Oxygen delivery to skeletal muscle fibers: effects of microvascular unit structure and control mechanisms

Abstract

The number of perfused capillaries in skeletal muscle varies with muscle activation. With increasing activation, muscle fibers are recruited as motor units consisting of widely dispersed fibers, whereas capillaries are recruited as groups called microvascular units (MVUs) that supply several adjacent fibers. In this study, a theoretical model was used to examine the consequences of this spatial mismatch between the functional units of muscle activation and capillary perfusion. Diffusive oxygen transport was simulated in cross sections of skeletal muscle, including several MVUs and fibers from several motor units. Four alternative hypothetical mechanisms controlling capillary perfusion were considered. First, all capillaries adjacent to active fibers are perfused. Second, all MVUs containing capillaries adjacent to active fibers are perfused. Third, each MVU is perfused whenever oxygen levels at its feed arteriole fall below a threshold value. Fourth, each MVU is perfused whenever the average oxygen level at its capillaries falls below a threshold value. For each mechanism, the dependence of the fraction of perfused capillaries on the level of muscle activation was predicted. Comparison of the results led to the following conclusions. Control of perfusion by MVUs increases the fraction of perfused capillaries relative to control by individual capillaries. Control by arteriolar oxygen sensing leads to poor control of tissue oxygenation at high levels of muscle activation. Control of MVU perfusion by capillary oxygen sensing permits adequate tissue oxygenation over the full range of activation without resulting in perfusion of all MVUs containing capillaries adjacent to active fibers.

Muscle Architecture and its Relationship to Muscle Circulation

“…Furthermore, MVU was not precisely aligned along the muscle fiber(s) (Emerson and Segal 1997), and rather spread to neighboring muscle fiber(s). This finding implies that blood flow cannot selectively increase to a specific muscle fiber or to a particular group of fibers, because whenever any capillary is perfused, all other capillaries in the same MVU are necessarily also perfused (Emerson and Segal 1997, Fuglevand and Segal 1997, Lo, et al, 2003. On the other hand, the muscle fibers belonging to the same MU are distributed diversely within the muscle.…”

“…On the other hand, the muscle fibers belonging to the same MU are distributed diversely within the muscle. Accordingly, a spatial mismatching occurs between perfused capillaries and activated muscle fibers (Lo, et al, 2003) (Figure 8). A simulation study by Fuglevand and Segal (1997) demonstrated that the widespread dispersion of MU fibers facilitates complete capillary (MVU) perfusion of muscle at low level activity.…”

Image-based modelling of skeletal muscle oxygenation

“…However, an investigation and verification of the usefulness of Voronoi tessellations to describe oxygenation volumes in 3D problems has not yet been conducted and remains to be shown. Most image-based models of tissue oxygen perfusion are based on 2D image data, and namely on histological images [65,139,142]. This is mainly due to the lack of relevant 3D datasets and/or efforts to reduce computing time.…”

Multi-scale Computational Models of Pro-angiogenic Treatments in Peripheral Arterial Disease

“…1). 3,9,14,20,27,30,[38][39][40]42,59,62 This threedimensional model is used in calculations of blood flow and oxygen distributions. However, due to the complexity of the system and the number of the parameters that are of physiological interest, we choose a twodimensional cross section of the tissue (400 · 208 lm 3 , boxed in Fig.…”