(Hypertension. 1995;26:20-25.)
© 1995 American Heart Association, Inc.
Articles |
Flow-Diameter Phase Shift
A Potential Indicator of Conduit Artery Function
From the Division of Hypertension, Centre Hospitalier Universitaire Vaudois (CHUV), Lausanne, Switzerland (D.H., R. Weber); Department of Internal Medicine, University of Pavia and Istituto di Ricovero e Cura a Carattere Scientifico, S Matteo, Italy (L.B., C.P.); Department of Cardiology, Inselspital, Bern, Switzerland (G.N., R. Wenzel); and the Biomedical Engineering Laboratory, Swiss Federal Institute of Technology, Lausanne, Switzerland (C.-A.P., N.S.).
Correspondence to Daniel Hayoz, MD, Division of Hypertension, CHUV, 1011 Lausanne, Switzerland.
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Abstract |
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Abstract This study assesses (1) the relation of the very-low-frequency vasomotion (<0.02 Hz) of the radial artery of young healthy volunteers to regional blood flow and (2) its distribution in the upper extremities. Radial artery diameters from comparable sites were measured on contralateral extremities in 18 young healthy volunteers by an echo tracking system simultaneously with blood flow velocity determined by continuous wave Doppler and blood pressure acquired by photoplethysmography in the middle finger. A synchronous global pattern of vasomotion was detected on contralateral radial arteries, suggesting the presence of either a centrally located pacemaker or a humoral system. Modulation of sympathovagal balance in 8 subjects did not significantly alter either the frequency or amplitude of the very-low-frequency vasomotor waves. Matching patterns of diameter and flow oscillations of the very-low-frequency type recorded at the same site were obtained in 10 strictly nonsmoking volunteers for given periods of time. A consistent phase lag was observed between flow and diameter signals. Flow always preceded the diameter fluctuations by a mean (±SEM) course of 20.8±1.56 seconds. Although the physiological basis for oscillatory behavior remains for the moment highly speculative, these results suggest that the very-low-frequency vasomotion pattern in this conduit vessel might be a flow- or shear stress–dependent phenomenon. Shear stress changes at the endothelium modulate vascular tone through the release of vasodilators. The noninvasive assessment of the diameter-flow relation may thus offer a new way of addressing vascular wall function in medium-sized and large arteries in subjects with cardiovascular risk factors.
Key Words: ultrasonography • blood flow • radial artery
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Introduction |
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Vasomotion, defined as the cyclic variation of vascular basal tone with time, has been extensively studied in the microcirculation. Rhythmic constriction and dilation of arterioles have been observed in a wide variety of tissues and species, from bat wings1 to human skin.2 The primary mechanisms as well as the physiological significance of vasomotion are at the moment not clearly understood, although numerous hypotheses have been raised. Energy saving by decreasing the resistance of the vessels during vasomotion (Poiseuille's law),3 increasing the rapidity of responsiveness to circulatory demands,3 counteracting myogenic response to pressure changes,4 5 and thermoregulation mechanisms6 are commonly presented as a rational basis of vasomotion.
Because of the lack of appropriate tools, conduit artery vasomotion has not yet been studied in great detail. We recently reported the presence of a very-low-frequency (VLF; <0.02 Hz) and high-amplitude (80 µm) vasomotion in the radial artery of young healthy volunteers.7 The pulse pressure–independent VLF diameter changes of this medium-sized artery were not found to be related to either heart rate or pressure signal fluctuations in a linear fashion when coherence analysis of the power spectral components was performed. Furthermore, the repercussion of vasomotion on the biomechanical properties of this muscular artery has also been assessed in healthy volunteers and found to be independent of the blood pressure effect. A direct correlation between the internal diameter and the cross-sectional distensibility of the vessel has been observed under resting conditions.7 Pressure-independent, short-term variations in elastic properties of the femoral artery, a muscular conduit vessel, have also been reported in humans by noninvasive ultrasound technique.8
Results from in vitro and in vivo studies have clearly demonstrated that an increase in flow or in viscosity of the perfusate, both factors that enhance shear stress, elicited in most cases an endothelium-dependent vasodilation.9 10 11 12 13 However, the identity of the mediators responsible for the effect seems to be species and vessel type dependent.13 14 15 Furthermore, some constrictive responses to flow increase have also been observed in animal experiments.16 17
The present study was designed to investigate further vasomotion in a peripheral conduit artery under noninvasive physiological conditions in healthy volunteers. Two main questions were to be addressed: (1) Are the VLF diameter changes in the left and the right radial arteries synchronous, thus suggesting some central pacemaker? (2) Does blood flow exhibit similar VLF oscillations? If the answer is yes, how do these relate to the diameter changes? Using a high-resolution echo tracking technique, we were able to measure continuously the necessary hemodynamic parameters, thus lowering the variability due to repeated measurements. Occurrence of vasomotion in the upper extremities and its relation to blood flow pattern was measured under resting conditions and under well-defined controlled situations such as lower body negative pressure and neck suction, leading to stimulation and attenuation of sympathetic nerve activity, respectively.
