Effects of exercise hyperaemia

In resting muscle, where there is a relatively high precapillary vasoconstrictor tone, mean capillary hydrostatic pressure and plasma oncotic pressure are both around 25 mmHg, so that there is a balance between inwardly and outwardly directed pressure gradients and no net water movement occurs across the capillary wall. When the muscle arterioles dilate with onset of exercise, however, the resulting fall in precapillary resistance automatically raises capillary hydrostatic pressure, to values as high as 50–60 mmHg when the arterioles are maximally dilated. Because this is far above the opposing oncotic pressure value, net extravasation of plasma water takes place until the resultant increase in interstitial hydrostatic pressure is sufficient to rebalance the outward/inward forces (Fortney et al 1981). At least at high muscle workloads, the outward water movement is increased further by the rise in interstitial osmolality caused by accumulation of muscle metabolites.

Since skeletal muscle makes up such a large proportion of total body mass, the volume of extravasated fluid within the muscles during whole-body dynamic exercise can be appreciable. At relatively heavy workloads, 10–12% of plasma volume (around 300 ml in a 70 kg person) is lost over the initial 10 min of activity (Fig. 9.1). Thus, over this period cardiac output also falls by around 300 ml provided heart rate remains constant, necessarily reducing muscle blood flow. Moreover, plasma loss results in a concomitant rise in haematocrit, elevating blood viscosity and so increasing cardiac workload.

Figure 9.1 Typical timecourse of plasma volume reduction during maintained exercise. Note the rapid fall due to muscle extravasation (1) and the slower decline associated with sweating (2). The delayed onset of pronounced sweating reflects the time taken for metabolic heat to accumulate in muscle and to diffuse from muscle to bloodstream.

Effect of heat production

Muscle activity generates metabolic heat and, therefore, potentially elevates core body temperature. Even at high work intensities, it takes at least several minutes for this heat to diffuse into the circulation and be detected by the hypothalamic thermostat. The initial stage of exercise is, therefore, independent of thermoregulatory considerations. As soon as cardiac output is warmed by more than around 0.01° C, however, compensatory heat loss processes begin to be activated. These impose new, increasingly severe limitations on the amount of blood available for muscle perfusion.

As mentioned in Chapter 6 (p. 68), the first of these processes is withdrawal of sympathetic vasoconstrictor tone from the cutaneous arterioles. In parallel, there is activation of cholinergic sympathetic nerves to eccrine sweat glands. Both the loss of sympathetic tone and the process of sweat production cause cutaneous vasodilation. As a result, skin blood flow rises from a resting value that is typically less than 500 ml/min at environmental temperatures below 25° C to as much as 3 l/min after 15–20 min of sustained heavy exercise, with a similar fall in muscle blood flow. The dilatation due to sweating is at least partly secondary to glandular release of kinins (see Chapter 6, p. 75) but may also involve release of unknown dilator factors from the sudomotor nerve endings (Joyner & Halliwill 2000). As well as serving to convey heat to the body/environment interface, the high skin blood flow is essential to provide water and electrolytes for sweat production. This typically reaches a maximum of around 1 l/h, but may be as high as 2 l/h in a person who exercises routinely in hot conditions.

Sweating produces a second phase of plasma volume reduction that typically becomes measurable around 20 min after commencement of exercise (Fig. 9.1). Although in theory plasma and interstitial fluids are in equilibrium, high rates of sweat production draw primarily on the plasma, so that blood volume falls and haematocrit rises progressively as the exercise bout continues. Both effects make muscle oxygenation progressively more and more inefficient.

Measurement of sweating

A wide range of techniques are available for measuring sweat production, but none are suitable for all applications. Choice of technique depends critically on the intensity of sweat secretion to be measured and the duration of measurement required. All techniques in routine use involve one of four basic principles, as summarized below.

Heart rate drift

During sustained dynamic exercise, heart rate begins to drift upwards from its previously stable level. The drift is prevented almost entirely by adequate fluid replacement during exercise, confirming that it involves reflex sympathetic compensation for the progressive fall in circulating plasma volume. In addition, prolonged muscle activity tends to involve progressive recruitment of larger numbers of muscle units as compensation for fatigue of those first recruited. Since greater descending motor drive is associated with greater activation of the cardiovascular centre, this also increases cardiac sympathetic drive.

The functional consequence of heart rate drift is further encroachment on ventricular filling time, introducing another factor that acts to limit muscle perfusion. Heart rate drift also needs to be borne in mind when absolute heart rate is being used to set training intensity, since 30 min whole-body activity at intensities of 80% or higher is associated typically with a drift of up to 15 beats/min.

Competition with other metabolically active tissues

Consideration of partitioning of cardiac output during exercise usually assumes that the only significant competition occurs between locomotor muscle and skin circulations, as discussed above. There are, however, two situations in which additional competitions must be considered.

One of these is that, in large-bodied, highly trained athletes, the metabolic demand of the respiratory muscles can be a potential limiting factor in locomotor muscle perfusion during intense activity (Dempsey et al 2006). In other subjects the amount of tissue involved is not sufficient to impose a significant perfusional load but, even so, it is possible that chemoreceptor inputs from metabolite build-up in respiratory muscles may contribute to the sensation of fatigue during intense activity.

