Muscle microvascular hemoglobin concentration and oxygenation within the contraction–relaxation cycle
Introduction
Rhythmic muscle contractions cause oscillations of inflowing arterial (Barcroft and Dornhorst, 1949, Lutjemeier et al., 2005, Walloe and Wesche, 1988) and outflowing venous (Grassi et al., 1996, Richardson and Saltin, 1998) blood flow. However, technological constraints have precluded analysis of any oscillatory patterns in microvascular blood volume and their effects on blood-myocyte gas exchange within the contraction cycle in human muscle. Even with analysis of muscle blood flow and kinetics, the tacit assumption has been that O2 exchange proceeds unimpeded and uniformly across the contraction–relaxation cycle (Grassi et al., 1996).
Notwithstanding the above, contraction-induced increases in intramuscular pressure have been considered to at least partially evacuate the muscle vascular bed (Vedsted et al., 2006) which would account for the retrograde arterial (Hoelting et al., 2001, Lutjemeier et al., 2005, Walloe and Wesche, 1988) and anterograde venous (Ameredes and Provenzano, 1997, Vedsted et al., 2006) blood “spurts.” If the source of these blood spurts was the microcirculation, in addition to intervening large arteriolar and venular sites, the reduction in microvascular red blood cell (RBC) volume during contraction would reduce or abolish the potential for blood-myocyte O2 delivery and relegate that delivery to the following relaxation phase. Such behavior would reduce the effective mean capillary RBC transit time and mandate a higher O2 flux density from each RBC during relaxation. In addition, because intramyocyte phosphocreatine concentration falls and those of phosphagen-linked mitochondrial controllers (e.g., free ADP, inorganic phosphate) rise rapidly during the contractile phase of the contraction cycle (Chung et al., 1998), the O2 supply would be decreasing at the very instant that O2 demand were rising.
In marked contrast to the notion that the microvascular bed is emptied of RBCs during contraction, Gray et al. (1967) demonstrated that maximal tetanic contractions did not cause microvascular collapse in the rat spinotrapezius muscle, while Poole et al. (1992) observed RBCs in myocardial capillaries during barium-induced hypersystole. These latter findings suggest that during the muscle contractile phase RBCs would be present in the capillaries – albeit at a reduced flux – to facilitate continued myocyte O2 delivery. Resolution of this issue in human muscle(s) during exercise is crucial for construction of O2 transport models that have physiological validity (Pittman, 2000).
Near infrared spectroscopy (NIRS) technology can track changes in muscle total hemoglobin/myoglobin concentration (total [Hb/Mb]) as well as that of oxygenated and deoxygenated (Hb/Mb) (as oxy-[Hb/Mb] and deoxy-[Hb/Mb], respectively) (DeLorey et al., 2004, Grassi et al., 2003, Kowalchuk et al., 2002). Recent advances in NIRS technology now allow for very rapid sampling (Gratton et al., 1997), providing the temporal resolution necessary to dynamically examine muscle microvascular hemoglobin concentration and oxygenation dynamically within the contraction–relaxation cycle. We conducted the experiment described herein to test the following hypotheses: (1) Microvascular total [Hb/Mb] would be preserved during contraction, and (2) there would be a cyclical pattern of deoxygenation/oxygenation that corresponded with the contraction/relaxation phases of the contraction cycle.
Section snippets
Subjects
Seven male and one female volunteer participated in the study. The physical characteristics of the subjects were (mean ± standard deviation): age 23 ± 2 years, height 175 ± 9 cm, and weight 71 ± 13 kg. Experimental procedures and all possible risks and discomforts associated with the experiment protocol were explained to each subject prior to their providing written consent. This study was approved by the Institutional Review Board for Research Involving Human Subjects at Kansas State University, where
Validation protocol
The responses of one subject during the validation protocol are shown in Fig. 1. Note that the level of noise or variability in each of the NIRS channels did not change from rest to passive movement. Further note that, in this subject, both the deoxy-[Hb/Mb] and oxy-[Hb/Mb] signals showed a progressive emergence of oscillations in concert with active contractions (Exercise), with deoxy-[Hb/Mb] increasing and oxy-[Hb/Mb] decreasing in approximate symmetry, such that total [Hb/Mb] did not change
Discussion
Two principal new findings arise from the present study. First, microvascular RBC volume was preserved during muscle contractions. Thus, RBCs are present in the capillaries – albeit at a reduced flux – which could facilitate continued oxygen delivery to the myocyte. Second, there was a cyclical pattern of deoxygenation/oxygenation that corresponded with the contraction/relaxation phases of the contraction cycle, with deoxy-[Hb/Mb] increasing significantly during the contractile phase. This
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