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Multiple mechanisms involved in regulating blood flow during exercise

This is an excerpt from Advanced Neuromuscular Exercise Physiology by Phillip Gardiner.


Muscle Blood Flow
During exercise, blood flow increases in working muscle as a function of workload, and the relationship is quite linear (Saltin et al. 1998). Muscle perfusion during exercise for a sedentary individual is about 250 milliliters per minute in 100 grams of tissue, and it can rise to 400 milliliters per minute in trained athletes (Saltin et al. 1998; Saltin 2007). Mechanical and biochemical mechanisms cause this increased muscle blood flow. However, the blood available for exercising muscles is not limitless—exercising at a high intensity with 15 kilograms of muscle (about 50% of the total muscle mass of a 75-kilogram man) can exceed the heart’s capacity to supply blood. Athletes such as cross-country skiers, who use their arms and legs at relatively high intensities for prolonged durations, experience this limit in blood availability. Therefore, there must be in place mechanisms that increase blood flow when there is metabolic demand as well as mechanisms that cause active muscles to undergo some level of vasoconstriction during exercise (Rowell 1997). During high blood flow, sympathetically mediated vasoconstriction is necessary to maintain peripheral resistance in order to maintain blood pressure (Saltin 2007). When metabolic rates and blood flow demands are high, such as when the arms and legs are working simultaneously, noradrenaline spillover from the legs helps to counteract the strong local vasodilator signals and helps to maintain central pressure.

Here we discuss some of the general physiological mechanisms that maintain blood pressure when muscle demands for oxygen delivery are high and also the local mechanisms that match blood flow to metabolic demand. As we shall see, there are many proposed mechanisms controlling exercise blood flow, with perhaps a significant degree of redundancy, so that finding the role played by individual mechanisms has not been possible to date.

Oxygen Delivery as the Regulated Parameter
What is the regulated variable in blood flow regulation? It appears to be oxygen delivery, and not blood flow per se, at least from studies in which arterial oxygen content has been decreased. Flow adjusts accordingly to achieve the appropriate oxygen delivery to the working muscle (Marsh and Ellerby 2006). The regulation of blood flow by oxygen delivery appears to be restricted to the oxygen bound to hemoglobin, since experiments have shown a close relationship between blood flow and oxygen bound to hemoglobin, independent of partial pressure of oxygen in blood (Gonzalez-Alonso et al. 2001). The relationship between blood flow and oxygen demand is also supported by the observation that blood flow appears to be a linear function of oxygen consumption, independent of the fiber type composition of the muscle (Marsh and Ellerby 2006). In addition, blood flow is related more to the metabolic rate of the contractile activity than to the work performed (Hamann et al. 2004, 2005).

There are several ways in which blood flow may be regulated by the oxygen content of the blood and, more specifically, the saturation level of hemoglobin. Hemoglobin may, via conformational and redox transitions, stimulate the release of vasodilator substances such as nitric oxide (NO), S-nitrosylated thiols, nitrite, and adenosine
triphosphate (ATP). Such a mechanism would help explain the close relationship between venous hemoglobin saturation and venous blood flow (Calbet et al. 2007; Gonzalez-Alonso et al. 2001).

Functional Sympatholysis
A rise in sympathetic nerve activity with exercise causes vasoconstriction in nonmuscular regions and also in inactive and active muscles. Mechanisms are in place to override active muscle vasoconstriction in an attempt to match blood flow to metabolic demand while maintaining blood pressure. One way this occurs is via functional sympatholysis, which is an inhibition of the sympathetically mediated vasoconstrictor response in active muscle as long as blood pressure is maintained. This is probably due to substances produced in the contracting muscle that inhibit alpha-1 or alpha-2 adrenergic receptor activation by the noradrenalin (NA) released from the nerve terminals. NO may be the blocker, although conflicting results have been reported (Dinenno and Joyner 2003; Saltin 2007; Tschakovsky and Joyner 2008; see later discussion). Adenosine may also play this role. It has also been demonstrated that the receptors for endothelin-1 (ET-1), endothelin receptor type A (ETA) and type B (ETB), may also play a role in muscle blood flow regulation during exercise. Like the blunting of adrenoreceptor sensitivity that occurs with exercise, responsiveness to the powerful vasoconstrictor ET-1 is also diminished during exercise by currently unknown metabolic mechanisms (Wray et al. 2008).

 

Mechanical Events
Investigators have demonstrated in elegant experiments that mechanical events alone can explain at least the initial rapid increase in muscle blood flow. Using the hamster cremaster microvascular preparation, Mihok and Murrant (2008) demonstrated that single electrically evoked contractions of 3 to 5 fibers (lasting 250-500 milliseconds) produced significant dilations in the arterioles overlapping these fibers. Clifford and colleagues (2006) carried this further to measure vasodilatation in isolated feed arteries of rat soleus muscles in response to externally applied pressure pulses. Their results also showed that mechanical stimuli alone result in vasodilatation. These researchers also denuded arterioles of the epithelium and found that the response was reduced but not eliminated. This finding demonstrated that the mechanical response of vasculature is mediated by both epithelial-dependent and epithelial-independent mechanisms.

Tschakovsky and colleagues (2004) measured changes in forearm blood flow resulting from single 1-second isometric contractions at intensities ranging from 5% to 70% of MVC. Their results demonstrated that there is a rapidly acting vasodilation that is proportional to muscle activation and is influenced by local arterial driving pressure (since flow increases were greater when the arm was below heart level).

Kirby and colleagues (2007) demonstrated the importance of extravascular pressure on the initial increases in muscle blood flow. In their studies, they compared immediate increases in blood flow resulting from pressure induced by inflating pressure cuffs around the muscle with voluntary and electrically evoked contractions. Their results demonstrated quite clearly the importance of mechanical influences on the rapid vasodilatation that occurs at the beginning of contraction. While the immediate increase (within two cardiac cycles) appears to be totally attributable to mechanical factors, other factors are involved in determining the peak flow response to contractile activity (Kirby et al. 2007). Generally, the results from these experiments demonstrated quite convincingly that mechanical factors are most important at the beginning of contractile activity, giving time for the release, accumulation, and diffusion of other substances that then play major roles in sustaining blood flow and matching it to metabolic demand.

There is little evidence that muscle pump plays a significant role as a mechanical factor in controlling muscle blood flow during exercise. While muscle pump does play a role, its contribution is modest in determining muscle blood flow, and it is not required for sustaining venous return, central venous pressure, stroke volume, or cardiac output during exercise (Gonzalez-Alonso et al. 2008; Tschakovsky et al. 1996).



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