness of physical training in modifying C-reactive protein (CRP) and cytokine levels. The only variable analyzed by the six studies in comparison to the control group versus resistance exercise was CRP. This protein showed no significant difference between groups. Between the two modes of exercise (aerobic and resistance), only one study demonstrated that aerobic exercise was more effective in reducing CRP. Conclusion. The evidence was insufficient to prove that aerobic or resistance exercise improves systemic levels of inflammatory markers in patients with T2DM.
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Byrkjeland R, Njerve IU, Arnesen H, Seljeflot I, Solheim S. Reduced endothelial activation after exercise is associated with improved HbA 1c in patients with type 2 diabetes and coronary artery disease. Diab Vasc Dis Res 2017; 14:94-103. [PMID: 28111980 DOI: 10.1177/1479164116679077] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/21/2022] Open
Abstract
OBJECTIVE We have previously reported insignificant changes in HbA1c after exercise in patients with both type 2 diabetes and coronary artery disease. In this study, we investigated the effect of exercise on endothelial function and possible associations between changes in endothelial function and HbA1c. METHODS Patients with type 2 diabetes and coronary artery disease ( n = 137) were randomised to 12 months exercise or standard follow-up. Endothelial function was assessed by circulating biomarkers (E-selectin, intercellular adhesion molecule-1, vascular cell adhesion molecule-1, von Willebrand factor, tissue plasminogen activator antigen, asymmetric dimethylarginine and L-arginine/asymmetric dimethylarginine ratio). Differences between the randomised groups were analysed by analysis of covariance and correlations by Spearman's rho or Pearson's correlation. RESULTS No effect of exercise on endothelial function was demonstrated. The changes in HbA1c in the exercise group correlated with changes in E-selectin ( r = 0.56, p < 0.001), intercellular adhesion molecule-1 ( r = 0.27, p = 0.052), vascular cell adhesion molecule-1 ( r = 0.32, p = 0.022) and tissue plasminogen activator antigen ( r = 0.35, p = 0.011). HbA1c decreased significantly more in patients with versus without a concomitant reduction in E-selectin ( p = 0.002), intercellular adhesion molecule-1 ( p = 0.011), vascular cell adhesion molecule-1 ( p = 0.028) and tissue plasminogen activator antigen ( p = 0.009). CONCLUSION Exercise did not affect biomarkers of endothelial function in patients with both type 2 diabetes and coronary artery disease. However, changes in biomarkers of endothelial activation correlated with changes in HbA1c, and reduced endothelial activation was associated with improved HbA1c after exercise.
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Affiliation(s)
- Rune Byrkjeland
- 1 Center for Clinical Heart Research (CCHR), Department of Cardiology, Oslo University Hospital, Ullevål, Oslo, Norway
- 2 Center for Heart Failure Research, Oslo University Hospital, Oslo, Norway
- 3 Faculty of Medicine, University of Oslo, Oslo, Norway
| | - Ida U Njerve
- 1 Center for Clinical Heart Research (CCHR), Department of Cardiology, Oslo University Hospital, Ullevål, Oslo, Norway
- 2 Center for Heart Failure Research, Oslo University Hospital, Oslo, Norway
- 3 Faculty of Medicine, University of Oslo, Oslo, Norway
| | - Harald Arnesen
- 1 Center for Clinical Heart Research (CCHR), Department of Cardiology, Oslo University Hospital, Ullevål, Oslo, Norway
- 2 Center for Heart Failure Research, Oslo University Hospital, Oslo, Norway
- 3 Faculty of Medicine, University of Oslo, Oslo, Norway
| | - Ingebjørg Seljeflot
- 1 Center for Clinical Heart Research (CCHR), Department of Cardiology, Oslo University Hospital, Ullevål, Oslo, Norway
- 2 Center for Heart Failure Research, Oslo University Hospital, Oslo, Norway
- 3 Faculty of Medicine, University of Oslo, Oslo, Norway
| | - Svein Solheim
- 1 Center for Clinical Heart Research (CCHR), Department of Cardiology, Oslo University Hospital, Ullevål, Oslo, Norway
- 2 Center for Heart Failure Research, Oslo University Hospital, Oslo, Norway
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Pearson MJ, Smart NA. Effect of exercise training on endothelial function in heart failure patients: A systematic review meta-analysis. Int J Cardiol 2016; 231:234-243. [PMID: 28089145 DOI: 10.1016/j.ijcard.2016.12.145] [Citation(s) in RCA: 82] [Impact Index Per Article: 9.1] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/20/2016] [Revised: 11/23/2016] [Accepted: 12/20/2016] [Indexed: 12/20/2022]
