Exploring the Association between Vascular Dysfunction and Skeletal Muscle Mass, Strength and Function in Healthy Adults: A Systematic Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. Literature Search
2.2. Inclusion Criteria
2.3. Data Extraction
2.4. Study Details and Sample Demographics
2.5. Assessment of Skeletal Muscle Health
2.6. Assessment of Vascular Health
3. Results
3.1. Macrovascular Studies
3.2. Microvascular Studies
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Study & Year | Design | Sample | Country | n | Male (%) | Age | Exclusion |
---|---|---|---|---|---|---|---|
Barnouin 2017 [33] | Cross-sectional | Healthy adults | UK | 47 | 77 | 22–74 | Cardiovascular, neuromuscular, or respiratory diseases |
Barrera 2014 [35] | Cross-sectional | Healthy adults | Chile | 259 | 49 | 29–88 | Undernutrition BMI < 18, cancer, autoimmune disease, kidney, liver or cardiac failure, diabetes, cognitive impairment, steroids or HRT |
Brightwell 2018 [26] | RCT | Healthy adults | USA | 23 | 30 | 65–82 | Diabetes, cancer, smoking, CVD, kidney disease, uncontrolled high blood pressure, low daily protein intake |
Chung 2018 [36] | Cross-sectional | Healthy adults | Korea | 1590 | 78 | 40–79 | Metabolic syndrome, HRT, any medication |
den Ouden 2013 [37] | Cross-sectional | Healthy adults | The Netherlands | 403 | 100 | 73–91 | Inability to visit the study center independently |
Dipla 2017 [55] | Cross-sectional | Healthy and hypertensive adults | Greece | 91 | 60 | 31–55 | CVD, diabetes |
Fahs 2017 [39] | Cross-sectional | Healthy adults | USA | 71 | 51 | 18–75 | Hypertension, participation in regular exercise, HRT |
Gonzales 2015 [40] | Cross-sectional | Healthy adults | USA | 45 | 44 | 60–78 | CVD, diabetes, pulmonary disease, HRT, obesity, medication for blood pressure or cholesterol |
Groen 2014 [61] | Cross-sectional | Healthy and T2DM adults | The Netherlands | 45 | 100 | 23–71 | Impaired renal or liver function, obesity, CVD, hypertension, advanced diabetes, insulin therapy |
Gueugneau 2016 [56] | Cross-sectional | Healthy and hypertensive adults | France | 37 | 100 | 21–74 | Prior myocardial infarction or stroke, heart failure, atrial fibrillation, diabetes, morbid obesity, Parkinson’s disease |
Heffernan 2012 [41] | Cross-sectional | Healthy adults | USA | 24 | 46 | 70–85 | Acute/terminal illness, coronary heart disease, myocardial infarction, hypertension, neuromuscular disease, HRT, diabetes, renal disease, BMI > 32.5 |
Im 2017 [42] | Cross-sectional | Healthy adults | Korea | 3356 | 100 | 40–64 | ABI < 0.9, high WBC count, cancer |
Khoudary 2015 [38] | Cross-sectional | Healthy adults | USA | 1103 | 0 | 56–62 | Stroke, angina or myocardial infarction, hysterectomy or bilateral oophorectomy, pregnancy, HRT |
Kohara 2017 [43] | Cross-sectional | Healthy adults | Japan | 1518 | 40 | 60–74 | CVD, PAD, stroke, coronary heart disease, and congestive heart failure |
Lee 2014 [44] | Cross-sectional | Healthy adults | Korea | 427 | 42 | 52–95 | n/r or unclear |
Lima-Junior 2018 [57] | Cross-sectional | Hypertensive adults | Brazil | 72 | 28 | 48–68 | <18 years, smoking, diabetics, CVD, inability to perform isometric handgrip, enrolled in physical activity program |
Mitchell 2013 [25] | RCT | Healthy adults | UK | 36 | 100 | 18–75 | Diabetes, CVD, BMI < 18 or >28 |
Ochi 2010 [46] | Cross-sectional | Healthy adults | Japan | 496 | 36 | n/r | Stroke, TIA, coronary heart disease and congestive heart failure |
