Local control of large arteries buffering function: role of the vascular smooth muscle.
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1 Local control of large arteries buffering function: role of the vascular smooth muscle. Bia D., Grignola J., Craiem D., Zócalo., Ginés F., Armentano R. Dpto. de Fisiología, Facultad de Medicina, Montevideo, Uruguay. Universidad Favaloro, Buenos Aires, Argentina ABSTRACT Introduction: The buffering function (BF) of large arteries is determined by the arterial wall mechanical properties and exerts a protective action to the heart as well as to the arterial system itself: it decreases heart work and it favors ventricular-arterial coupling maintaining arterial impedance with minimal change; it decreases arterial wall fatigue by pulsatile stress and it allows an almost continuous flow to reach the capillaries. Objective: We compared the viscoelastic properties of the aorta and pulmonary arteries and the effects of vascular smooth muscle (VSM) activation on the local and global BF. Material and methods: Aortic and pulmonary artery pressure and diameter were measured in six anesthetized sheep during: basal condition, arterial hypertension produced by passive mechanical occlusion (PH), and by pharmacological activation of VSM through i/v phenylephrine (AH). Elasticity (E) and viscosity (η) were calculated (Kelvin-Voigt), and buffering function was characterized a) local, by a parietal time constant or η/e ratio, and b) global of each circuit, by the diastolic time constant of pressure, τ (Windkessel). Results: Aortic viscoelasticity was higher than pulmonary (p<0.05), however both arteries had similar parietal buffering function. The systemic circuit presented a higher global buffering function (p<0.05). During PH, E was significantly increased without h modification, and with a significantly reduction of η/e and τ in both arteries. During AH, h increased (p<0.05), meanwhile η/e and t returned to basal values. Conclusions: Aorta presented a higher viscoelasticity than pulmonary artery, with a similar η/e ratio. Systemic t was higher than pulmonary circuit. While E depends on intravascular pressure, η is a marker of the amount and grade of VSM activation. The VSM activation could be benefit to the cardiovascular system maintaining the BF during arterial hypertension. We propose a local control of large arteries BF depending on the modulation of VSM activation. INTRODUCTION The flow and pressure waves caused by the ventricular activity must be softened or buffered by the large arterial system to ensure an optimal and continuous peripheral blood supply [1]. Indeed, the buffering function exerts a protective action to the heart as well as to the arterial system itself: it decreases heart work and it favors ventricular-arterial coupling; it decreases arterial wall fatigue by pulsatile stress and it allows an almost continuous flow to reach the capillaries [1,2]. In both, pulmonary and systemic circuits, the global buffering function (GBF) is determined by vascular (i.e. vascular length and cross-section, arterial wall properties, site dependent summation of incident and reflected pulses) and blood (i.e. viscosity) factors [3]. The aorta (AO) and main pulmonary artery (PA), contribute to the buffering by means of their arterial wall buffer function (WBF). The WBF is mainly determined by the arterial wall elastic and viscous properties and not only by the pure elastic properties (distensibility or compliance) [1]. The acute changes in the arterial wall elastic (E) and viscous modulus (η) are due to (a) the mechanical effect of arterial pressure (P) variations, and [2] functional modifications of vascular smooth muscle (VSM) tone [2,4,5]. The direct effect of VSM activation on the viscoelastic behavior of large arteries is a controversial topic [6]. The non-linearity in the wall artery pressure-diameter (P-D) relation is the most important problem in the analysis of the direct VSM effects. When VSM activation modify directly the arterial wall viscoelasticity, the simultaneous P increase caused by peripherial (arteriolar) constriction, provoke a P -dependent change in the arterial wall properties. To separate the direct, P-independent (or intrinsic) and the P-dependent changes, an isobaric analysis with and without VSM activation is necessary [5,7,8,9,10]. Arterial viscoelasticity under VSM activation has been studied in the systemic circulation [5,8]. However, to our
2 knowledge, no study assessing the effect of the in vivo VSM activation on viscoelastic properties of the PA has been reported. Additionally, no connection was established between the Aortic (AO) and pulmonary artery (PA) segmental or local wall viscoelastic behaviour, and the whole systemic and pulmonary circulation behavior, respectively. OBJECTIVE The goal of this study was to determine the in vivo local PA and ascending AO viscoelastic properties and the direct effects of large arteries VSM activation, on the WBF and GBF. MATERIAL AND METHODS: Surgical preparation Six adult sheep were anesthetized and the respiration was maintained with a positive P ventilator (Dragger SIMV Polyred 201, Spain). The ascending AO, and the PA and its main branches (left and right pulmonary arteries), were exposed through a left thoracotomy. A P microtransducer (Konigsberg Instruments, Inc., Pasadena, CA) was inserted in the ascending AO and PA through a stab wound. To measure external AO and PA diameter (D), ultrasonic crystals (5 MHz) were sutured to the adventitia of each artery, and connected to a sonomicrometer (Triton Technology Inc. San Diego, CA). Two cuff occluder were implanted around (a) the left pulmonary artery and (the thoracic descending AO, at least mm distally from ultrasonic crystals. This ensured that no artifacts appeared in D measurements during arterial occlusions. Experimental Protocol After surgical instrumentation, P and D signals were recorded and stored during three steady-state conditions: 1) Control or normal pressure steady state (NPS). 