Abstract
OBJECTIVE Endothelial dysfunction contributes to the development and progression of cardiovascular disease and heart failure (HF) and is associated with an increased risk of mortality. Flow-mediated dilation (FMD) is widely utilised to assess endothelial function and is improved with exercise training in heart failure patients. The aim of this meta-analysis is to quantify the effect of exercise training in patients with heart failure. BACKGROUND A large number of studies now exist that have examined endothelial function in patients with heart failure. We sought to add to the current literature by quantifying the effect of exercise training on endothelial function. METHODS We conducted database searches (PubMed, EMBASE, PROQUEST and Cochrane Trials Register to June 2016) for exercise based rehabilitation trials in heart failure, using search terms exercise training, endothelial function, flow-mediated dilation (FMD) and endothelial progenitor cells (EPCs). RESULTS The 16 included studies provided a total of 529 participants, 293 in an intervention and 236 in controls groups. FMD was improved with exercise training in exercise vs. control, SMD of 1.08 (95%CI 0.70 to 1.46, p<0.00001). CONCLUSION Overall exercise training improved endothelial function, assessed via FMD, and endothelial progenitor cells in heart failure patients.
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Affiliation(s)
- M J Pearson
- School of Science and Technology, University of New England, Armidale, NSW 2351, Australia
| | - N A Smart
- School of Science and Technology, University of New England, Armidale, NSW 2351, Australia.
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Abstract
The objectives of this study were (1) to examine the prevalence of diabetes and hypertension among church personnel in North-Eastern Democratic Republic of Congo, and (2) to identify socio-demographic factors and health behaviors that are associated with these outcomes. Data for this study were obtained from a sample of 670 pastors and their wives, and other church workers in North-Eastern Congo in 2014/2015. Pearson chi square and binary logistic regression analyses were conducted with diabetes status and hypertension as outcome variables. A little over one in ten respondents (11.3 %; n = 76) were diabetic. Of the 76 respondents with diabetes, 49, or approximately two-thirds (64 %) were aged 50 and over. Of the respondents aged 70 and above, 85.5 % were found to be hypertensive. Adjusting for all other predictors, respondents who were older, market women/homemakers, and those who used vehicles as opposed to walking or biking as their means of transport were more likely to be diabetic. Also, respondents who were older or overweight were more likely to have hypertension. The paper discusses the results and their implication for public health policy on diabetes prevention, particularly among older individuals who are religious workers in Africa.
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Hwang MH, Lee S. Insulin resistance: vascular function and exercise. Integr Med Res 2016; 5:198-203. [PMID: 28462118 PMCID: PMC5390417 DOI: 10.1016/j.imr.2016.06.001] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/12/2016] [Revised: 05/30/2016] [Accepted: 06/02/2016] [Indexed: 12/19/2022] Open
Abstract
Insulin resistance associated with metabolic syndrome and Type 2 diabetes mellitus is an epidemic metabolic disorder, which increases the risk of cardiovascular complications. Impaired vascular endothelial function is an early marker for atherosclerosis, which causes cardiovascular complications. Both experimental and clinical studies indicate that endothelial dysfunction in vasculatures occurs with insulin resistance. The associated physiological mechanisms are not fully appreciated yet, however, it seems that augmented oxidative stress, a physiological imbalance between oxidants and antioxidants, in vascular cells is a possible mechanism involved in various vascular beds with insulin resistance and hyperglycemia. Regardless of the inclusion of resistance exercise, aerobic exercise seems to be beneficial for vascular endothelial function in both large conduit and small resistance vessels in both clinical and experimental studies with insulin resistance. In clinical cases, aerobic exercise over 8 weeks with higher intensity seems more beneficial than the cases with shorter duration and lower intensity. However, more studies are needed in the future to elucidate the physiological mechanisms by which vascular endothelial function is impaired in insulin resistance and improved with aerobic exercise.
