(Hypertension. 1995;25:272-277.)
© 1995 American Heart Association, Inc.
Articles |
Carotid Artery Mechanical Properties of Dahl Salt-Sensitive Rats
From the Department of Internal Medicine and INSERM (U337), Broussais Hospital, Paris, France.
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Abstract |
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Abstract We evaluated the mechanical properties of the carotid artery in anesthetized Dahl rats with or without long-term treatment with the diuretic compound indapamide. The mechanical properties of the carotid artery were evaluated by establishing pressure-volume curves in situ in vivo before and after total relaxation of arterial smooth muscle by potassium cyanide. Dahl salt-sensitive and salt-resistant rats were fed either a low (0.4%) or high (7%) NaCl diet for 5 weeks. In each group, half the rats received for the same period of time oral treatment with indapamide (3 mg/kg per day). Blood pressure, heart rate, and pressure-volume curves were studied at the end of the 5-week period. In untreated Dahl salt-sensitive rats, the pressure-volume curve of the carotid artery was shifted to the right compared with that in untreated Dahl salt-resistant rats. The finding was observed even after potassium cyanide and regardless of the NaCl diet (P<.01 between Dahl salt-sensitive and -resistant rats). Indapamide was able to prevent the development of hypertension in Dahl salt-sensitive rats receiving a high NaCl diet (185±7 versus 146±8 mm Hg in untreated and treated Dahl salt-sensitive rats with a high NaCl diet, P<.0005). In the other groups, indapamide had no effect on blood pressure. Indapamide treatment increased carotid arterial static compliance in Dahl salt-sensitive rats with a high or low NaCl diet and to a lesser extent in Dahl salt-resistant rats. The increase was observed even after total relaxation of carotid arterial smooth muscle by potassium cyanide. These results suggest that (1) the mechanical properties of the carotid arteries were altered in Dahl salt-sensitive rats independently of NaCl diet and transmural pressure changes, and (2) the diuretic compound indapamide prevented the disturbed mechanical properties of the carotid artery in Dahl salt-sensitive rats with a high or low NaCl diet, acting on both arterial structure and function. Sodium sensitivity (and not sodium intake) influences the changes in the carotid artery mechanical properties of Dahl rats.
Key Words: compliance • sodium • indapamide • hypertension, sodium-dependent • carotid artery
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Introduction |
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Alterations in the mechanical properties of the large arteries are a common phenomenon in hypertension.1 These alterations reduce the buffering function of the elastic arteries and play a part in increasing left ventricular afterload.2 However, increased arterial stiffness in hypertension is not uniformly observed. In human hypertension, the compliance of the radial artery has been found to be normal or even increased.3 In animal models, a decrease in the viscoelastic properties of the arteries is observed in Goldblatt hypertension and in spontaneously hypertensive rats.4 5 However, in deoxycorticosterone (DOCA)–salt hypertension,6 arterial compliance is increased at an early stage, pointing to complex relations between sodium and arterial mechanics in hypertensive animals.
The literature has shown subtle links relating the sodium ion to the mechanical properties of hypertensive arteries. In both essential and renal human hypertension, increased sodium intake is associated with increased aortic rigidity independent of blood pressure (BP) changes.7 8 In essential hypertension, reduced sodium intake is associated with a dilation of muscular but not of elastic arteries.9 In animal hypertension, Levy et al10 11 showed that the diuretic compounds cicletanine and indapamide increased carotid arterial compliance independently of BP changes, a finding that has not been commonly noticed in humans.12 Finally, there is limited data on the mechanical properties of the carotid artery in the most common variety of salt-sensitive hypertension in animals, ie, in Dahl rats. Furthermore, in this particular strain, the changes in arterial mechanics produced by diuretic compounds have not been evaluated. This is a surprising condition because the Dahl salt-sensitive (DS) rat is known to develop hypertension when fed a high salt diet,13 14 and this hypertension is prevented by diuretic substances.15 16 Furthermore, it has been shown that these rats frequently develop arterial and arteriolar lesions.15 17 18
The purpose of the present study was to evaluate the mechanical properties of the carotid artery in DS and Dahl salt-resistant (DR) rats with or without salt-dependent hypertension. In this respect, we investigated carotid arterial mechanics under two different conditions: (1) in untreated Dahl rats receiving a low or high salt diet, and (2) in Dahl rats treated by the diuretic compound indapamide19 in order to prevent the development of hypertension in the DS strain.