2) Active hypertension (AHT): systemic and pulmonary hypertension induced by Intravenous infusion of phenylephrine (PHE, 5 mg/kg/min, Sigma, St. Louis, MO). 3) Passive hypertension (PHT): systemic and pulmonary hypertension provoked by occlusion of the left pulmonary artery and the descending AO. After acquisition of the NPS the occluders were compressed in order to obtain a high-pressure non-active state for 5 seconds. Pressure levels were established to ensure isobaric conditions between this maneuver and the AHT [5,8,10]. Ten minutes were allowed to elapse between these interventions to return to control values. During PHE infusion the instantaneous P and D recordings were monitored until stabilization was achieved. A lapse of minutes were generally enough to ensure a steady state under PHE infusion. At the end of each experiment, the animal was sacrificed, conformed to international norms (NIH Pub N 86-23, revised 1985). Data Collection The P and D signals were displayed in real time and digitally stored for later analysis. Under steady-state conditions, approximately consecutive beats during NPS, PHP and AHT conditions were sampled and analyzed. During all the acquisitions the ventilator was turned off. Viscoelastic Model. A Kelvin-Voigt Viscoelastic model was used to characterize the arterial wall mechanical properties. Accordingly, total P developed by the AO or PA wall to resist stretching can be separated into an elastic and a viscous P component [5,7,8] : As viscous P is proportional to the first derivative of the arterial D, the elastic P component can be obtained as: where η is the arterial wall viscous modulus. To separate the purely elastic wall properties, the viscous term must be subtracted from the total P, finding the optimal value through the hysteresis loop disappearance criteria [5,7,8]. The resulting elastic behavior in the P-D loop can be used to calculate the elastic modulus (E) as the slope of a linear regression fit to the diastolic phase. To analyze the temporal response of the arterial wall, as in a Kelvin-Voigt model, the following P-D equation, using (1) (2) and the calculated E, is proposed
3 where the η/e constant time would characterize the diameter temporal exponential response to a steep pressure increase, or in other terms the arterial wall buffering function (WBF): To evaluate the systemic and pulmoanry circuits global buffering function (GBF), a constant time (τ) indicator is proposed and beat to beat estimated using the temporal arterial P variation and the exponential decay time method described elsewhere [9]. The accuracy of the exponential fit was demonstrated in each condition by r 2, which was between and In all conditions, mean r was > Statistical Analysis. All measurements and calculated values are expressed as mean ± SD. The presence of significant differences was assessed using ANOVA for repeated measures followed by a Bonferroni τ test. A significance p threshold value of 0.05 was adopted. RESULTS In the table I the hemodynamic and mechanical parameters of AO and PA, during all experimental conditions are shown. Note that the mean P resulted similar in each artery during PHT and AHT, determining isobaric states. DISCUSSION The P-D relationship was obtained in the in-vivo preparation by means of a reliable ultrasonic dimension technique and a high fidelity solid state P gauge, widely used by our group in the systemic [5,8] and pulmonary [10] circulation. The E and η modulus were extracted from P-D loops using the hysteresis elimination criteria [5,8]. To determine the direct effects of VSM activation on the AO and PA WBF and GBF, a comparison of the viscoelastic behavior with and without VSM activation, at the same level of mean arterial P (isobaric study) was accomplished (Table I). The VSM of both circuits was activated with PHE, a sympathomimetic drug with a direct α1-receptor stimulant effect and minimal central action [10]. PA and ascending AO VSM activation was evidenced during PHE infusion, by the isobaric mean D reduction (Table I). Arterial wall's response to occlusion maneuvers, only reflects its intrinsic passive elastic properties because changes in P and D are extremely rapid [8,10]. Aortic E and η were higher than pulmonary (p<0.05) ones. Both arteries' E increased (p<0.05) (stiffening effect) with the P rise induced by PHT, but only in AO's E increased (p<0.05) during AHT. There was significant augmentation (p<0.05) of the AO and PA η during AHT. Generally it is assumed that the elastin and collagen determine the arterial wall elastic response, while the VSM is the main responsible for the viscous behavior [11]. Our data show, that while E depends on intravascular P and VSM activation, η only depends on VSM tone. AO has major net elastic and VSM amounts with respect to PA, and consequently it has higher viscoelastic levels. Since η remained almost stable between NPS and PHT, viscosity P- independence is suggested and the η increase during AHT might be associated with the VSM activation. A higher viscosity denotes a greater energy cost during vascular pulsate expansion in each cardiac cycle.