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Affiliation(s)
- Moon-Hyon Hwang
- Division of Health and Exercise Science, Incheon National University, Incheon, Korea.,Sport Science Institute, Incheon National University, Incheon, Korea
| | - Sewon Lee
- Sport Science Institute, Incheon National University, Incheon, Korea.,Division of Sport Science, Incheon National University, Incheon, Korea
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Abstract
Progress in the modification of conventional coronary risk factors and lifestyle behavior has reduced the incidence of atherosclerotic coronary artery disease; nonetheless, it continues to be the leading cause of mortality in the world. This might be attributed to the defective risk stratifying and prevention strategy for coronary artery disease. In the current clinical setting, atherosclerotic coronary artery disease risk is estimated on the basis of identifying and quantifying only traditional risk factors; it does not take into consideration nontraditional risk factors. In addition, most of the prevailing therapies for atherosclerosis are targeted toward traditional risk factors rather than atherosclerosis itself. It is desirable to develop a method that can directly assess the activity of atherogenesis at every moment. Endothelial function is an integrated index of all atherogenic and atheroprotective factors present in an individual including nontraditional factors and heretofore unknown factors, and it is reported to have additional predictive value for future cardiovascular events to traditional risk factors. Moreover, endothelial function has a pivotal role in all phases of atherosclerosis, from initiation to atherothrombotic complication, and is reversible at every phase, indicating that endothelial function-guided therapies might be effective and feasible in cardiovascular practice. Thus, the introduction of endothelial function testing into clinical practice might enable us to innovate individualized cardiovascular medicine. In this review, we summarize the current knowledge on the contribution of endothelial dysfunction to atherogenesis and review the methods that assess endothelial function. Finally, we focus on the effects of major antiatherosclerotic disease therapies on endothelial function and argue the possibility of noninvasive assessment of endothelial function aiming at individualized cardiovascular medicine.
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Rodríguez-Núñez I, Romero F, Saavedra MJ. [Exercise-induced shear stress: Physiological basis and clinical impact]. ARCHIVOS DE CARDIOLOGIA DE MEXICO 2016; 86:244-54. [PMID: 27118039 DOI: 10.1016/j.acmx.2016.03.001] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/16/2015] [Revised: 02/10/2016] [Accepted: 03/17/2016] [Indexed: 11/30/2022] Open
Abstract
The physiological regulation of vascular function is essential for cardiovascular health and depends on adequate control of molecular mechanisms triggered by endothelial cells in response to mechanical and chemical stimuli induced by blood flow. Endothelial dysfunction is one of the major risk factors for cardiovascular disease, where an imbalance between synthesis of vasodilator and vasoconstrictor molecules is one of its main mechanisms. In this context, the shear stress is one of the most important mechanical stimuli to improve vascular function, due to endothelial mechanotransduction, triggered by stimulation of various endothelial mechanosensors, induce signaling pathways culminating in increased bioavailability of vasodilators molecules such as nitric oxide, that finally trigger the angiogenic mechanisms. These mechanisms allow providing the physiological basis for the effects of exercise on vascular health. In this review it is discussed the molecular mechanisms involved in the vascular response induced by shear stress and its impact in reversing vascular injury associated with the most prevalent cardiovascular disease in our population.
