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Cardiovascular Adaptations to Exercise Training

Ylva Hellsten, Michael Nyberg

10.1002/cphy.c140080

Source: Volume 6, Issue 1, January 2016

Published online: December 2015

Full Article on Wiley Online Library



ABSTRACT

Aerobic exercise training leads to cardiovascular changes that markedly increase aerobic power and lead to improved endurance performance. The functionally most important adaptation is the improvement in maximal cardiac output which is the result of an enlargement in cardiac dimension, improved contractility, and an increase in blood volume, allowing for greater filling of the ventricles and a consequent larger stroke volume. In parallel with the greater maximal cardiac output, the perfusion capacity of the muscle is increased, permitting for greater oxygen delivery. To accommodate the higher aerobic demands and perfusion levels, arteries, arterioles, and capillaries adapt in structure and number. The diameters of the larger conduit and resistance arteries are increased minimizing resistance to flow as the cardiac output is distributed in the body and the wall thickness of the conduit and resistance arteries is reduced, a factor contributing to increased arterial compliance. Endurance training may also induce alterations in the vasodilator capacity, although such adaptations are more pronounced in individuals with reduced vascular function. The microvascular net increases in size within the muscle allowing for an improved capacity for oxygen extraction by the muscle through a greater area for diffusion, a shorter diffusion distance, and a longer mean transit time for the erythrocyte to pass through the smallest blood vessels. The present article addresses the effect of endurance training on systemic and peripheral cardiovascular adaptations with a focus on humans, but also covers animal data. © 2016 American Physiological Society. Compr Physiol 6:1‐32, 2016.