4 The η/e time constant is usually adopted to quantify the arterial wall's temporal diameter response to a steep P increase (elastomeric approach). A large η/e value, according with a slow response, suggests an enhanced WBF by means of a more pronounced attenuation of the P oscillations. Both arteries had similar WBF, while the systemic circuit presented a higher GBF (p<0.05). During PHT, in both arteries, the η/e ratio decreased with respect to NPS due to the E increase and the η stability, revealing a minor arterial WBF. On the contrary, for the same P level with PHE, the η/e ratio remained near the NPS level, suggesting that viscosity may play an important role in the arterial response stability. Now, focusing in the whole systemic and pulmonary circulation behavior and among the "lumped" parameters that can be simply estimated for each cardiac cycle, the time constant (τ) was chosen. The diastolic arterial P decrease, fitted to a monoexponential model, yields τ as a reliable and interesting indicator [12]. It can be considered as the product of the total vascular resistance and the overall compliance of the arterial tree, the so-called total arterial compliance [9]. The time constant τ reflects the mechanical behavior of the arterial tree, and indicates the restoration of energy stored by the arterial wall during the elastic distension due to ventricular ejection. The GBF state was higher (p<0.05) in the systemic circuit respect to the pulmonary one, and did not change during AHT but diminished during PHT, respect NPS and AHT. We postulate that, although the P variations play an important passive role in the arterial wall mechanical behavior as it determines the site in the non linear arterial P-D relation in which the PA or AO have their WBF operational or work point, the VSM tone can modulate the arterial mechanical properties, and consequently adapt the WBF in an active way (with expenditure of energy), to a particular haemodynamic condition. About this, the local (large arteries) and/or generalized (all the circuit) VSM activation could be beneficial to the cardiovascular system maintaining the WBF and/or the GBF, despite of an acute P increase. CONCLUSIONS We propose a local or WBF control due the VSM activation modulation. The AO viscoelasticity was higher PA one, but the η/e ratio was similar. The VSM activation determines the isobaric E decrease and η increase and remains the arterial WBF elevated, near NPS level, despite of the P increase. The enhanced systemic circuit's GBF (indicated by τ) could be due to its longer effective length respect to the pulmonary path, but not due to a higher local or WBF property, respect PA. The VSM activation in the PA and AO would help to preserve the WBF during systemic and/or pulmonary P elevation, increasing the beat to beat energy dissipation which contributes to maintain the whole systemic and pulmonary buffering function. REFERENCES 1. O'Rourke MF. Second workshop on structure and function of large arteries. Part I. Mechanical principles in arterial disease. Hypertension 1995; 26: Simon AC, O'Rourke MF, Levenson J. Arterial distensibility and its effect on wave reflection and cardiac loading in cardiovascular disease. Cor Artery Dis 1991; 2: Li John K-J. Arterial System Dynamics. New York University Press, Simon A, Levenson J. Effect of hypertension on viscoelasticity of large arteries in humans. CurHypertension Reports 2001;3: Armentano RL, Barra JG, Levenson J, Simon A, Pichel RH. Arterial wall mechanics in conscious dogs: assessment of viscous, inertial, and elastic moduli to characterize the aortic wall behavior. Circ Res 1995;76: Dobrin PB, Rovick AA. Influence of vascular smooth muscle on contractile mechanics and elasticity of arteries. Am J Physiol 1969;217: Armentano RL, Megnien JL, Simon A, Bellenfant F, Barra JG, Levenson J. Effects of hypertension on viscoelasticity of carotid and femoral arteries in humans. Hypertension 1995; 26: Barra JG, Armentano RL, Levenson J, Cabrera Fischer EI, Pichel RH, Simon A. Assessment of smooth muscle contribution to descending thoracic aortic elastic mechanics in conscious dogs. Circ Res 1993; 73: Simon AC, Safar ME, Levenson JA, London GM, Levy BI, Chau NP. An evaluation of large arteries compliance in man. Am J Physiol 1979; 237:H550-H Bia D, Grignola JC, Armentano RL, Ginés F. Improved pulmonary buffering function during phenylephrine-induced pulmonary hypertension. Mol Cell Biochem 2003; 246: Wells SM, Langille BL, Lee JM, Adamson SL. Determinants of mechanical properties in the developing ovine thoracic aorta. Am J Physiol 1999; 277 (4 Pt 2):H1385-H Molino P, Cerutti C, Julien C, Cuisinaud G, Gustin M-P Paultre C. Beat-to -beat estimation of windkessel model parameters in conscious rats. Am. J. Physiol 1998; 274:H171-H177. Your questions, contributions and commentaries will be answered by the authors in the Basic Research list. Please fill in the form and press the "Send" button.
5 Question, contribution or commentary: Name and Surname:: Country:: Argentina Send Erase Top Updating: 10/29/2003
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