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Affiliation(s)
- Iván Rodríguez-Núñez
- Laboratorio de Biología del Ejercicio, Escuela de Kinesiología, Facultad de Ciencias de la Salud, Universidad San Sebastián, Concepción, Chile; Carrera de Kinesiología, Facultad de Salud, Universidad Santo Tomás, Concepción, Chile; Programa de Doctorado en Ciencias Médicas, Facultad de Medicina, Universidad de la Frontera. Laboratorio de Neurociencia y Biología de péptidos CEBIOR-CEGIN BIOREN, Depto. Ciencias Preclínicas, Facultad Medicina, UFRO, Temuco, Chile; Programa de Magíster en Kinesiología Cardiorrespiratoria, Facultad de Ciencias de la Salud, Universidad San Sebastián, Concepción, Chile.
| | - Fernando Romero
- Programa de Doctorado en Ciencias Médicas, Facultad de Medicina, Universidad de la Frontera. Laboratorio de Neurociencia y Biología de péptidos CEBIOR-CEGIN BIOREN, Depto. Ciencias Preclínicas, Facultad Medicina, UFRO, Temuco, Chile
| | - María Javiera Saavedra
- Programa de Magíster en Kinesiología Cardiorrespiratoria, Facultad de Ciencias de la Salud, Universidad San Sebastián, Concepción, Chile
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Jarrete AP, Zanesco A, Delbin MA. Assessment of endothelial function by flow-mediated dilation in diabetic patients: Effects of physical exercise. MOTRIZ: REVISTA DE EDUCACAO FISICA 2016. [DOI: 10.1590/s1980-65742016000100001] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Affiliation(s)
| | - Angelina Zanesco
- Universidade Estadual Paulista "Júlio de Mesquita Filho", Brazil
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Pedralli ML, Waclawovsky G, Camacho A, Markoski MM, Castro I, Lehnen AM. Study of endothelial function response to exercise training in hypertensive individuals (SEFRET): study protocol for a randomized controlled trial. Trials 2016; 17:84. [PMID: 26873336 PMCID: PMC4752791 DOI: 10.1186/s13063-016-1210-y] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/09/2015] [Accepted: 02/03/2016] [Indexed: 02/06/2023] Open
Abstract
Background Endothelial dysfunction is a hallmark of diabetes mellitus and systemic arterial hypertension (SAH) and an early maker for atherosclerosis. Aerobic exercise training is known to enhance endothelial function, but little is understood about the effects of resistance or combined exercise training on endothelial function. The aim of this study is to investigate the effect of a 12-week aerobic (AT), resistance (RT), or combined (aerobic and resistance, CT) training program on endothelial function and assess associated effects on blood pressure in individuals with SAH. Methods/design Eighty-one subjects with SAH aged 18 to 70 years will be selected and randomly assigned to three types of exercise training: AT, RT or CT. The study will involve the following procedures and tests: anamnesis, anthropometric assessment, echocardiography, blood pressure measurements through ambulatory blood pressure monitoring, flow-mediated dilation, ergospirometry, one repetition maximum test (1-RM), and blood collection (number of circulating endothelial progenitor cells, number of circulating endothelial microparticles, lipid profile, glucose, glycated hemoglobin, and creatinine). The AT intervention will consist of a 40-min exercise session with progressive intensities ranging from 50 to 75 % of heart rate reserve. The RT intervention will consist of a 40-minute session with four sets of six to 12 repetitions with a rest period of 60 to 90 seconds between each set and each type of exercise. Weight loads will be adjusted to 60 to 80 % of 1-RM for six types of exercise. The CT intervention will consist of a 20-min aerobic exercise session, followed by an additional 20-min resistance exercise session; each resistance exercise will have two sets less to match the total training volume. Discussion The study results are expected evidence of cardiovascular protective effects of different types of exercise training through the modulation of endothelial function in hypertensive individuals. Knowing the magnitude of improvement of endothelium-dependent vasodilation for the different types of exercise training can provide scientific evidence for the prescription of exercise programs for vascular protection targeting hypertensive individuals. Trial registration The Brazilian Clinical Trials Registry (http://www.ensaiosclinicos.gov.br/) under RBR-9ygmdn and dated 1 March 2015.