Phillips 2012 [34] | RCT | Healthy adults | UK | 51 | 57 | 21–72 | Muscle wasting, metabolic or respiratory diseases, CVD, chronic diseases |
Prior 2016 [47] | Cross-sectional | Healthy adults | USA | 76 | 42 | 45–80 | Coronary artery disease, heart failure, PAD, stroke, liver, kidney or lung disease, smoking |
Sampaio 2014 [58] | Cross-sectional | Healthy and hypertensive adults | Japan | 175 | 48 | 70–77 | Moderate cognitive impairment, uncontrolled cardiovascular, pulmonary or metabolic diseases, stroke, Parkinson’s disease, PAD, orthopedic disease |
Sanada 2010 [48] | Cross-sectional | Healthy adults | Japan | 1488 | 29 | 18–85 | CVD, beta-blockers, HRT, athletes |
Shimizu 2017 [59] | Cross-sectional | Hypertensive adults | Japan | 795 | 57 | 60–89 | Participants without hypertension, BMI < 18.5, high BP, history of stroke |
Shiotsu 2018 [49] | RCT | Healthy adults | Japan | 45 | 100 | 63–85 | Current participation in structured exercise program, CVD, musculoskeletal disease, diabetes |
Suwa 2018 [50] | Cross-sectional | Healthy adults | Japan | 1354 | 100 | 35–59 | CVD, history of stroke |
Timmerman 2012 [20] | RCT | Healthy older adults | USA | 6 | 50 | 67–73 | Obesity, chronic diseases |
Verdijk 2016 [27] | RCT | Healthy adults | The Netherlands | 30 | 100 | 19–83 | CVD, PAD, diabetes, inability to participate in an exercise program |
Wong 2018 [60] | RCT | Hypertensive adults | Korea | 41 | 0 | 49–67 | Pre-menopause, CVD, diabetes, HRT, smoking, exercise, endocrine disorders, psychiatric disorders |
Wüst 2009 [62] | Cross-sectional | Adults | UK | 11 | 45 | n/r | n/r or unclear |
Yamamoto 2009 [51] | Cross-sectional | Healthy adults | Japan | 526 | 34 | 20–83 | Obesity, chronic diseases, smoking, ABI < 0.9, any medication |
Yoo 2018 [53] | Cross-sectional | Community-dwelling older adults | Korea | 236 | 0 | 67–79 | CVD, cognitive disorder, malignancy |
Yoshizawa 2009 [52] | RCT | Healthy adults | Japan | 35 | 0 | 32–59 | Chronic diseases, smoking, any medication |
Zhang 2019 [54] | Cross-sectional | Community-dwelling older adults | China | 1002 | 42 | 65–81 | n/r or unclear |
Study & Year | Parameter | Region | Modality | Device |
---|---|---|---|---|
Brightwell 2018 * [26] | Muscular strength | Appendicular | Peak leg torque | Biodex isokinetic dynamometer |
Chung 2018 [36] | Muscular strength | Appendicular | Hand-grip strength | Hand-grip dynamometer |
den Ouden 2013 [37] | Muscular strength | Appendicular | Hand-grip strength | JAMAR hand-grip dynamometer |
Dipla 2017 [55] | Muscular strength | Appendicular | Hand-grip strength | Biopac hand-grip dynamometer |
Lima-Junior 2018 [57] | Muscular strength | Appendicular | Hand-grip strength | Hand-grip dynamometer |
Shimizu 2017 [59] | Muscular strength | Appendicular | Hand-grip strength | Smedley hand-grip dynamometer |
Wong 2018 [60] | Muscular Strength | Appendicular | 8-RM | Cybex dynamometer |
Yoo 2018 [53] | Muscular strength | Appendicular | Hand-grip strength | T.K.K hand-grip dynamometer |
Im 2017 [42] | Muscle mass | Whole body | BIA | Inbody |
Kohara 2017 [43] | Muscle mass | Whole body | BIA, CT | Omron, GE |
Lee 2014 [44] | Muscle mass | Whole body | BIA | InBody |
Mitchell 2013 * [25] | Muscle mass | Appendicular | DXA | Lunar |
Sampaio 2014 [58] | Muscle mass | Whole body | BIA | n/r |