Second, although the exercise response relies on increased, sympathetically mediated peripheral resistance in the splanchnic circulation, this is effective only while the metabolic rate of the splanchnic tissues remains low. Ingestion of a substantial meal within 1–2 h of exercise will activate gastric, hepatic and intestinal metabolism, and the associated splanchnic hyperaemia due to release of local metabolites and hormones must limit the absolute blood flow available to active skeletal muscles. More importantly, because skeletal muscle and splanchnic beds are the two regions that contribute most to peripheral resistance changes during regulation of blood pressure, overriding sympathetic tone in both of them simultaneously makes it extremely difficult to maintain a blood pressure gradient adequate for effective muscle perfusion.

Figure 9.2 adds these limiting factors to our flow chart of the matrix of responses to exercise.

Figure 9.2 Expansion of Figure 8.3, with the factors discussed in this chapter denoted in red.

Temperature and humidity

Since the need for heat loss imposes major limitations on muscle blood flow, it is predictable that environments that affect thermoregulatory efficiency will influence exercise capacity. Thus, time to fatigue is increased under cold conditions due to both reduced skin blood flow and sweating (Blanchet et al 2003). During rapid exposure to a very cold environment (such as on immersion in cold water) there is profound cutaneous vasoconstriction that can result in dramatic elevation of blood pressure and it is possible that, even with less extreme activation of skin cold receptors, the pressure gradient for muscle perfusion during exercise will be somewhat higher than under thermoneutral conditions. It is, however, not known whether this has any real effect on the efficiency of muscle perfusion.

The redistribution of cardiac output associated with reduced cutaneous perfusion leads to increased renal blood flow, glomerular filtration and urine formation (cold diuresis). In addition, the reduced humidity of cold air means that there is an increase in evaporative water loss associated with ventilation. While these factors provide additional sources of fluid loss during prolonged exercise, effective blood volume is usually conserved by the lower rate of sweating.

In cold environments, other issues that combine circulatory and thermoregulatory considerations may complicate the situation further. Thus, varying efficiencies of insulative clothing may create microenvironments that range from one that tends towards producing hypothermia due to evaporative and convective cooling to one that retards heat loss so much that it produces hyperthermia. In addition, extreme cold especially in windy conditions can overwhelm the cold dilator response that normally protects digits, ears and nose (see Chapter 5, p. 58) and result in freezing of cells in these tissues (frostbite).

Hot environments will reduce time to fatigue because of greater skin blood flow and of more rapid depletion of plasma volume by sweating. In addition, environmental humidity has a profound influence because it dictates the efficiency of sweat evaporation. Under conditions of high relative humidity, evaporation may be virtually eliminated and so sweating produces no heat loss. In response, sweat production is increased. This may result in maximal sweat production and substantial plasma volume loss (up to 2 l/h) at work rates that would, under dry conditions, produce only trivial sweating.

Even without taking into consideration the progressive encroachment on circulatory performance caused by hot conditions, absolute exercise capacity is lower in the heat. Expansion of vascular volume caused by generalized dilation of the cutaneous veins reduces venous return and so lowers stroke volume. As a result, maximal heart rate is reached at a cardiac output that may be as little as 80% of that achieved under thermoneutral conditions, and maximum work capacity is reduced correspondingly.

Aquatic vs. terrestrial exercise

The relative inefficiency of swimming due to the high density of the medium is to some extent countered by the absence of some of the problems that limit terrestrial exercise. The high thermal conductivity of water means that heat loss occurs very rapidly and without the need for massive cutaneous vasodilation or sweating. As well, effective circulating blood volume is increased, both by lack of gravitational pooling and by the fact that the external pressure of the water compresses the superficial veins. Together, these factors allow muscle perfusion to be a higher proportion of cardiac output than during terrestrial activity and for it to be maintained stable for far longer periods.

Breath-hold swimming underwater triggers a unique pattern of reflex cardiovascular changes, consisting of bradycardia and a generalized increase in peripheral resistance that includes vasoconstriction of skeletal muscle blood vessels. Extensive experimentation has shown that in diving animals, such as seals, this so-called diving response can produce heart rates as low as 5–10 beats/min, with almost complete cessation of blood flow through the exercising skeletal muscles. This reduces dramatically the rate of oxygen consumption and carbon dioxide production and allows these animals to undertake dives that may last for more than 30 min. In man, the diving response is much less pronounced.

Specialized diving species have powerful sympathetic innervation of the larger arteries supplying limb muscles, so they can shut off blood flow external to the muscles. By contrast, blood flow to exercising muscles in man falls only moderately because the vasoconstrictor innervation is localized to the microcirculation within the muscle, so its effect is opposed by the vasodilator effect of local metabolites. As a result, muscle perfusion and consequent build-up of carbon dioxide in the bloodstream cannot be avoided, and breath-holding is possible for only 1–2 min at most before arterial hypercapnia activates the central chemoreceptors and produces an irresistible urge to breathe.

Children

Old age

Although the increasingly sedentary lifestyle that often accompanies ageing itself limits exercise, increasing age can also be shown to be associated with significant changes in cardiovascular correlates of exercise.