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Affiliation(s)
- Marinei Lopes Pedralli
- Laboratório de Investigação Clínica, Instituto de Cardiologia / Fundação Universitária de Cardiologia - ICFUC, Av. Princesa Isabel, 395. Bairro Santana, 90620 001, Porto Alegre, RS, Brazil. .,Universidade Luterana do Brasil - ULBRA, Torres, Rio Grande do Sul, Brazil.
| | - Gustavo Waclawovsky
- Laboratório de Investigação Clínica, Instituto de Cardiologia / Fundação Universitária de Cardiologia - ICFUC, Av. Princesa Isabel, 395. Bairro Santana, 90620 001, Porto Alegre, RS, Brazil.
| | - Augusto Camacho
- Laboratório de Investigação Clínica, Instituto de Cardiologia / Fundação Universitária de Cardiologia - ICFUC, Av. Princesa Isabel, 395. Bairro Santana, 90620 001, Porto Alegre, RS, Brazil.
| | - Melissa Medeiros Markoski
- Laboratório de Investigação Clínica, Instituto de Cardiologia / Fundação Universitária de Cardiologia - ICFUC, Av. Princesa Isabel, 395. Bairro Santana, 90620 001, Porto Alegre, RS, Brazil.
| | - Iran Castro
- Laboratório de Investigação Clínica, Instituto de Cardiologia / Fundação Universitária de Cardiologia - ICFUC, Av. Princesa Isabel, 395. Bairro Santana, 90620 001, Porto Alegre, RS, Brazil.
| | - Alexandre Machado Lehnen
- Laboratório de Investigação Clínica, Instituto de Cardiologia / Fundação Universitária de Cardiologia - ICFUC, Av. Princesa Isabel, 395. Bairro Santana, 90620 001, Porto Alegre, RS, Brazil. .,Faculdade Sogipa de Educação Física, Porto Alegre, Rio Grande do Sul, Brazil.
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Olver TD, Laughlin MH. Endurance, interval sprint, and resistance exercise training: impact on microvascular dysfunction in type 2 diabetes. Am J Physiol Heart Circ Physiol 2016; 310:H337-50. [PMID: 26408541 PMCID: PMC4796622 DOI: 10.1152/ajpheart.00440.2015] [Citation(s) in RCA: 55] [Impact Index Per Article: 6.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/08/2015] [Accepted: 09/16/2015] [Indexed: 01/02/2023]
Abstract
Type 2 diabetes (T2D) alters capillary hemodynamics, causes capillary rarefaction in skeletal muscle, and alters endothelial and vascular smooth muscle cell phenotype, resulting in impaired vasodilatory responses. These changes contribute to altered blood flow responses to physiological stimuli, such as exercise and insulin secretion. T2D-induced microvascular dysfunction impairs glucose and insulin delivery to skeletal muscle (and other tissues such as skin and nervous), thereby reducing glucose uptake and perpetuating hyperglycemia and hyperinsulinemia. In patients with T2D, exercise training (EX) improves microvascular vasodilator and insulin signaling and attenuates capillary rarefaction in skeletal muscle. EX-induced changes subsequently augment glucose and insulin delivery as well as glucose uptake. If these adaptions occur in a sufficient amount of tissue, and skeletal muscle in particular, chronic exposure to hyperglycemia and hyperinsulinemia and the risk of microvascular complications in all vascular beds will decrease. We postulate that EX programs that engage as much skeletal muscle mass as possible and recruit as many muscle fibers within each muscle as possible will generate the greatest improvements in microvascular function, providing that the duration of the stimulus is sufficient. Primary improvements in microvascular function occur in tissues (skeletal muscle primarily) engaged during exercise, and secondary improvements in microvascular function throughout the body may result from improved blood glucose control. We propose that the added benefit of combined resistance and aerobic EX programs and of vigorous intensity EX programs is not simply "more is better." Rather, we believe the additional benefit is the result of EX-induced adaptations in and around more muscle fibers, resulting in more muscle mass and the associated microvasculature being changed. Thus, to acquire primary and secondary improvements in microvascular function and improved blood glucose control, EX programs should involve upper and lower body exercise and modulate intensity to augment skeletal muscle fiber recruitment. Under conditions of limited mobility, it may be necessary to train skeletal muscle groups separately to maximize whole body skeletal muscle fiber recruitment.