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Methods |
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Sixty-two male DS and DR rats were used in these experiments (Mollergaard Breeding Center, Skensved, Denmark). The rats were delivered to our animal house at 7 weeks of age. They were divided into eight groups according to the strain (DS and DR), sodium diet (low [L], 0.4% and high [H], 7% NaCl), and treatment. The different diets were given for 5 weeks. Treatment with indapamide (3 mg/kg per day) was administered by gavage, starting on the first day of the different NaCl diets and for the entire 5 weeks. Both diets contained the same amount of potassium (0.73%). Tap water was provided ad libitum throughout the study. During this period, all rats were housed at a constant temperature (24±1°C) (±1 SEM) and humidity, with a 12-hour light/dark cycle. The protocol was approved by the ethics committee of Institut National de la Santé et de la Recherche Médicale (INSERM, Paris, France).
On the day of the experiment, rats were anesthetized with pentobarbital (60 mg/kg IP), intubated, and ventilated.4 20 21 The right femoral and left carotid arteries were cannulated for direct arterial pressure recording and arterial compliance measurements. BP and heart rate were continuously recorded with a Statham P23XL pressure transducer, Gould Brush pressure computer, and Gould Brush 2400 recorder. For the evaluation of arterial mechanical properties, the left carotid artery was cannulated with an 80-cm-long nylon tube (diameter, 0.6 mm) filled with an Evans blue isosmotic solution (Tyrode-albumin) (Fig 1).4 21 The cannula was connected to a manometer pressurized at adjustable pressure values. A three-way tap was connected between the manometer and the nylon tube, enabling a part of the tube to be filled so that the position of the meniscus could be observed. After the chest was opened, the root of the left carotid artery was dissected and a clamp positioned at the junction with the aorta. This preparation allowed us to isolate in situ a 14- to 20-mm segment of carotid for study.
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To start the measurements, the isolated arterial segment was submitted to atmospheric pressure for 5 minutes, and the position of the meniscus was noted. The artery was then submitted to a pressure step of 25 mm Hg. The movement of the meniscus, representing changes in the contained volume within the artery, was followed and noted every 10 seconds for 5 minutes. During the first 30 to 45 seconds, the inflow was rapid and then became linear with time. The initial transient increase in volume with pressure was assumed to result from viscoelastic behavior of the tissue and relaxation of vascular smooth muscle. The subsequent linear inflow within the carotid artery after this initial increase in arterial volume could be attributed to fluid filtration through the vascular wall. An estimate of the initial increase in volume that was not due to viscoelastic effects was obtained by extrapolating the linear portion of the inflow curve to the time when the pressure step was applied. These measurements were repeated for pressures ranging from 25 to 175 mm Hg (up to 225 mm Hg in the untreated DSH group) in steps of 50 mm Hg. The static compliance of the isolated segment of carotid artery (CC) was calculated for each pressure level as the quotient of the extrapolated volume increase (expressed per unit carotid artery length) and the pressure step imposed (50 mm Hg). From these measurements, the curve relating the change in carotid arterial volume to transmural pressure was calculated. Then the same measurements were performed after total relaxation of arterial smooth muscle by local application of potassium cyanide (KCN), as previously described.20 21 We previously checked that the CC values did not differ when measured for increasing pressure steps (from 25 to 175 mm Hg) or for decreasing pressures (from 175 to 25 mm Hg).4 5 In addition, we performed two series of CC measurements separated by a 1-hour interval, which showed that CC values measured for the same transmural pressures were not affected by a 1-hour delay. Reproducibility was within 95%. Pressure was maintained at each level for 5 minutes. In the present experiments, we used steps of 50 mm Hg instead of 25 mm Hg for the study of the CC–transmural pressure relation. We checked that the results of the two different procedures gave quite similar results, thus enabling us to shorten the duration of the experiments. In addition, the results could be easily summarized using, for the presentation of results, four different transmural pressure ranges: 25 to 75, 75 to 125, 125 to 175, and 175 to 225 mm Hg.5 Because of the fragility of the rats, the latter pressure range was performed only in the untreated DSH group. Because of the curvilinearity of the arterial volume-pressure relation, it has long been recognized that in the lower pressure ranges (below 125 mm Hg), the tension is borne predominantly by elastin and smooth muscle, whereas in the higher pressure ranges (above 125 mm Hg), the tension is borne mainly by collagen matrix.2
Compliance values were studied for all pressure steps. A specific analysis was then performed for operating pressure, ie, variation of carotid artery volume for imposed pressure steps within the range of the systemic systolic and diastolic BP values of the corresponding animals (125 to 175 mm Hg in all groups except untreated DSH rats, in which the operating pressures were between 175 and 225 mm Hg).
All results are expressed as mean±1 SEM. A two-way ANOVA was used to evaluate the role of strain and diet on the arterial parameters in the different groups. The effects of indapamide were tested with a two-way ANOVA (group-treatment). These tests were performed for each pressure step of the volume-pressure relation. A paired Student's t test was performed to compare compliance values before and after KCN. For statistics, a value of P<.05 was considered significant.
