The effects of aging on capillary hemodynamics in contracting rat spinotrapezius muscle

Abstract

Advancing age alters the structural and functional determinants of convective and diffusive muscle oxygen (O 2 ) flux. However, capillary red blood cell (RBC) hemodynamics have not been investigated during contractions in muscles of old animals. PURPOSE:To test the hypothesis that aging induces significant alterations in capillary hemodynamics during electrically-induced contractions in the spinotrapezius muscle of old Fischer 344 x Brown Norway rats when compared to younger counterparts.

Dynamics of muscle microcirculatory and blood–myocyte O2 flux during contractions

“…It is known that, due in part to the endothelial surface layer (often termed the ‘glycocalyx’), there are differential flow rates of plasma and RBCs within and among capillaries such that microvascular hematocrit in resting muscle is far below systemic (e.g., Klitzman and Duling, 1979; Sarelius and Duling, 1982; Desjardins and Duling, 1987,1990; Kindig and Poole, 1998, 2001; Poole et al 1997; Frisbee and Barclay, 1998; Kindig et al 2002; Copp et al 2009). Thus, from rest to exercise an increased microvascular hematocrit towards systemic (Klitzman and Duling, 1979; Kindig et al 2002; Copp et al 2009) may therefore, in theory, raise muscle [hemoglobin] as much as 2–3 fold. Accordingly, if we were to accept that most (say 80%, a figure in the range of common usage) of capillaries did not flow at rest and were recruited during exercise, muscle [hemoglobin] would be expected to increase up to four-fold from this effect alone, and with increased microvascular hematocrit, this could be several-fold higher again.…”

“…2. Capillary hematocrit increases from ~15% towards systemic levels (~45%, Klitzman and Duling, 1979; Kindig et al 2002; Copp et al 2009) such that, in the extreme, each capillary may contain up to 2–3 times as many RBCs during exercise compared with rest thereby increasing the instantaneous O 2 diffusive conductance (DO 2 , Federspiel and Popel, 1986; Groebe and Thews, 1990; Malvin and Wood, 1992). An elevated capillary hematocrit increases the likelihood that transverse histological sections will transect an RBC within a given capillary.…”

“…Poole et al 2005) as well as by advanced age (Babcock et al 1994; Chilibeck et al 1998; Barstow and Scheuermann, 2005), and there is evidence that this slowing occurs consequent to O 2 delivery limitation as schematized in Figure 8. Intravital microscopy of spinotrapezius muscles from Type II diabetic (Padilla et al 2006), CHF (Kindig et al 1999; Richardson et al 2003) and aged (Russell et al 2003; Poole and Ferreira, 2007; Copp et al 2009) animals offers mechanistic insights into how deficits in microvascular function contribute to perfusive and diffusive impediments in the O 2 transport pathway. One expression of these impediments is the mismatching of O 2 delivery-to- V̇ O 2 which often produces aberrant P mv O 2 profiles particularly during the first 30–60 seconds following the onset of contractions and during recovery (Figure 9, Diederich et al 2002; Behnke et al 2004; McDonough et al 2004; Poole et al 2005; Ferreira et al 2006; Behnke et al 2007; Poole and Musch, 2010; Hirai et al 2009).…”

Slower V˙O2 Kinetics in Older Individuals

“…Related to this, older rats have shown a reduced lineal density of RBC-perfused capillaries running next to a fiber, which is compensated at rest by increases in RBC velocity so that O 2 delivery is similar in both old and young rats (75). However, old rats exposed to electrically induced muscle contractions do not display the same increase in capillary RBC velocity that their younger counterparts exhibit (19). In addition, it has been demonstrated that old rats exhibit a transiently reduced microvascular pressure of O 2 across the rest-contractions transition that is likely to impair O 2 exchange from the capillaries to the fibers (6).…”

Acute ascorbic acid and hindlimb skeletal muscle blood flow distribution in old rats: rest and exercise

“…For example, older subjects demonstrate attenuated arteriolar vasodilation in response to acetylcholine (Kirby et al 2009) and muscle contractions (Jackson, et al 2010) that results in a reduction (Proctor et al 2004;Schrage et al 2007;Copp et al 2009) and (or) maldistribution of skeletal muscle blood flow away from highly oxidative and towards more glycolytic muscle fibers (Musch et al 2004;Hirai et al 2011a) when compared with younger counterparts. These impairments conspire to reduce maximum O 2 uptake and exercise tolerance in elderly subjects (Posner et al 1986;McGuire et al 2001) and impact negatively upon quality of life.…”