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Affiliation(s)
- T Dylan Olver
- Department of Biomedical Sciences, University of Missouri, Columbia, Missouri;
| | - M Harold Laughlin
- Department of Biomedical Sciences, University of Missouri, Columbia, Missouri; Department of Medical Pharmacology and Physiology, University of Missouri School of Medicine, Columbia, Missouri
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Coombes JS, Sharman JE, Fassett RG. Astaxanthin has no effect on arterial stiffness, oxidative stress, or inflammation in renal transplant recipients: a randomized controlled trial (the XANTHIN trial). Am J Clin Nutr 2016; 103:283-9. [PMID: 26675778 DOI: 10.3945/ajcn.115.115477] [Citation(s) in RCA: 34] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/22/2015] [Accepted: 11/03/2015] [Indexed: 12/31/2022] Open
Abstract
BACKGROUND There is evidence that renal transplant recipients have accelerated atherosclerosis that is manifest by increased cardiovascular morbidity and mortality. The high incidence of atherosclerosis is, in part, related to increased arterial stiffness, vascular dysfunction, elevated oxidative stress, and inflammation associated with immunosuppressive therapy. The carotenoid astaxanthin has shown potent antioxidant and anti-inflammatory properties. OBJECTIVE The aim was to investigate the effects of oral astaxanthin on arterial stiffness, oxidative stress, and inflammation in renal transplant recipients. DESIGN This trial used a randomized, placebo-controlled, double-blind design in which 61 patients received either 12 mg astaxanthin/d or an identical placebo orally for 1 y. Primary outcomes were 1) arterial stiffness measured by aortic pulse wave velocity (PWV), 2) oxidative stress assessed by total plasma F2-isoprostanes, and 3) inflammation assessed by plasma pentraxin-3. Secondary outcomes included vascular function, carotid artery intima-media thickness, augmentation index, central blood pressure, subendocardial viability ratio, and additional measures of oxidative stress and inflammation. Patients underwent assessments at baseline and at 6 and 12 mo. RESULTS Fifty-eight participants completed the study. There were no significant between-group differences in the changes in any of the primary outcome measures (PWV changed by +9.5% and +6.0%, F2-isoprostanes changed by -3.0% and -9.7%, and pentraxin-3 changed by +50.6% and -11.0% in the placebo and astaxanthin groups, respectively). There were no significant between-group differences in secondary outcome measures. Larger-than-expected variability decreased the power of the study and increased the possibility of a type 2 statistical error. CONCLUSION Astaxanthin (12 mg/d for 12 mo) had no effect on arterial stiffness, oxidative stress, or inflammation in renal transplant recipients. This trial was registered at the Australian New Zealand Clinical Trials Registry (http://www.anzctr.org.au/) as ACTRN12608000159358.
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Affiliation(s)
- Jeff S Coombes
- School of Human Movement and Nutrition Sciences, University of Queensland, St. Lucia, Australia; and
| | - James E Sharman
- Menzies Research Institute Tasmania, University of Tasmania, Hobart, Australia
| | - Robert G Fassett
- School of Human Movement and Nutrition Sciences, University of Queensland, St. Lucia, Australia; and
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Dias KA, Green DJ, Ingul CB, Pavey TG, Coombes JS. Exercise and Vascular Function in Child Obesity: A Meta-Analysis. Pediatrics 2015; 136:e648-59. [PMID: 26260721 DOI: 10.1542/peds.2015-0616] [Citation(s) in RCA: 33] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 06/25/2015] [Indexed: 11/24/2022] Open
Abstract
CONTEXT Conduit artery flow-mediated dilation (FMD) is a noninvasive index of preclinical atherosclerosis in humans. Exercise interventions can improve FMD in both healthy and clinical populations. OBJECTIVE This systematic review and meta-analysis aimed to summarize the effect of exercise training on FMD in overweight and obese children and adolescents as well as investigate the role of cardiorespiratory fitness (peak oxygen consumption [Vo2peak]) on effects observed. DATA SOURCES PubMed, Medline, Embase, and Cinahl databases were searched from the earliest available date to February 2015. STUDY SELECTION Studies of children and/or adolescents who were overweight or obese were included. DATA EXTRACTION Standardized data extraction forms were used for patient and intervention characteristics, control/comparator groups, and key outcomes. Procedural quality of the studies was assessed using a modified version of the Physiotherapy Evidence Base Database scale. RESULTS A meta-analysis involving 219 participants compared the mean difference of pre- versus postintervention vascular function (FMD) and Vo2peak between an exercise training intervention and a control condition. There was a significantly greater improvement in FMD (mean difference 1.54%, P < .05) and Vo2peak (mean difference 3.64 mL/kg/min, P < .05) after exercise training compared with controls. LIMITATIONS Given the diversity of exercise prescriptions, participant characteristics, and FMD measurement protocols, varying FMD effect size was noted between trials. CONCLUSIONS Exercise training improves vascular function in overweight and obese children, as indicated by enhanced FMD. Further research is required to establish the optimum exercise program for maintenance of healthy vascular function in this at-risk pediatric population.