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Results |
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Table 1 shows the values of mean BP, heart rate, and body weight in the different groups of Dahl rats on the day of the experiment. In the untreated groups, mean BP was significantly higher in the DSH rats compared with the other three groups. In the indapamide-treated rats, such differences were not observed, indicating that indapamide treatment prevented the development of salt-dependent hypertension in the DS rats. Indapamide treatment reduced heart rate in the DRH rats (P<.05); in the other groups, treatment did not modify HR (Table 1).
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Tables 2 and 3 summarize compliance values (m3 · 10-9/mm Hg per meter carotid artery) for the different pressure steps in the eight rat groups. In all four DR groups, maximal compliance values were observed at pressures between 75 and 125 mm Hg. In the two untreated DS groups, compliance increased from 25 to 125 mm Hg and then remained unchanged between 125 and 175 mm Hg. For higher levels, 175 to 225 mm Hg, compliance values decreased significantly. In the two treated DS groups, maximal compliance values were reached at 175 mm Hg because treatment preferentially increased compliance values at the pressure levels of 125 to 175 mm Hg (Tables 2 and 3).
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Table 2 shows that in untreated rats, compliance was lower in DS compared with DR rats for pressure levels up to 125 mm Hg. For higher pressure levels, DS and DR rats showed similar compliance values. Thus, the curve relating the change in carotid arterial volume versus transmural pressure was shifted to the right in DS rats, indicating a stiffer wall in this strain (P<.01) (Fig 2, top). Salt diet had no effect on the pressure-volume curve in DR and DS rats. Table 2 indicates that after acute local intracarotid injection of KCN, compliance increased in all groups for pressure steps up to 125 mm Hg. For higher pressure steps, KCN had no effect.
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Table 3 shows that in indapamide-treated rats, compliance was lower in DS compared with DR rats but only for pressure levels up to 125 mm Hg. A significant shift to the right of the DS pressure-volume curve resulted, indicating a stiffer wall in this strain, whatever the salt diet (Fig 2, bottom). KCN administration induced effects similar to those in the untreated groups. A two-way ANOVA showed a significant interaction (P<.05) between indapamide treatment and rat strain on arterial compliance at pressure levels of 125 to 175 mm Hg, ie, indapamide increased compliance preferentially in DS rats compared with DR rats. For lower pressure levels, compliance was similar in treated and untreated animals.
Fig 3 summarizes the values of operating carotid compliance in untreated and treated rats. In untreated animals, DSH rats had a lower operating compliance compared with DSL rats because of the higher level of systemic BP (see Table 2). Indapamide-treated rats showed significantly higher values of operating compliance compared with untreated rats.
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Discussion |
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In the present study, we evaluated the mechanical properties of the carotid artery in DS rats with or without salt loading using a method that was able to measure the arterial compliance in situ for a large range of imposed transmural pressure levels, with respect to the anatomy, vascularization, and innervation of the carotid artery. This method has already been validated.4 5 10 11 20 21 Using this model, we observed that the pressure-volume curve in untreated DS rats compared with that in DR rats was shifted to the right, reflecting increased arterial stiffness in the DS strain. The compliance values of DS rats were very close to those observed in previous studies in spontaneously hypertensive rats and significantly lower than the values recorded in normotensive Wistar-Kyoto rats.13 20 21
The shift of the carotid pressure-volume relation in DS rats exhibited three dominant characteristics. First, the alteration was not related to salt diet, because DS rats on either a low or high NaCl diet had identical pressure-volume curves. Second, the level of compliance was dependent on pressure. More specifically, operating compliance was lower in DSH than in DSL rats (Table 2) exclusively because of the fact that the pressure-volume curve is sigmoidal2 and that the very high pressure levels (observed in DSH rats) are on the shallower terminal part of the curve. Third, it appears that in terms of the contribution of sodium intake and pressure dependency of the carotid mechanics, the present findings agree with those reported by Cox6 in DOCA hypertensive rats. This author showed that in the particular model of salt- and volume-dependent hypertension, the magnitude of the arterial pressure increase and not the level of sodium intake determined the status of the carotid arterial wall behavior. The same pattern was observed in Dahl rats. Thus, the principal difference between the results of Cox and those of the present findings results from the genetic predisposition observed in DS and DR rats. Another interesting particularity of Dahl rats appears in the present study: The genetic predisposition to sodium sensitivity did not affect to the same extent the resistant arterioles and the large conduit carotid artery. Indeed, DS rats receiving a low salt diet have altered compliance despite BP levels similar to those in DR rats, ie, the same degree of arteriolar dilation.
