Skeletal muscle blood flow capacity: role of muscle pump in exercise hyperemia

Jasperse JL, Shoemaker JK, Gray EJ, Clifford PS. Positional differences in reactive hyperemia provide insight into initial phase of exercise hyperemia. J Appl Physiol 119: 569 -575, 2015. First published July 2, 2015; doi:10.1152/japplphysiol.01253.2013.-Studies have reported a greater blood flow response to muscle contractions when the limb is below the heart compared with above the heart, and these results have been interpreted as evidence for a skeletal muscle pump contribution to exercise hyperemia. If limb position affects the blood flow response to other vascular challenges such as reactive hyperemia, this interpretation may not be correct. We hypothesized that the magnitude of reactive hyperemia would be greater with the limb below the heart. Brachial artery blood flow (Doppler ultrasound) and blood pressure (finger-cuff plethysmography) were measured in 10 healthy volunteers. Subjects lay supine with one arm supported in two different positions: above or below the heart. Reactive hyperemia was produced by occlusion of arterial inflow for varying durations: 0.5 min, 1 min, 2 min, or 5 min in randomized order. Peak increases in blood flow were 77 Ϯ 11, 178 Ϯ 24, 291 Ϯ 25, and 398 Ϯ 33 ml/min above the heart and 96 Ϯ 19, 279 Ϯ 62, 550 Ϯ 60, and 711 Ϯ 69 ml/min below the heart (P Ͻ 0.05). Thus a standard stimulus (vascular occlusion) elicited different responses depending on limb position. To determine whether these differences were due to mechanisms intrinsic to the arterial wall, a second set of experiments was performed in which acute intraluminal pressure reduction for 0.5 min, 1 min, 2 min, or 5 min was performed in isolated rat soleus feed arteries (n ϭ 12). The magnitude of dilation upon pressure restoration was greater when acute pressure reduction occurred from 85 mmHg (mimicking pressure in the arm below the heart; 28.3 Ϯ 7.9, 37.5 Ϯ 5.9, 55.1 Ϯ 9.9, and 68.9 Ϯ 8.6% dilation) than from 48 mmHg (mimicking pressure in the arm above the heart; 20.8 Ϯ 4.8, 22.6 Ϯ 4.4, 31.2 Ϯ 5.8, and 49.2 Ϯ 7.1% dilation). These data support the hypothesis that arm position differences in reactive hyperemia are at least partially mediated by mechanisms intrinsic to the arterial wall. Overall, these results suggest the need to reevaluate studies employing positional changes to examine muscle pump influences on exercise hyperemia. muscle blood flow; muscle contraction; skeletal muscle pump; functional hyperemia AT THE ONSET OF DYNAMIC EXERCISE, there is a rapid increase in blood flow [30,31,41, and see Fig. 2 in Clifford and Hellsten (5)]. In fact, even a single muscle contraction produces a prompt increase in blood flow (1,7,14,26,36,39). There has been a debate over the last few decades about whether this rapid hyperemia is due to the muscle pump mechanism or to rapid vasodilation (5, 35).The muscle pump, as described by Laughlin (20), depends on an increased pressure gradient across the skeletal muscle vascular bed. Muscle contraction compresses the veins within the contracting muscle, expelling blood from the veins. ...

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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

Jasperse

Shoemaker

Gray

et al. 2015

“…Several studies have compared the hyperemia induced by a single contraction with that evoked by a brief increase in external pressure (6,24,31). While this approach provided good evidence of a mechanically dependent hyperemia, it did not help in understanding the possible contribution by the "muscle pump" mechanism (26,45). In fact, both maneuvers squeeze and empty intramuscular vessels, thus reducing venous blood pressure and increasing perfusion pressure (muscle pump).…”

Section: The Rapid Hyperemic Response To Brief Spontaneous Contractionsmentioning

confidence: 99%

“…First of all, external compression of the forearm is not an unequivocal means to induce a myogenic response since the compression-induced depletion of venous compartments may contribute to the hyperemia according to the muscle pump mechanism (26,45). Surprisingly, the contraction-induced hyperemia has never been directly compared with the response to artery occlusion, which would overcome this limitation.…”