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Affiliation(s)
- Katrin A Dias
- School of Human Movement and Nutrition Sciences, The University of Queensland, St Lucia, Brisbane, Queensland, Australia
| | - Daniel J Green
- School of Sport Science, Exercise and Health, The University of Western Australia, Crawley, Western Australia, Australia; Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, Merseyside, United Kingdom
| | - Charlotte B Ingul
- Department of Circulation and Medical Imaging, Norwegian University of Science and Technology, Trondheim, Norway; and
| | - Toby G Pavey
- School of Human Movement and Nutrition Sciences, The University of Queensland, St Lucia, Brisbane, Queensland, Australia
| | - Jeff S Coombes
- School of Human Movement and Nutrition Sciences, The University of Queensland, St Lucia, Brisbane, Queensland, Australia;
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Effect of combining music media therapy with lower extremity exercise on elderly patients with diabetes mellitus. Int J Nurs Sci 2015. [DOI: 10.1016/j.ijnss.2015.07.008] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
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Ramos JS, Dalleck LC, Tjonna AE, Beetham KS, Coombes JS. The Impact of High-Intensity Interval Training Versus Moderate-Intensity Continuous Training on Vascular Function: a Systematic Review and Meta-Analysis. Sports Med 2015; 45:679-92. [DOI: 10.1007/s40279-015-0321-z] [Citation(s) in RCA: 290] [Impact Index Per Article: 29.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/23/2022]
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40
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Hwang MH, Kim S. Type 2 Diabetes: Endothelial dysfunction and Exercise. J Exerc Nutrition Biochem 2014; 18:239-47. [PMID: 25566460 PMCID: PMC4241901 DOI: 10.5717/jenb.2014.18.3.239] [Citation(s) in RCA: 31] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/04/2014] [Revised: 09/16/2014] [Accepted: 09/26/2014] [Indexed: 01/22/2023] Open
Abstract
PURPOSE Vascular endothelial dysfunction is an early marker of atherosclerosis characterized by decreased nitric oxide bioavailability in the vascular endothelium and smooth muscle cells. Recently, some animal models and in vitro trials demonstrated that excessive superoxide production from mitochondria within vascular endothelial cells played a role in the pathogenesis of atherosclerosis in type 2 diabetes. This review provides a systematic assessment of the effectiveness of exercise to identify effective approaches to recognize diabetes risk and prevent progression to heart disease. METHODS A systematic literature search was conducted to retrieve articles from 1979 to 2013 using the following databases: the MEDLINE, PubMed. Articles had to describe an intervention that physical activity and exercise to identify effective approaches to heart and vascular endothelium. RESULTS Currently, physical activity and exercise guidelines aimed to improve cardiovascular health in patients with type 2 diabetes are nonspecific. Benefit of aerobic exercise training on vascular endothelial function in type 2 diabetic patients is still controversial. CONCLUSION it is necessary to demonstrate the mechanism of endothelial dysfunction from live human tissues so that we can provide more specific exercise training regimens to enhance cardiovascular health in type 2 diabetic patients.
