Skeletal muscle vasodilatation during maximal exercise in health and disease

Abstract

Maximal exercise vasodilatation results from the balance between vasoconstricting and vasodilating signals combined with the vascular reactivity to these signals. During maximal exercise with a small muscle mass the skeletal muscle vascular bed is fully vasodilated. During maximal whole body exercise, however, vasodilatation is restrained by the sympathetic system. This is necessary to avoid hypotension since the maximal vascular conductance of the musculature exceeds the maximal pumping capacity of the heart. Endurance training and high-intensity intermittent knee extension training increase the capacity for maximal exercise vasodilatation by 20-30%, mainly due to an enhanced vasodilatory capacity, as maximal exercise perfusion pressure changes little with training. The increase in maximal exercise vascular conductance is to a large extent explained by skeletal muscle hypertrophy and vascular remodelling. The vasodilatory capacity during maximal exercise is reduced or blunted with ageing, as well as in chronic heart failure patients and chronically hypoxic humans; reduced vasodilatory responsiveness and increased sympathetic activity (and probably, altered sympatholysis) are potential mechanisms accounting for this effect. Pharmacological counteraction of the sympathetic restraint may result in lower perfusion pressure and reduced oxygen extraction by the exercising muscles. However, at the same time fast inhibition of the chemoreflex in maximally exercising humans may result in increased vasodilatation, further confirming a restraining role of the sympathetic nervous system on exercise-induced vasodilatation. This is likely to be critical for the maintenance of blood pressure in exercising patients with a limited heart pump capacity.

Figure 1. High heterogeneity of skeletal muscle blood flow in humans

Mean blood flow (A) and relative dispersion of blood flow (B) in the different portions of the quadriceps femoris muscle measured with positron emission tomography and H₂¹⁵O during intermittent leg extension isometric contractions (Kalliokoski et al. 2000). *P < 0.01 rest versus exercise, †P < 0.001versus resting RF and VL, ‡P < 0.001 versus exercising RF and VL, §P < 0.001 versus resting VL. VL: vastus lateralis; RF: rectus femoris, VM: vastus medialis; VI: vastus intermedious.

Figure 2. The combined vasodilatory capacity of the arm and leg muscles exceeds the pumping capacity of the heart (Calbet et al. 2004a)

Cross-country skiers were studied during submaximal (76% ) skiing while using arm and legs (diagonal technique), only arm (double poling technique) and leg skiing (like skating). They were also studied during maximal exercise with the diagonal technique. Trunk and head perfusion at maximal diagonal was calculated by subtracting peak leg and arm blood flows from peak cardiac output. The maximal theoretical cardiac output was calculated by adding the maximal values that were observed for leg blood flow (during maximal diagonal), the peak arm blood flow (observed during double poling) and the 5 l min⁻¹ of blood flow necessary to perfuse the head and trunk. The latter gave 4 l min¹ more cardiac output than actually measured, implying that in humans with well trained arm and leg muscles the combined peak perfusion of the head trunk and arm muscle exceeds the pumping capacity of the heart. This also implies that during maximal upright arm and leg combined exercise, muscle vasodilatation must be restrained to avoid hypotension. (Figure from Calbet & Joyner, 2010.)

Figure 3. Changes in peak leg blood flow after three different knee extension training programs: anaerobic intervalic (Ana I), aerobic intervalic (Aer I), and submaximal aerobic (Sub A)

The three groups improved similarly their peak leg by 32%, and this improvement was due to a 30% increase in leg blood flow (Whole group) (Blomstrand et al. 2011).

Figure 4. Maximal post-ischaemic vasodilatation in the dominant and non-dominant arms of tennis players and control subjects with similar , measured with plethysmography after 5 min of arterial occlusion coupled with 1 min of exercise

In the tennis players maximal forearm hyperaemia was 42% higher in the dominant than in the non-dominant forearm (Sinoway et al. 1986).

Figure 5. Relative change in brachial artery flow mediated dilatation from baseline in response to ischaemic exercise across the 8-week handgrip exercise training in healthy young men

One arm was trained with a cuff around the arm inflated at 60 mmHg to prevent shear stress. Error bars represent SEM. *P < 0.05 between the cuffed and non-cuffed arm (Tinken et al. 2010).