Sanada 2010 [48] | Muscle mass | Whole body | DXA | Hologic |
Timmerman 2012 * [20] | Muscle anabolic response | Appendicular | Muscle biopsy | Bergström needle |
Zhang 2019 [54] | Muscle mass | Whole body | BIA | InBody |
Barnouin 2017 * [33] | Muscle CSA | Appendicular | Muscle biopsy | Bergström needle |
Gueugneau 2016 * [56] | Muscle CSA | Appendicular | Muscle biopsy | Bergström needle |
Ochi 2010 [46] | Muscle CSA | Appendicular | CT | GE |
Wüst 2009 * [62] | Muscle CSA | Appendicular | Muscle biopsy | Percutaneous needle |
Gonzales 2015 [40] | Muscular function | Whole body | 400 m walk | Polar monitor (to track HR during walk) |
Khoudary 2015 [38] | Muscular function | Whole body | 40-foot walking speed, sit-to-stand test | n/r |
Suwa 2018 [50] | Muscular function | Appendicular | Arm extensibility test | n/r |
Yamamoto 2009 [51] | Muscular function | Whole body | Sit and reach test | Takei Scientific digital flexibility testing device |
Yoshizawa 2009 [52] | Muscular function | Whole body | 1-RM, aerobic capacity | Selectorized weight machines, cycle ergometer |
Barrera 2014 [35] | Muscular strength and function | Whole body | 12-min walk, TUG, hand-grip strength | Digital force transducer and hand-grip dynamometer |
Fahs 2017 [39] | Muscular strength and muscle mass | Whole body | 1-RM, DXA | Selectorized weight machines, Hologic |
Groen 2014 * [61] | Muscle mass and CSA | Appendicular | CT, muscle biopsy | n/r, percutaneous needle |
Heffernan 2012 [41] | Muscle strength and power | Appendicular | 1-RM | Keiser Sports |
Phillips 2012 [34] | Muscle mass and strength | Whole body | DXA, leg extension 75% 1-RM | Lunar, Leisure Lines |
Prior 2016 * [47] | Muscle mass and CSA | Whole body | DXA, CT | Lunar, Siemens |
Shiotsu 2018 [49] | Muscular strength and function | Whole body | 1-RM, hand-grip strength, 10-m walk, sit and reach test | Leg press/curl, chest/shoulder press, seated row, hand-grip dynamometer |
Verdijk 2016 * [27] | Muscular strength and muscle mass | Whole body | 1-RM, CT, DXA, muscle biopsy | Technogym, Phillips Medical, GE, percutaneous needle |
Study & Year | Parameter | Vascular Site | Method | Device |
---|---|---|---|---|
Chung 2018 [36] | PWV | Brachial-ankle | Volume-plethysmographic apparatus | Colin Medical |
Fahs 2017 [39] | PWV | Carotid-femoral | Applanation tonometry | SphygmoCor |
Gonzales 2015 [40] | PWV | Carotid-femoral | Applanation tonometry | SphygmoCor |
Im 2017 [42] | PWV | Carotid-ankle | Oscillometric | Fukuda Denshi |
Kohara 2017 [43] | PWV | Brachial-ankle | Volume-plethysmographic apparatus | Omron |
Ochi 2010 [46] | PWV | Brachial-ankle | Volume-plethysmographic apparatus | Omron |
Sampaio 2014 [58] | PWV | Carotid-ankle | Oscillometric | Fukuda Denshi |
Sanada 2010 [48] | PWV | Brachial-ankle | Volume-plethysmographic apparatus | Colin Medical |
Shiotsu 2018 [49] | PWV | Carotid-femoral | Oscillometric | Fukuda Denshi |
Wong 2018 [60] | PWV | Brachial-ankle | Volume-plethysmographic apparatus | Colin Medical |
Yamamoto 2009 [51] | PWV | Brachial-ankle | Volume-plethysmographic apparatus | Omron |
Yoshizawa 2009 [52] | PWV | Carotid-femoral | Volume-plethysmographic apparatus | Colin Medical |
Zhang 2019 [54] | PWV | Brachial-ankle | Volume-plethysmographic apparatus | Omron |
Barrera 2014 [35] | CIMT | Carotid | Ultrasound | GE |
den Ouden 2013 [37] | CIMT | Carotid | Ultrasound | ATL Ultramark IV |
