Mechanical influences on skeletal muscle vascular tone in humans: insight into contraction‐induced rapid vasodilatation

Abstract

We tested the hypothesis that mechanical deformation of forearm blood vessels via acute increases in extravascular pressure elicits rapid vasodilatation in humans. In healthy adults, we measured forearm blood flow (Doppler ultrasound) and calculated forearm vascular conductance (FVC) responses to whole forearm compressions and isometric muscle contractions with the arm above heart level. We used several experimental protocols to gain insight into how mechanical factors contribute to contraction-induced rapid vasodilatation. The findings from the present study clearly indicate that acute increases in extravascular pressure (200 mmHg for 2 s) elicit a significant rapid vasodilatation in the human forearm (peak ΔFVC∼155%). Brief, 6 s sustained compressions evoked the greatest vasodilatation (ΔFVC∼260%), whereas the responses to single (2 s) and repeated compressions (five repeated 2 s compressions) were not significantly different (ΔFVC∼155% versus ∼115%, respectively). This mechanically induced vasodilatation peaks within 1-2 cardiac cycles, and thus is dissociated from the temporal pattern normally observed in response to brief muscle contractions (∼4-7 cardiac cycles). A non-linear relation was found between graded increases in extravascular pressure and both the immediate and peak rapid vasodilatory response, such that the responses increased sharply from 25 to 100 mmHg, with no significant further dilatation until 300 mmHg (maximal ΔFVC∼185%). This was in contrast to the linear intensity-dependent relation observed with muscle contractions. Our collective findings indicate that mechanical influences contribute largely to the immediate vasodilatation (first cardiac cycle) observed in response to a brief, single contraction. However, it is clear that there are additional mechanisms related to muscle activation that continue to cause and sustain vasodilatation for several more cardiac cycles after contraction. Additionally, the potential contribution of mechanical influences to the total contraction-induced hyperaemia appears greatest for low to moderate intensity single muscle contractions, and this contribution becomes less significant for sustained and repeated contractions. Nevertheless, this mechanically induced vasodilatation could serve as a feedforward mechanism to increase muscle blood flow at the onset of exercise, as well as in response to changes in contraction intensity, prior to alterations in local vasodilating substances that influence vascular tone.

Positional differences in reactive hyperemia provide insight into initial phase of exercise hyperemia

“…Additionally, experiments measuring blood flow to the canine hindlimbs (14,15) indicate that vasodilation is necessary for the immediate hyperemia at the onset of muscle contraction. Studies published over the last decade have provided evidence for the involvement of adenosine (2), potassium (8,9), and vascular compression (6,16,37) in rapid vasodilation of the skeletal muscle resistance vasculature.…”

Evidence that the contraction-induced rapid hyperemia in rabbit masseter muscle is based on a mechanosensitive mechanism, not shared by cutaneous vascular beds

“…However, a recent study indicates that K ϩ , released by con-tracting muscle fibers, could also mediate an early dilatory effect (2), which leaves the issue unsettled. Based on the similarity in the rapid hyperemic responses that have been reported in different preparations in response to short-lasting muscle contractions and mechanical stimuli (6,8,10,18,24,33,38,47), we hypothesized that a single mechanosensitive mechanism, activated by changes in transmural pressure, could underlie the different responses. Moreover, since it has been proposed that this rapid hyperemia is functionally meant to provide a prompt increase in muscle perfusion at the onset of exercise (9), we aimed to investigate whether this reactivity to the mechanical stimulus was differently exhibited by muscular and cutaneous vascular beds.…”

“…A third issue concerns the accuracy in detecting the latency of the rapid dilatation with respect to muscle contraction, which is crucial to discriminate between the faster mechanical vs. the slower metabolic mechanism. Based on different experimental models, such latency is currently reported to be "Ͻ1 s" (24,33,41,47), which is considered too short for the metabolic action to develop (11, 50). However, a recent study indicates that K ϩ , released by conAddress for reprint requests and other correspondence: S. Roatta, Dip.…”

“…They showed, in fact, that the rapid hyperemia provoked by a 1-s tetanic stimulation of the isolated calf muscle of the dog could be reproduced, although with lower magnitude, by a brief external compression of the muscle performed through an inflatable cuff (31). The concept of a mechanically induced dilatation has recently found renewed support, based on in vitro (10) as well as in vivo studies performed on several animal models (19, 33), including humans (6,11,24). In particular it has been shown that the increase in extravascular pressure could induce the rapid dilatation of an isolated muscle artery (10) and that the rapid blood flow increase evoked by a brief handgrip was closely reproduced by a brief external compression of the forearm (6, 24).…”

“…The concept of a mechanically induced dilatation has recently found renewed support, based on in vitro (10) as well as in vivo studies performed on several animal models (19,33), including humans (6,11,24). In particular it has been shown that the increase in extravascular pressure could induce the rapid dilatation of an isolated muscle artery (10) and that the rapid blood flow increase evoked by a brief handgrip was closely reproduced by a brief external compression of the forearm (6,24). These data led some authors to reconsider the myogenic response as one of the possible mechanisms behind the exercise-induced rapid dilatation (10,11,14).…”