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Methods |
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Subjects
Eighteen healthy volunteers (11 men and 7 women; mean age, 28 years; range, 21 to 37 years) were studied in the supine position in a quiet room maintained at a constant temperature of 22°C. Each had a normal physical examination. None of the subjects was taking medication. They were asked to refrain from smoking or drinking coffee before the experiment. All subjects were informed of the nature of the study and gave their oral consent. The protocol of the study was approved by the Hospital Ethics Committee.
Hemodynamic Measurements
All measurements were performed simultaneously on
both sides after electrocardiogram leads and a
strain-gauge respiration strap (built in our laboratory) had been
placed. The diameter measurements were performed after 30 minutes of
rest on the radial arteries, 5 cm proximal to the wrist. The supinated
arms were placed in a splint to avoid involuntary movements. A
description of the measuring device (NIUS 02, Asulab SA), which is an
upgraded version of an apparatus that used hardware
tracking,7 18 and reproducibility data have been reported
previously.19 Briefly, the ultrasonic echoes reflected by
the interfaces between blood and both anterior and posterior walls
(radio frequency echo line) were sampled at 100 MHz and stored at a
repetition frequency of 500 Hz. The vascular interfaces were
subsequently selected by the operator on the radio frequency echo line
and automatically tracked to obtain the diameter and its variation over
time. The exact position of each selected interface was obtained by
calculating the real-time position of the maximum of the corresponding
peak in the radio frequency line. The initial resolution given by the
100-MHz sampling frequency (corresponding to a spatial depth of 7.5
µm) was improved to approximately 1 µm. The diameter signal was
finally stored at 50 Hz. The reduction from the repetition frequency to
this final sampling frequency was performed by averaging 10 samples,
which allowed reductions in both noise and memory requirement.
Blood pressure was measured in the middle finger by a photoplethysmographic instrument (Finapres, Ohmeda) linked to the ultrasonic echo tracking device. This apparatus provides noninvasive continuous recordings of finger blood pressure with a resolution of 0.25 kPa (2 mm Hg). This technique has been studied extensively and described in detail elsewhere.20
Forearm blood flow velocity was measured by continuous- wave Doppler (8-MHz transducer at a 60° angle, Doptek 2002) distal to the 10-MHz probe, aimed at the site of diameter measurements. No interferences between the two waves were noted throughout the duration of the experiment. Resting blood flow (in milliliters per minute) is the product of time-averaged mean velocity and arterial cross-sectional area obtained simultaneously from the arterial diameter. Capillary skin blood flow was measured by laser Doppler flowmetry (LDF) (Perimed PF3) with unheated skin probes. Flow motion was recorded with identical skin probes placed on two correspondent volar surfaces of the right and left thumb fingers.
Lower Body Negative Pressure and Neck Suction
Subjects were positioned in a Plexiglas chamber sealed at their
iliac crest and tightly secured by a belt to avoid displacement into
the chamber when vacuum was turned on. The negative pressure at -40
mm Hg was applied manually with a vacuum cleaner. The chamber pressure
was monitored with the use of a solid-state manometer. The neck suction
was applied by means of a molded lead collar connected to a vacuum
cleaner whose power was modulated by a second computer (Apple II, Apple
Inc) equipped with a 12-bit digital-to-analog board through a
phase-control power unit. Neck suction could thus be generated with a
predetermined signal shape and frequency and pressure swing (from 0.02
to 0.2 Hz with 0 to -40 mm Hg suction swing).21
The data, with the exception of diameter and flow signals, were digitized on-line by a 12-bit analog-to-digital convertor (NB-MIO-16 board; National Instruments) at a sampling rate of 500 Hz for each channel. The convertor was connected to a Macintosh II computer (Apple Inc).