Khoudary 2015 [38] | CIMT | Carotid | Ultrasound | Teratech Corp |
Shimizu 2017 [59] | CIMT | Carotid | Ultrasound | GE |
Suwa 2018 [50] | CIMT | Carotid | Ultrasound | Aplio |
Heffernan 2012 [41] | Aix | Radial | Applanation tonometry | Omron |
Lee 2014 [44] | Aix | Radial | Applanation tonometry | SphygmoCor |
Lima-Junior 2018 [57] | Aix | Radial | Applanation tonometry | EndoPAT |
Dipla 2017 [55] | FMD | Brachial | Muscle oxygenation apparatus | NIRS Artinis |
Yoo 2018 [53] | FMD | Brachial | Applanation tonometry | EndoPAT |
Phillips 2012 [34] | LBF | Femoral | Doppler ultrasound | Toshiba |
Barnouin 2017 * [33] | C: F Ratio | Femoral | Immunohistochemistry | Bergström needle |
Brightwell 2018 * [26] | C: F Ratio | Femoral | Immunohistochemistry | Bergström needle |
Groen 2014 * [61] | C: F Ratio | Femoral | Immunohistochemistry | Percutaneous needle |
Gueugneau 2016 * [56] | C: F Ratio | Femoral | Immunohistochemistry | Bergström needle |
Prior 2016 * [47] | C: F Ratio | Femoral | Immunohistochemistry | Percutaneous needle |
Verdijk 2016 * [27] | C: F Ratio | Femoral | Immunohistochemistry | Percutaneous needle |
Wüst 2009 * [62] | C: F Ratio | Femoral | Immunohistochemistry | Percutaneous needle |
Mitchell 2013 * [25] | MBF | Femoral | Contrast-enhanced ultrasound | Sonovue |
Timmerman 2012 * [20] | MBF | Femoral | Doppler ultrasound | Philips ATL |
Study & Year | Sample | Age | Muscle and Vascular Association | Type of Association | Finding |
---|---|---|---|---|---|
Barrera 2014 [35] | Healthy adults | 29–88 | Muscular strength/function and CIMT | Difference between groups (p < 0.05) † | In older adults, CIMT is negatively associated with muscular strength and function |
Chung 2018 [36] | Healthy adult men | 40–79 | Muscular strength and PWV | Difference between groups (p < 0.05) † | In middle-aged and older adults, arterial stiffness is negatively associated with muscular strength and function |
den Ouden 2013 [37] | Healthy older men | 73–91 | Muscular strength and CIMT | Correlation (r = −0.17; p < 0.05) | In older men, CIMT is negatively associated with muscular strength |
Dipla 2017 # [55] | Healthy and hypertensive adults | 31–55 | Muscular strength and muscle perfusion | Difference between groups (p < 0.05) † | Hypertensive adults have reduced tissue oxygen saturation compared to healthy controls; to produce same amount of torque compared to healthy controls requires a two-fold increase in BP |
Fahs 2017 [39] | Healthy adults | 18–75 | Muscular strength and PWV | Correlation (r = −0.230/−0.484; p < 0.05) | In adults, arterial stiffness is negatively correlated with absolute and relative muscular strength |
Gonzales 2015 [40] | Healthy older adults | 60–78 | Muscular function and PWV | Beta coefficient (p < 0.05) | In older adults, arterial stiffness is positively correlated with muscle fatigue |
Heffernan 2012 [41] | Healthy older adults | 70–85 | Muscular power and augmentation index | Correlation (r = -0.54; p < 0.05) | In older adults, arterial stiffness is negatively associated with muscular power |
Im 2017 [42] | Healthy adult men | 40–64 | Muscle mass and PWV | Correlation (p < 0.05) | In middle-aged men, arterial stiffness is negatively correlated with muscle mass |
Khoudary 2015 [38] | Healthy older women | 56–62 | Muscle function and CIMT | Beta coefficient (0.028; p < 0.05) | In older women, CIMT is negatively associated with muscle function |