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Figure 1. Figure 1. Heart rate (A), stroke volume (B), and cardiac output (C) in relation to systemic V· O2 in untrained and trained subjects and elite athletes.
Figure 2. Figure 2. Skeletal muscle sympathetic nervous activity (MSNA) during knee‐extensor exercise and venous norepinephrine concentrations during cycling exercise in the untrained and trained state. MSNA was measured by microneurography in the resting leg. Adapted from (346) and (457) with permission of the American Physiological Society. MSNA = Muscle sympathetic nerve activity.
Figure 3. Figure 3. Blood volume (A), erythrocyte and plasma volume (B), and hematocrit (C) in untrained and trained subjects and elite athletes.
Figure 4. Figure 4. Femoral arterial blood flow and arterio‐venous O2 difference during submaximal (A) and maximal (B) single leg knee‐extensor exercise with a previously immobilzed leg, untrained and trained leg. Immobilization lasted for 2 weeks and was achieved by casting. Blood flow was determined by ultrasound Doppler methodology, arterio‐venous oxygen extraction was obtained by measurements of oxygen content in blood drawn simultaneously from the femoral artery and femoral vein. Adapted from (292) and (298) with permission of the American Physiological Society.
Figure 5. Figure 5. Regulation of skeletal muscle blood flow during exercise. Several vasoactive mechanisms are involved in the regulation of skeletal muscle blood flow during exercise and together these mechanisms secure a highly precise oxygen delivery for the energy production required for the contractile work of the muscle. The vasodilator mechanisms include endothelial dependent vasodilatation which can be induced both by mechanical influence, primarily via shear stress, but also chemically via compounds such as ATP and adenosine. In response to the contractile work, skeletal muscle cells can produce and release vasodilator compounds including nitric oxide (NO) and ATP. NO and ATP can also be produced by red blood cells in response to off‐loading of oxygen from the hemoglobin molecule which occurs in the arterioles and capillaries. Coordination of blood flow in the microvascular system is facilitated by retrograde conducted vasodilation. In conducted vasodilation an electrical signal and a calcium wave travel in retrograde direction leading to vasodilatation in upstream arterioles. Finally, specific compounds such as ATP may reduce the efficacy of sympathetic activity in the skeletal muscle arterioles, thereby reducing the constrictive effect. ATP: Adenosine 5′triphosphate, NO: nitric oxide; ROS: reactive oxygen species; EDHF: endothelial‐derived hyperpolarizing factor.
Figure 6. Figure 6. The effect of endurance training on vasodilators and vasoconstrictors involved in the regulation of skeletal muscle blood flow. Skeletal muscle blood flow regulation is brought about by a balance between on one hand sympathetic vasoconstriction and other vasoconstrictors such as endothelin 1 (ET‐1) and thromboxane (TXA2) and on the other hand vasodilators formed in the active muscle, of which nitric oxide (NO) and prostacyclin (PGI2) appear to be central. Another important aspect in skeletal muscle blood flow regulation is the substantial interaction between vasodilator systems and compounds. For example, ATP and adenosine can mediate vasodilatation via activation of receptors on the endothelial cells resulting in the formation of NO and PGI2. NO and PGI2 in turn interact in a redundant manner so that when one is inhibited the other system can compensate. The effect of training on the formation of vasodilators and constrictors (marked by blue arrows) has not been fully clarified and the attempt to illustrate changes in this figure is tentative. Studies show that the concentrations of NO and prostacyclin in plasma and the muscle interstitium are either enhanced or remain unaltered at rest and during exercise. Adenosine and ATP levels in the muscle interstitium may increase with training, however, in parallel, the vascular sensitivity to nucleotides is reduced. On the constrictor side, ET‐1 and TXA2 have been shown to be reduced in plasma at rest whereas plasma noradrenaline is reduced during exercise indicating an attenuated sympathetic drive. ATP = Adenosine 5'triphosphate, ADO = adenosine; PGI2 = prostacyclin; NO = nitric oxide; NE = Noradrenaline, ET‐1 = endothelin‐1, TXA2 = thromboxane A2. p and i in figure beside blue arrows specify that changes were observed in plasma and muscle interstitium, respectively.
Figure 7. Figure 7. Femoral arterial blood flow during knee‐extensor exercise without and with arterial infusion of tyramine (induces a release of norepinephrine from sympathetic nerve endings) with a previously immobilized, untrained, and trained limb. Immobilization lasted for two weeks and was achieved by casting. Blood flow was determined by ultrasound Doppler methodology, arterio venous oxygen extraction was obtained by measurements of oxygen content in blood drawn simultaneously from the femoral artery and femoral vein. Adapted from (292) and (295) with permission.
Figure 8. Figure 8. Capillary‐to‐fiber ratio in untrained (VO2max: ∼50 mL O2 min−1 kg−1) young men before (0 weeks) and after 7 weeks of exercise training (7 weeks) and in trained (VO2max: ∼66 mL O2 min−1 kg−1) young men (cross‐sectional). The 7‐week training period consisted of high‐intensity interval training. Capillary number was obtained by counting of immunohistochemically stained transverse muscle sections cut from frozen muscle (m.v. lateralis) samples. Fitness level was determined by measurements of expired air during a graded cycle test to exhaustion. Adapted from (210) and (201) with permission.
Figure 9. Figure 9. Capillary‐to‐fiber ratio in relation to maximal oxygen uptake in young, middle‐aged, and older men of different training status. Capillary number and muscle fibers were obtained by counting of immunohistochemically stained transverse muscle sections cut from frozen muscle (m.v. lateralis) samples. Maximal oxygen uptake was determined by measurements of expired air during a graded cycle test to exhaustion. Data adapted, with permission, from (150,191,201) and from Andersen and Bangsbo (previously unpublished data) and Nyberg, Hellsten and Mortensen (previously unpublished data).
Figure 10. Figure 10. Dynamic muscle contraction provides mechanical signals of importance for capillary growth: the associated increase in blood flow to the muscle leads to an increase in shear stress on the capillary endothelium and the contractile process induces passive stretch of the tissue. This mechanical impact promotes formation of angioregulatory factors, both pro‐ and antiangiogenic in nature. To what extent capillary growth occurs in the muscle is determined by the balance between the pro and the antiangiogenic factors. One of the most central proangiogenic factors is vascular endothelial growth factor (VEGF) which interacts closely with nitric oxide formed from endothelial nitric oxide synthase (eNOS), whereas thrombospondin‐1 (TSP‐1) may be a key antiangiogenic factor. Apart from muscle contraction, hypoxia can induce angiogenesis in part by an increase in the transcription factor hypoxia inducible factor‐1α (HIF‐1α) which promotes VEGF expression. However, the actual impact of hypoxia on human muscle capillarization is less certain. MMP: Matrix metalloproteinase, VEGF, vascular endothelial growth factor; eNOS: endothelial nitric oxide synthase; TSP‐1 thrombospondin.1; TIMP‐1: tissue inhibitor of matrix metalloproteinase; ANG: angiopoietin; PF‐4: platelet factor 4; Tie‐2: angiopoietin receptor 2.
Figure 11. Figure 11. Capillary‐to‐fiber ratio in relation to Myosin Heavy chain 1 (MHC I) positive muscle fibers in subjects of different fitness level (25‐65 mL O2 min−1 kg−1) and age (20‐71 years). Capillary number and muscle fibers were obtained by counting of immunohistochemically stained transverse muscle sections cut from frozen muscle (m.v. lateralis) samples. Data adapted, with permission, from (150) and Nyberg, Hellsten and Mortensen (previously unpublished data).
Figure 12. Figure 12. Time course of relative cardiovascular changes in response to endurance training. The relative changes in cardiovascular parameters in relation to duration of regular exercise training are estimated based on data from the literature on humans. The included data stem form healthy individuals and the training regimens used in the different studies range from moderate to high intensity aerobic exercise conducted for >30 min, 2 to 4 times per week. The data on well‐trained stem from individuals who have participated in endurance training for several years but that are not competing athletes. Note that for some of the parameters data only exist for a training duration of two months and the amount of data available for 6‐ and 12‐month durations of training is limited for all other variables. For all cardiovascular variables, it is clear that the largest change occurs at the onset of a training program, an effect that likely reflects that the signals for adaptation, for example, shear stress‐induced signaling, are the greatest at the onset of exercise training but then level off as adaptations occur. Figure A represents the time course of relative changes in Left ventricular (LV) end diastolic volume, maximal cardiac output, blood volume, and maximum oxygen uptake. Figure B represents the time course of relative changes in capillary to muscle fiber ratio, maximal skeletal muscle blood flow measured in the leg, FMD, arterial wall thickness, and arterial diameter of conduit arteries.