mentioning

confidence: 99%

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

Turturici

Mohammed

Roatta

2012

Turturici M, Mohammed M, Roatta S. Evidence that the contraction-induced rapid hyperemia in rabbit masseter muscle is based on a mechanosensitive mechanism, not shared by cutaneous vascular beds. J Appl Physiol 113: 524 -531, 2012. First published June 7, 2012 doi:10.1152/japplphysiol.00237.2012.-Several mechanisms have been hypothesized to contribute to the rapid hyperemia at the onset of exercise. The aim of the present study was to investigate the role played by the mechanosensitivity of the vascular network. In 12 anesthetized rabbits blood flow was recorded from the exclusively muscular masseteric artery in response to brief spontaneous contractions (BSC) of the masseter muscle, artery occlusion (AO), muscle compression (MC), and muscle stretch (MS). Activation of masseter muscle was monitored by electromyography (EMG). Responses to AO were also recorded from the mostly cutaneous facial and the central ear arteries. Five animals were also tested in the awake condition. The hyperemic response to BSC (peak amplitude of 394 Ϯ 82%; time to peak of 1.8 Ϯ 0.8 s) developed with a latency of 300 -400 ms from the beginning of the EMG burst and 200 -300 ms from the contractioninduced transient flow reduction. This response was neither different from the response to AO (peak amplitude ϭ 426 Ϯ 158%), MC, and MS (P ϭ 0.23), nor from the BSC response in the awake condition. Compared with the masseteric artery, the response to AO was markedly smaller both in the facial (83 Ϯ 18%,) and in the central ear artery (68 Ϯ 20%) (P Ͻ 0.01). In conclusion, the rapid contractioninduced hyperemia can be replicated by a variety of stimuli affecting transmural pressure in muscle blood vessels and is thus compatible with the Bayliss effect. This prominent mechanosensitivity appears to be a characteristic of muscle and not cutaneous vascular beds. muscle stretch; myogenic response; rapid dilatation; reactive hyperemia; muscle compression SKELETAL MUSCLE BLOOD FLOW has long been known to exhibit a rapid increase at the onset of exercise (1,9,12,22,27). The mechanisms behind this phenomenon are still a matter of debate despite the many new insights provided by different research groups in recent years. In particular it has been shown that the contraction-induced compression of venous compartments (muscle pump) cannot fully account for the blood flow increase and that the additional occurrence of a rapid active dilatation is required (18,33,45,46). Other studies have shown that this rapid dilatation is mediated neither by changes in sympathetic neural drive (7, 41), nor by ACh spillover from the motor endplate (6, 33), nor by endothelium-released NO (6), although this last assertion is debated (see DISCUSSION). As early as 1974, Mohrman and Sparks (31) hypothesized that the rapid dilatation could result from the myogenic response of muscle blood vessels to decreased transmural pressure, which in turn results from the increase in intramuscular (extravascular) pressure produced by the contraction. They showed, in fact, that the rapid hypere...

“…As the muscle contracts, it compresses the veins within the muscle and expels the venous contents toward the heart. On relaxation, it is hypothesized that the muscle fibers that are tethered to the walls of the veins open the lumen of the compliant vessels and create low pressure (7,9). Because the venous circulation contains one-way valves, oneway flow is ensured, and the enhanced arteriovenous pressure gradient results in an increase in arterial inflow to skeletal muscle (7).…”

mentioning

confidence: 99%

Muscle blood flow response to contraction: influence of venous pressure

Valić

Buckwalter²,

Clifford³

2005

The skeletal muscle pump is thought to be at least partially responsible for the immediate muscle hyperemia seen with exercise. We hypothesized that increases in venous pressure within the muscle would enhance the effectiveness of the muscle pump and yield greater postcontraction hyperemia. In nine anesthetized beagle dogs, arterial inflow and venous outflow of a single hindlimb were measured with ultrasonic transit-time flow probes in response to 1-s tetanic contractions evoked by electrical stimulation of the sciatic nerve. Venous pressure in the hindlimb was manipulated by tilting the upright dogs to a 30°angle in the head-up or head-down positions. The volume of venous blood expelled during contractions was 2.2 Ϯ 0.2, 1.6 Ϯ 0.2, and 1.4 Ϯ 0.2 ml with the head-up, horizontal, and head-down positions, respectively. Although altering hindlimb venous pressure influenced venous expulsion during contraction, the increase in arterial inflow was similar regardless of position. Moreover, the volume of blood expelled was a small fraction of the cumulative arterial volume after the contraction. These results suggest that the muscle pump is not a major contributor to the hyperemic response to skeletal muscle contraction. exercise; hyperemia; muscle pump; vasodilation; dog IT IS WELL KNOWN THAT, DURING EXERCISE, there is an elevation in blood flow to exercising skeletal muscle. The muscle pump is hypothesized to elevate skeletal muscle blood flow by mechanical factors (16). As the muscle contracts, it compresses the veins within the muscle and expels the venous contents toward the heart. On relaxation, it is hypothesized that the muscle fibers that are tethered to the walls of the veins open the lumen of the compliant vessels and create low pressure (7, 9). Because the venous circulation contains one-way valves, oneway flow is ensured, and the enhanced arteriovenous pressure gradient results in an increase in arterial inflow to skeletal muscle (7).Studies employing both human and animal models have shown that skeletal muscle blood flow is significantly elevated within 1 s after the release of a brief tetanic contraction (1,15,19). Despite this rapid blood flow response in vivo, direct observations of arteriolar diameter reveal that dilation of the skeletal muscle arterioles occurs more slowly (4, 6, 21). Because activation of the muscle pump is temporally compatible with the immediate increase in blood flow seen at the onset of exercise, this observation has been used as prima facie evidence that the muscle pump must be responsible for the rapid increase in skeletal muscle blood flow with the initiation of exercise (16).Fundamental to the muscle pump theory of blood flow control is that muscular contraction lowers venous pressure within the active muscle, thus widening the arteriovenous pressure gradient. However, the relationship between venous pressure within the muscle before contraction and the ability of the muscle pump to produce skeletal muscle hyperemia is a question open for investigation (8). In the present stu...