Kohara 2017 [43] | Healthy older adults | 60–74 | Muscle mass and PWV | Correlation (r = −0.24; p < 0.05) | In older adults, arterial stiffness is negatively correlated with muscle mass |
Lee 2014 [44] | Healthy older adults | 52–95 | Muscle mass and augmentation index | Beta coefficient (p < 0.05) | In older adults, arterial stiffness is negatively associated with muscle mass |
Lima-Junior 2018 # [57] | Hypertensive older adults | 48–68 | Muscular strength and augmentation index | Beta coefficient (−0.49; p < 0.05) | In older adults with hypertension, arterial stiffness is negatively associated with muscular strength |
Ochi 2010 [46] | Healthy adults | n/r | Muscle CSA and PWV | Correlation (r = −0.34; p < 0.05) | In men, arterial stiffness is negatively associated with muscle mass |
Phillips 2012 * [34] | Healthy adults—resistance exercise | 21–72 | Muscle mass/strength and leg blood flow | Difference between groups (p < 0.05) † | Following resistance exercise training, adults experience increases in leg blood flow, muscle mass and strength regardless of age in response to feeding |
Sampaio 2014 # [58] | Healthy and hypertensive older adults | 70–77 | Muscle mass and PWV | Odds ratio (1.82; p < 0.05) | In healthy and hypertensive older adults, arterial stiffness is negatively associated with muscle mass |
Sanada 2010 [48] | Healthy adults | 41–71 | Muscle mass and PWV | Difference between groups (p < 0.05) † | Women with sarcopenia have higher arterial stiffness compared to healthy controls |
Shimizu 2017 # [59] | Hypertensive older adults | 60–89 | Muscular strength and CIMT | Difference between groups (p < 0.05) † | In older adults with hypertension, CIMT is negatively associated with muscular strength |
Shiotsu 2018 * [49] | Healthy older men—resistance exercise | 63–85 | Muscular strength/function and PWV | Difference between groups (p < 0.05) † | Following resistance exercise training, older men experience a decrease in arterial stiffness and an increase in muscular strength/function |
Suwa 2018 [50] | Healthy adult men | 35–59 | Muscular function and CIMT | Beta coefficient (−0.189; p < 0.05) | In middle-aged adults, CIMT is negatively associated with arm flexibility |
Wong 2018 *# [60] | Hypertensive older women—stair climbing exercise | 49–67 | Muscular strength and PWV | Correlation (r = −0.47; p < 0.05) | Following stair climbing training, hypertensive older women experience a decrease in arterial stiffness and an increase in muscular strength |
Yamamoto 2009 [51] | Healthy adults | 40–83 | Muscular function and PWV | Correlation (r = 0.17/0.45; p < 0.05) | In middle-aged and older adults, arterial stiffness is negatively correlated with flexibility |
Yoo 2018 [53] | Older women | 67–79 | Muscular strength and endothelial function | Correlation (r = 0.176; p < 0.05) | After adjusting for comorbidities, in older women, endothelial function is positively correlated with muscular strength |
Yoshizawa 2009 * [52] | Healthy women—aerobic exercise | 32–59 | Muscular function and PWV | Difference between groups (p < 0.05) † | Following aerobic training, middle-aged women experience a decrease in arterial stiffness and an increase in muscular function |
Zhang 2019 [54] | Older adults | 65–81 | Muscle mass and PWV | Odds ratio (1.11; p < 0.05) | After adjusting for comorbidities, in older adults, arterial stiffness is negatively associated with muscle mass |