Power Spectral Analysis
Power spectral analysis was performed on diameter and
blood flow signals with the use of an autoregressive
model.22 Spectral components were obtained by a
decomposition method to measure the area below each spectral
peak.22 According to the autoregressive model, each peak
identifies the presence of an oscillatory component; however, to
distinguish between signal and noise, only components above 5% of
total variability were considered real. Three frequency bands were
considered: a VLF band (<0.02 Hz), a low-frequency band (from 0.03 to
0.15 Hz), and a high-frequency band (from 0.18 to 0.35 Hz).
Coherence Analysis
To assess the phase stability of pairs of
oscillations with identical frequencies (blood flow and
diameter), we applied a squared coherence function. This is a
mathematical bivariate spectral analysis method that allows
determination of the presence of a blood flow–related diameter
fluctuation. As the correlation coefficient, this function spans from 0
(no relationship between the two signals) to 1 (strong relationship).
The squared coherence function was evaluated by an autoregressive
algorithm with the use of the method described by Baselli et
al.23 With their method, only spectral components with
high squared coherence (>0.5) were considered to demonstrate a
significantly stable phase relationship between the two signals.
Statistical Analysis
Coherence function was used as a statistical test for each pair
of oscillations.
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Results |
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VLF oscillations were consistently identified in the diameter and the flow signals but not in blood pressure or heart rate. The VLF vasomotion of the radial arteries was present in the 18 subjects studied but with varying amplitudes (range, 40 to 180 µm). However, the cyclic variation of diameters displayed different patterns. Fairly periodic signals, as previously described,7 were identified in 5 of the 18 subjects, whereas in the remaining 13 volunteers a somewhat random pattern of vasomotion was observed (Fig 1). The time series of the diameter signals obtained simultaneously at both radial arteries showed superimposable patterns without a significant phase lag between opposite sides, as shown in the top panel of Fig 2, confirming earlier findings by Porret et al.24 This is further emphasized by the squared coherence function analysis between the diameter signals obtained over a few periods (5 minutes) of the VLF oscillations. Indeed, the high squared coherence demonstrated the presence of a linear relationship between the two diameters in all subjects (values >0.5). When longer time series (20 minutes) were analyzed, the function yielded values less than 0.5, suggesting a transient absence of linearity between the two signals. The loss of congruency resulted either from the occasional occurrence of a spontaneous vasoconstrictive activity originating most likely from local sources (Fig 2, bottom panel) or from the absence of a vasomotion cycle. These local constrictions neither significantly altered the baseline cyclic variation of diameter nor influenced the regional or distal blood flow pattern, as assessed in the latter case by LDF. Sporadically, VLF diameter oscillations disappeared unilaterally for very short periods of time (one or two complexes). Skin blood flow recorded by LDF in both thumbs disclosed synchronous patterns that were closely related to those obtained in the radial arteries, although brief periods with loss of synchronization were also observed (Fig 3).
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Similar VLF fluctuations of regional blood flow were also identified in all volunteers. They showed matching contralateral patterns and always preceded luminal changes. However, the characteristic frequency responses (inertia) of the two signals differed significantly. Indeed, as shown in Fig 4, the diameter signal displayed a dampened response when compared with blood flow. Furthermore, a consistent phase lag between the cyclic variations of blood flow and of diameter was obtained in all volunteers. Fig 5 shows the flow-related diameter oscillation as expressed by the squared coherence function between the diameter and flow signals. A value greater than 0.5 was obtained for the two signals at the three previously described frequency components, with a negative phase shift between them. The negative sign means that the second signal (flow) precedes the first one (diameter). The time delay between the signals was found to be very stable and averaged 20.8±1.56 seconds in the 10 nonsmoking volunteers (mean±SEM). The effects of sympathovagal stimulation on vasomotion of the conduit artery did not significantly alter the baseline cyclic variations of diameter. Simulation of orthostatic stress by applying -40 mm Hg to lower body or rising carotid sinus transmural pressure by neck suction (40 mm Hg) had no effect on either frequency or amplitude of the VLF diameter oscillations during application of the respective stimuli. A delayed vasoactive response cannot be formally excluded since the recording periods did not exceed stimulation time. At 0.1 Hz, the sinusoidal neck suction did, however, accentuate synchronization of blood pressure, heart rate, and cutaneous vasomotion at low-frequency (0.1 Hz) and high-frequency (0.25 Hz) oscillations without affecting slower components. No coherence between the respiratory cycle and the VLF oscillations of flow or diameter was observed.