Figure 1. Heart rate (A), stroke volume (B), and cardiac output (C) in relation to systemic V· O2 in untrained and trained subjects and elite athletes.


Figure 2. Skeletal muscle sympathetic nervous activity (MSNA) during knee‐extensor exercise and venous norepinephrine concentrations during cycling exercise in the untrained and trained state. MSNA was measured by microneurography in the resting leg. Adapted from (346) and (457) with permission of the American Physiological Society. MSNA = Muscle sympathetic nerve activity.


Figure 3. Blood volume (A), erythrocyte and plasma volume (B), and hematocrit (C) in untrained and trained subjects and elite athletes.


Figure 4. Femoral arterial blood flow and arterio‐venous O2 difference during submaximal (A) and maximal (B) single leg knee‐extensor exercise with a previously immobilzed leg, untrained and trained leg. Immobilization lasted for 2 weeks and was achieved by casting. Blood flow was determined by ultrasound Doppler methodology, arterio‐venous oxygen extraction was obtained by measurements of oxygen content in blood drawn simultaneously from the femoral artery and femoral vein. Adapted from (292) and (298) with permission of the American Physiological Society.


Figure 5. Regulation of skeletal muscle blood flow during exercise. Several vasoactive mechanisms are involved in the regulation of skeletal muscle blood flow during exercise and together these mechanisms secure a highly precise oxygen delivery for the energy production required for the contractile work of the muscle. The vasodilator mechanisms include endothelial dependent vasodilatation which can be induced both by mechanical influence, primarily via shear stress, but also chemically via compounds such as ATP and adenosine. In response to the contractile work, skeletal muscle cells can produce and release vasodilator compounds including nitric oxide (NO) and ATP. NO and ATP can also be produced by red blood cells in response to off‐loading of oxygen from the hemoglobin molecule which occurs in the arterioles and capillaries. Coordination of blood flow in the microvascular system is facilitated by retrograde conducted vasodilation. In conducted vasodilation an electrical signal and a calcium wave travel in retrograde direction leading to vasodilatation in upstream arterioles. Finally, specific compounds such as ATP may reduce the efficacy of sympathetic activity in the skeletal muscle arterioles, thereby reducing the constrictive effect. ATP: Adenosine 5′triphosphate, NO: nitric oxide; ROS: reactive oxygen species; EDHF: endothelial‐derived hyperpolarizing factor.


Figure 6. The effect of endurance training on vasodilators and vasoconstrictors involved in the regulation of skeletal muscle blood flow. Skeletal muscle blood flow regulation is brought about by a balance between on one hand sympathetic vasoconstriction and other vasoconstrictors such as endothelin 1 (ET‐1) and thromboxane (TXA2) and on the other hand vasodilators formed in the active muscle, of which nitric oxide (NO) and prostacyclin (PGI2) appear to be central. Another important aspect in skeletal muscle blood flow regulation is the substantial interaction between vasodilator systems and compounds. For example, ATP and adenosine can mediate vasodilatation via activation of receptors on the endothelial cells resulting in the formation of NO and PGI2. NO and PGI2 in turn interact in a redundant manner so that when one is inhibited the other system can compensate. The effect of training on the formation of vasodilators and constrictors (marked by blue arrows) has not been fully clarified and the attempt to illustrate changes in this figure is tentative. Studies show that the concentrations of NO and prostacyclin in plasma and the muscle interstitium are either enhanced or remain unaltered at rest and during exercise. Adenosine and ATP levels in the muscle interstitium may increase with training, however, in parallel, the vascular sensitivity to nucleotides is reduced. On the constrictor side, ET‐1 and TXA2 have been shown to be reduced in plasma at rest whereas plasma noradrenaline is reduced during exercise indicating an attenuated sympathetic drive. ATP = Adenosine 5'triphosphate, ADO = adenosine; PGI2 = prostacyclin; NO = nitric oxide; NE = Noradrenaline, ET‐1 = endothelin‐1, TXA2 = thromboxane A2. p and i in figure beside blue arrows specify that changes were observed in plasma and muscle interstitium, respectively.