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Affiliation(s)
- Moon-Hyon Hwang
- Division of Clinical and Translational Science, Georgia Regents University, Georgia, USA
| | - Sangho Kim
- School of Global Sport Studies, Korea University, Sejong, Korea
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Michal M, Simon P, Gori T, König J, Wild PS, Wiltink J, Tug S, Sterzing B, Unterrainer J, Münzel T, Beutel ME. Psychodynamic Motivation and Training program (PMT) for the secondary prevention in patients with stable coronary heart disease: study protocol for a randomized controlled trial of feasibility and effects. Trials 2013; 14:314. [PMID: 24066805 PMCID: PMC3819661 DOI: 10.1186/1745-6215-14-314] [Citation(s) in RCA: 10] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/03/2013] [Accepted: 09/16/2013] [Indexed: 01/29/2023] Open
Abstract
BACKGROUND Nonpharmacological secondary prevention of coronary heart disease is considered a safe and effective measure to substantially reduce mortality. Despite the effectiveness of lifestyle changes, the compliance rate of patients is very low mainly due to psychosocial barriers. Psychotherapeutic approaches that address how persons think about themselves and their behaviors appear to have a significant potential for improving health behavior. METHODS/DESIGN Against this background, our study aims to examine the feasibility and effects of a Psychodynamic Motivation and Training program (PMT) as compared to one session of advice in exercise training (EX) and treatment as usual (TAU). For that purpose, 90 patients with stable coronary heart disease and a physically inactive lifestyle will be randomly assigned to the three groups (each with n = 30). The primary outcome is the change in the individual anaerobic threshold as determined by spiroergometry from baseline to six month follow-up. Secondary endpoints include change in endothelial function, biomarkers of inflammation and oxidative stress, quality of life, symptoms of fatigue, illness perception and feasibility of the treatment approach. We hypothesize that physical fitness will improve more in PMT than in EX and TAU, with PMT and EX more than TAU, and that the effects will be more pronounced for participants with current mental or psychosocial distress. DISCUSSION The results of the study will help to determine the effectiveness of a psychodynamic lifestyle change approach and to identify measures for designing specifically tailored interventions to improve compliance with cardiovascular prevention. TRIAL REGISTRATION ClinicalTrials.gov Identifier: NCT01445808.
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Affiliation(s)
- Matthias Michal
- Department of Psychosomatic Medicine and Psychotherapy, University Medical Center of the Johannes Gutenberg University Mainz, Untere Zahlbacher Strasse 8, Mainz 55131, Germany
| | - Perikles Simon
- Department of Sports Medicine, Rehabilitation and Disease Prevention, Institute for Sport Sciences, Johannes Gutenberg University Mainz, Mainz, Germany
| | - Tommaso Gori
- Department of Medicine II, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany
| | - Jochem König
- Institute of Medical Biostatistics, Epidemiology & Informatics, University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany
| | - Philipp S Wild
- Department of Medicine II, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany
| | - Jörg Wiltink
- Department of Psychosomatic Medicine and Psychotherapy, University Medical Center of the Johannes Gutenberg University Mainz, Untere Zahlbacher Strasse 8, Mainz 55131, Germany
| | - Suzan Tug
- Department of Sports Medicine, Rehabilitation and Disease Prevention, Institute for Sport Sciences, Johannes Gutenberg University Mainz, Mainz, Germany
| | - Björn Sterzing
- Department of Sports Medicine, Rehabilitation and Disease Prevention, Institute for Sport Sciences, Johannes Gutenberg University Mainz, Mainz, Germany
| | - Josef Unterrainer
- Institute of Medical Psychology and Sociology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany
| | - Thomas Münzel
- Department of Medicine II, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany
| | - Manfred E Beutel
- Department of Psychosomatic Medicine and Psychotherapy, University Medical Center of the Johannes Gutenberg University Mainz, Untere Zahlbacher Strasse 8, Mainz 55131, Germany
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