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Discussion |
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In this study we demonstrated (1) the similitude of cyclic variation of blood flow and diameter with a stable phase lag between the two parameters and (2) the symmetrical vasomotion pattern in the radial arteries and in the cutaneous microvasculature. Therefore, it seems most unlikely that the VLF diameter oscillations identified in the radial artery are modulated by local pacemaker activity as previously suggested7 25 26 or originate from propagative mechanisms.27 Indeed, the symmetrical and synchronous distribution of the vasoactive waves in both arms suggests that they are controlled by a central vasomotor source. Synchronous VLF vasomotion in the cutaneous microcirculation has recently been observed in humans by LDF when both hands were tested.28 The synchronicity of the LDF waves was observed on average during 60% of the total observation time. Here we show that the baseline pattern of VLF may at times be disturbed by unilateral spontaneous contractile activities that most likely originate from local pacemakers without perturbation of its baseline oscillatory activity. Episodic loss of unilateral vasoactive complexes was also encountered in the volunteers during the longest recordings. Synchronicity of vasomotion in the microcirculation measured by LDF in both thumbs was observed in all subjects studied. The microcirculation and macrocirculation were mostly related, although occasionally this synchronicity was not apparent.
The demonstration of a high squared coherence between blood flow and diameter spectral components suggests that a blood flow–related fluctuation in diameter exists. The presence of a phase lag between flow and diameter (flow leading diameter) implies that the absence of immediate diameter dilation induces an increase in flow velocity that raises shear stress at the conduit artery. Regional flow oscillation resulting from cyclic variations of the microvasculature patency may translate into modulation of the release of vasomediators in the radial artery in an effort to maintain constant shear stress in a feedback mechanism.29 The lack of coherence between the components of blood pressure and diameter signals, as previously described, makes a myogenic response to intravascular pressure changes an unsatisfactory explanation for the observed cyclic variations discussed here.5 On the other hand, a nonlinear relationship between blood pressure fluctuation and blood flow versus diameter responses cannot be formally excluded since the analysis applied here does not allow testing for this possibility.
Modulation of the sympathovagal balance by applying lower body negative pressure and neck suction did not significantly alter the pattern of VLF cyclic variation of blood flow or diameter, although blood pressure and heart rate responded appropriately to these stimuli. To assess whether vasoactive substances could be responsible for the observed synchronization, simultaneous recordings of the parameters in the upper and lower extremities remain to be performed. However, we did study a 23-year-old woman 1 year after bilateral surgical thoracic sympathectomy (T2-4) because of hyperhydrosis. Synchronicity of flow and diameter fluctuations of very low amplitude were preserved, although the patient was clinically cured of her sweating problem in both upper extremities, which argues against possible reinnervation (data not shown). The absence of modification of the VLF vasomotion in the conduit artery during sympathovagal stimulation and the preservation of synchronicity 1 year after sympathectomy suggest that the control mechanism does not necessarily follow the neurovegetative network. However, this does not completely rule out a possible role of the autonomic nervous system.
Vasomotion remains a very complex phenomenon. Nevertheless, we demonstrate here the existence of a flow-related diameter fluctuation in the radial artery. It has been shown in vitro that conduit as well as resistance vessels display spontaneous periodic vasomotion30 31 whose frequency and amplitude depend on a pressure-sensitive myogenic response32 33 34 and on the frequency and amplitude of pulsatile flow.35 Here in vivo flow changes due to nonperiodic cyclic variation in patency of the microcirculation may further transform spontaneous periodic activity into a more chaotic pattern by way of a shear stress negative feedback mechanism. Although the nature of the vasodilators remains for the moment controversial, study of the coupling in the time domain of the two signals may provide a noninvasive way to assess vascular responsiveness to stress modifications. In vitro studies have revealed that the delay between the increase in diameter elicited by an increase in perfusion was on the order of 20 seconds, a value similar to the one observed here.12
Within a cardiac cycle the mean blood flow fluctuation is on average greater than the VLF cycle, contrasting with the diameter dynamics (Fig 6). A mechanoreceptor system sensitive to shear stress changes, behaving as a low-pass filter with respect to its input stimulus, must then be responsible for transducing shear stress changes to intracellular effectors. Because of the time delay caused by the biochemical processes involved in vasomotion, only the slower changes in shear stress can be adequately sensed by the endothelial cells. Analysis of the coupling of flow and diameter signals may provide a tool to unmask functional alterations long before structural lesions occur in subjects exposed to cardiovascular risk factors. Further studies aimed at assessing this flow-diameter phase lag among selected groups of subjects will clarify the usefulness of this noninvasive approach.
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