Figure 7. Femoral arterial blood flow during knee‐extensor exercise without and with arterial infusion of tyramine (induces a release of norepinephrine from sympathetic nerve endings) with a previously immobilized, untrained, and trained limb. Immobilization lasted for two weeks and was achieved by casting. Blood flow was determined by ultrasound Doppler methodology, arterio venous oxygen extraction was obtained by measurements of oxygen content in blood drawn simultaneously from the femoral artery and femoral vein. Adapted from (292) and (295) with permission.


Figure 8. Capillary‐to‐fiber ratio in untrained (VO2max: ∼50 mL O2 min−1 kg−1) young men before (0 weeks) and after 7 weeks of exercise training (7 weeks) and in trained (VO2max: ∼66 mL O2 min−1 kg−1) young men (cross‐sectional). The 7‐week training period consisted of high‐intensity interval training. Capillary number was obtained by counting of immunohistochemically stained transverse muscle sections cut from frozen muscle (m.v. lateralis) samples. Fitness level was determined by measurements of expired air during a graded cycle test to exhaustion. Adapted from (210) and (201) with permission.


Figure 9. Capillary‐to‐fiber ratio in relation to maximal oxygen uptake in young, middle‐aged, and older men of different training status. Capillary number and muscle fibers were obtained by counting of immunohistochemically stained transverse muscle sections cut from frozen muscle (m.v. lateralis) samples. Maximal oxygen uptake was determined by measurements of expired air during a graded cycle test to exhaustion. Data adapted, with permission, from (150,191,201) and from Andersen and Bangsbo (previously unpublished data) and Nyberg, Hellsten and Mortensen (previously unpublished data).


Figure 10. Dynamic muscle contraction provides mechanical signals of importance for capillary growth: the associated increase in blood flow to the muscle leads to an increase in shear stress on the capillary endothelium and the contractile process induces passive stretch of the tissue. This mechanical impact promotes formation of angioregulatory factors, both pro‐ and antiangiogenic in nature. To what extent capillary growth occurs in the muscle is determined by the balance between the pro and the antiangiogenic factors. One of the most central proangiogenic factors is vascular endothelial growth factor (VEGF) which interacts closely with nitric oxide formed from endothelial nitric oxide synthase (eNOS), whereas thrombospondin‐1 (TSP‐1) may be a key antiangiogenic factor. Apart from muscle contraction, hypoxia can induce angiogenesis in part by an increase in the transcription factor hypoxia inducible factor‐1α (HIF‐1α) which promotes VEGF expression. However, the actual impact of hypoxia on human muscle capillarization is less certain. MMP: Matrix metalloproteinase, VEGF, vascular endothelial growth factor; eNOS: endothelial nitric oxide synthase; TSP‐1 thrombospondin.1; TIMP‐1: tissue inhibitor of matrix metalloproteinase; ANG: angiopoietin; PF‐4: platelet factor 4; Tie‐2: angiopoietin receptor 2.


Figure 11. Capillary‐to‐fiber ratio in relation to Myosin Heavy chain 1 (MHC I) positive muscle fibers in subjects of different fitness level (25‐65 mL O2 min−1 kg−1) and age (20‐71 years). Capillary number and muscle fibers were obtained by counting of immunohistochemically stained transverse muscle sections cut from frozen muscle (m.v. lateralis) samples. Data adapted, with permission, from (150) and Nyberg, Hellsten and Mortensen (previously unpublished data).


Figure 12. Time course of relative cardiovascular changes in response to endurance training. The relative changes in cardiovascular parameters in relation to duration of regular exercise training are estimated based on data from the literature on humans. The included data stem form healthy individuals and the training regimens used in the different studies range from moderate to high intensity aerobic exercise conducted for >30 min, 2 to 4 times per week. The data on well‐trained stem from individuals who have participated in endurance training for several years but that are not competing athletes. Note that for some of the parameters data only exist for a training duration of two months and the amount of data available for 6‐ and 12‐month durations of training is limited for all other variables. For all cardiovascular variables, it is clear that the largest change occurs at the onset of a training program, an effect that likely reflects that the signals for adaptation, for example, shear stress‐induced signaling, are the greatest at the onset of exercise training but then level off as adaptations occur. Figure A represents the time course of relative changes in Left ventricular (LV) end diastolic volume, maximal cardiac output, blood volume, and maximum oxygen uptake. Figure B represents the time course of relative changes in capillary to muscle fiber ratio, maximal skeletal muscle blood flow measured in the leg, FMD, arterial wall thickness, and arterial diameter of conduit arteries.
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Article Title: Cardiovascular Adaptations to Exercise Training
 

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Ylva Hellsten, Michael Nyberg. Cardiovascular Adaptations to Exercise Training. Compr Physiol 2015, 6: 1-32. doi: 10.1002/cphy.c140080