Competition for blood flow distribution between respiratory and locomotor muscles: implications for muscle fatigue

Abstract

Sympathetically induced vasoconstrictor modulation of local vasodilation occurs in contracting skeletal muscle during exercise to ensure appropriate perfusion of a large active muscle mass and to maintain also arterial blood pressure. In this synthesis, we discuss the contribution of group III-IV muscle afferents to the sympathetic modulation of blood flow distribution to locomotor and respiratory muscles during exercise. This is followed by an examination of the conditions under which diaphragm and locomotor muscle fatigue occur. Emphasis is given to those studies in humans and animal models that experimentally changed respiratory muscle work to evaluate blood flow redistribution and its effects on locomotor muscle fatigue, and conversely, those that evaluated the influence of coincident limb muscle contraction on respiratory muscle blood flow and fatigue. We propose the concept of a "two-way street of sympathetic vasoconstrictor activity" emanating from both limb and respiratory muscle metaboreceptors during exercise, which constrains blood flow and O₂ transport thereby promoting fatigue of both sets of muscles. We end with considerations of a hierarchy of blood flow distribution during exercise between respiratory versus locomotor musculatures and the clinical implications of muscle afferent feedback influences on muscle perfusion, fatigue, and exercise tolerance.

Keywords: blood flow; diaphragm; exercise; metaboreflex; sympathetic vasoconstriction; work of breathing.

Fig. 1.

Summary of the effects of unloading the inspiratory muscles during heavy-intensity exercise. Shown are representative within-breath esophageal (A: P_es) and transdiphragmatic pressure-time (B: P_di) traces for 1 subject ensemble averaged over 1 min during spontaneous breathing (control) and proportional assist ventilation (PAV) at exercise iso-time. Note that with the use of PAV the esophageal and P_di during inspiration were reduced by 50–70% vs control. Tracings from Romer et al. .

Fig. 2.

Schematic of a “2-way street of sympathetic vasoconstrictor activity” emanating from both limb and respiratory muscle metaboreceptors during exercise, which serves to constrain blood flow and O₂ transport. High-intensity contractions of both sets of muscles causes increased group III and IV afferent activity leading to a sympathetically mediated vasoconstriction of respiratory and limb locomotor muscle vasculatures, thereby contributing to their mutual fatigue during whole body exercise.

Fig. 3.

Blood flow to inspiratory (A) and expiratory (B) muscles of ponies at rest at rest and during maximal exercise. Data are from Manohar . EXT. OBL. ABD., external oblique abdominis; INT. OBL. ABD., internal oblique abdominis; TRANS. ABD., transverse abdominis; RECUTS ABD, rectus abdominis; TRANSV. THORACIS, transverse thoracis. Note, that without exception blood flow to the respiratory musculature during maximal exercise was significantly increased relative to resting conditions. Note that blood flow to the diaphragm exceeded 300 ml·min⁻¹·100g⁻¹; neither diaphragm flow or vascular conductance was increased further upon infusion of a vasodilator during maximal exercise.

Fig. 4.

Respiratory muscle blood flow during maximal exercise. Shown are 3 distinct approaches to assessing respiratory muscle blood flow that yield comparable estimates of the fraction of cardiac output. Harms et al. (33) determined leg blood flow (thermodilution) during bouts of maximal exercise in trained cyclists (V̇o_2max = 62 ml·kg⁻¹·min⁻¹). Respiratory muscle work was either unaltered (control condition), reduced (proportional assist ventilator), increased (resistive load). Blood flow to the respiratory muscles was assumed to be equal to a measured fall in cardiac output obtained with respiratory muscle unloading at V̇o_2max and extrapolated to zero work of breathing. Calbet et al. (17) studied healthy active men (V̇o_2max = 49 ml·kg⁻¹·min⁻¹; 3.7 l/min) who performed upright cycle exercise to exhaustion while blood flow to the arms and legs was determined (thermodilution). Blood flow to the “trunk” was calculated as the difference between cardiac output and arm and leg blood flow and included into a lumped parameter the blood flow directed to the head, neck, heart, abdominal viscera, kidneys, respiratory muscles, and gluteal muscles. Manohar (51) injected radionuclide-labeled microspheres into the left ventricle of maximally exercising ponies, and blood flow increased significantly in all respiratory muscles. Blood flow was measured in inspiratory and expiratory muscles (individual muscles are shown in Fig. 3).

Fig. 5.

Metabolic and hemodynamic responses during incremental exercise and isocapnic resting hyperpnoea. Data are from Vogiatzis et al. (83). Oxygen uptake (A), cardiac output (B), heart rate (C), stroke volume (D), intercostal muscle blood flow (E), and quadriceps muscle blood flow (F) at different levels of minute ventilation during exercise (△) and isocapnic, resting hyperpnoea (▲). Muscle blood flow was determined using near-infrared spectroscopy and indocyanine green (ICG) (see text). Values are means ± SE for 10 subjects. †Significant differences (P < 0.05) between exercise-induced hyperpnea and voluntary hyperpnea at rest at comparable levels of ventilation. Note that intercostal muscle blood flow increased progressively with mild- through moderate-intensity exercise, plateaued, and fell to resting levels as exercise intensity increased further; whereas intercostal blood flow increased progressively with increasing ventilation during voluntary hyperpnea at rest.

Fig. 6.

Individual values for sternocleidomastoid (A), vastus lateralis (B), and vastus medialis (C) blood flow index and work of breathing during cycling exercise at 85% of maximal work rate. Open shapes represent the respiratory muscle unloading condition with the proportional assist ventilator (PAV) and filled shapes represent the respiratory muscle loading condition with increased airway resistance. SCM, sternocleidomastoid; VL, vastus lateralis; VM, vastus medialis; WOB, work of breathing. Note that SCM flow increases and limb flow decreases with respiratory muscle loading and the SCM flow decreases and limb flow increases with respiratory muscle unloading. These findings demonstrate that respiratory muscle work significantly influences the distribution of blood flow to both respiratory and locomotor muscles under conditions of intense exercise. Data are from Dominelli et al. (25).