Study & Year | Sample | Age | Muscle and Vascular Association | Type of Association | Finding |
---|---|---|---|---|---|
Barnouin 2017 [33] | Healthy adults | 22–74 | Muscle fiber CSA and capillary density | Correlation (R2 = 0.46; p < 0.05) | In young and older adults, capillary-to-fiber ratio is positively correlated with muscle mass |
Brightwell 2018 * [26] | Healthy older adults—aerobic exercise | 65–82 | Muscular strength and capillary density | Difference between groups (p < 0.05) † | Following aerobic training, older adults experience an increase in capillary density and an increase in muscular strength |
Groen 2014 [61] | Healthy adult men | 23–71 | Muscle fiber CSA and capillary density | Difference between groups (p < 0.05) † | Older adults have reduced capillary-to-fiber ratio and muscle mass compared to young controls |
Gueugneau 2016 # [56] | Healthy and hypertensive older men | 72–74 | Muscle fiber CSA and capillary density | Difference between groups (p < 0.05) † | Older adults with hypertension have lower capillary-to-fiber ratio and muscle mass compared to healthy older controls |
Mitchell 2013 [25] | Healthy adult men | 18–75 | Muscle mass and microvascular blood flow | Difference between groups (p < 0.05) † | Young adults have higher muscle mass and have higher microvascular blood flow in response to feeding compared to healthy older adults |
Prior 2016 [47] | Healthy adults | 45–80 | Muscle mass and capillary density | Correlation (r = 0.30–0.37; p < 0.05) | In adults, capillary-to-fiber ratio is positively correlated with muscle mass |
Timmerman 2012 [20] | Healthy older adults—aerobic exercise | 67–73 | Muscle protein synthesis and microvascular blood flow | Difference between groups (p < 0.05) † | Following aerobic exercise, older adults experience improved microvascular flow and muscle protein synthesis |
Verdijk 2016 * [27] | Healthy older adults—resistance exercise | 65–83 | Muscle fiber CSA/strength and capillary density | Difference between groups (p < 0.05) † | Following resistance training, older adults experience an increase in capillary-to-fiber ratio and an increase in muscle mass and strength |
Wüst 2009 [62] | Adults | n/r | Muscle fiber CSA and capillary density | Correlation (r = 0.62; p < 0.05) | In adults, capillary-to-fiber ratio is positively correlated with muscle mass |
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Dvoretskiy, S.; Lieblein-Boff, J.C.; Jonnalagadda, S.; Atherton, P.J.; Phillips, B.E.; Pereira, S.L. Exploring the Association between Vascular Dysfunction and Skeletal Muscle Mass, Strength and Function in Healthy Adults: A Systematic Review. Nutrients 2020, 12, 715. https://doi.org/10.3390/nu12030715
Dvoretskiy S, Lieblein-Boff JC, Jonnalagadda S, Atherton PJ, Phillips BE, Pereira SL. Exploring the Association between Vascular Dysfunction and Skeletal Muscle Mass, Strength and Function in Healthy Adults: A Systematic Review. Nutrients. 2020; 12(3):715. https://doi.org/10.3390/nu12030715
Chicago/Turabian StyleDvoretskiy, Svyatoslav, Jacqueline C. Lieblein-Boff, Satya Jonnalagadda, Philip J. Atherton, Bethan E. Phillips, and Suzette L. Pereira. 2020. "Exploring the Association between Vascular Dysfunction and Skeletal Muscle Mass, Strength and Function in Healthy Adults: A Systematic Review" Nutrients 12, no. 3: 715. https://doi.org/10.3390/nu12030715