Recently, similar findings were observed in sodium-sensitive borderline hypertensive subjects.8 Compliance of the carotid, brachial, and femoral territories was reduced in salt-sensitive subjects compared with salt-resistant borderline hypertensive subjects for the same level of mean arterial pressure and vascular resistance.
In our study, the genetic predisposition associated with the disturbed carotid pressure-volume curve of DS rats is difficult to elucidate for several reasons. First, it is well known that for the arterial smooth muscle of hypertensive rats, there is a genetic facilitation to vascular tissue adaptation, a process that has been recognized previously in the resistant arteries of DS rats.22 Second, the genetic background may contribute to the arterial changes either through intrinsic facilitation of cellular growth or by way of genetically reinforced neurogenic or hormonal influences. In the present investigation, the observed changes in the pressure-volume curve after KCN strongly suggested that both structural and functional components are involved in the carotid abnormalities. From the literature, two possibilities can be hypothesized. First, the connective tissue surrounding vascular smooth muscle cells may participate in the changes in arterial stiffness, particularly because extracellular matrix has as high a capacity for binding cations as sodium23 because of the presence of highly sulfated glycosaminoglycan chains.24 Second, the arteries of DS rats, particularly the aorta, are highly sensitive to vanadate, a potent inhibitor of Na+,K+-ATPase.25 Finally, Na+-K+ pump activities in these arteries have been found to be increased.25 26
Since the genetic characteristics of DS rats may influence the adaptive properties of the vascular tissue, the study of the changes of the carotid pressure-volume relation after prevention of hypertension is important. Previous studies15 16 repeatedly showed that treatment of Dahl rats with various diuretic agents was able to prevent the development of salt-sensitive hypertension. Accordingly, in the present study, indapamide treatment completely prevented the development of salt-dependent hypertension in Dahl rats. However, studies in the literature16 27 also have indicated that each diuretic compound may have specific effects on arterial smooth muscle. For instance, Limas et al28 and Uehara et al29 showed that cicletanine and indapamide were able to release vasorelaxant prostaglandins in DS rats, whereas treatment with thiazides had no effect on these vasodilating substances. In the present study, indapamide not only completely prevented the development of salt-dependent hypertension in Dahl rats but also changed the mechanical properties of the carotid artery.
An increase in operating compliance was observed even in the rat groups in which no significant change in BP was observed (DSL, DRL, and DRH) (Fig 3). For the DSH group, the increase in operating compliance was due to two factors: a reduction in BP toward lower pressure ranges in which tension is borne predominantly by elastin and smooth muscle, and a shift of the pressure-volume curve to the left. Using the same experimental procedure, Levy et al10 showed that local intracarotid applications of indapamide improved arterial mechanical properties in DOCA-salt hypertension independently of transmural pressure changes. In addition to these findings, in the Dahl rats of the present study, long-term treatment with indapamide was able to improve the elastic properties of the carotid artery wall even in animals without salt loading. This finding supports the hypothesis that indapamide acted on the arterial wall independently of its natriuretic effect.13 19 30 Schini et al31 reported that indapamide was able to increase the release of vasodilators in isolated arterial segments and to alter endothelial function.
In the present investigation, the effects of indapamide on carotid compliance should be compared with those produced acutely by local application of KCN. Total smooth muscle relaxation after KCN increased compliance in all groups for pressure steps up to 125 mm Hg. At higher pressure levels, compliance did not change because arterial tension is known to bear on collagen matrix in the presence of a completely elongated vascular smooth muscle.2 20 After indapamide treatment, arterial compliance increased at pressure ranges higher than 125 mm Hg. This observation suggests that the drug acted on the structural parameters of the arterial wall and especially on the collagen matrix. Two arguments are in favor of this interpretation: the high capacity of collagen for binding sodium23 within the arterial wall, and the change in the fibronectin expression of arterial smooth muscle that was observed after indapamide or hydrochlorothiazide administration in stroke-prone hypertensive rats.30 Finally, it is possible that the genetic predisposition of Dahl rats also may be responsible for carotid artery changes. Indeed, after indapamide, the compliance changes were more pronounced in DS than in DR rats.
At this point, it is important to consider several limitations for the interpretation of this data. First, the model requires anesthesia, which may be partly responsible for some hemodynamic changes, such as the slight decrease in heart rate observed in DRH treated animals. Second, although the model used allowed us to evaluate the mechanical properties of the carotid artery in vivo in situ, flow was nevertheless interrupted, and it is possible that this procedure may partly modify endothelial function, which is altered in DS rats.32 Finally, Dahl rats are a complex genetic model, in which not only the vascular system but also the kidney, endocrine glands, and nervous system are involved.27 32 33 Despite such limitations, it appears clear that the carotid artery wall mechanics of DS rats involve both pressure dependency and genetic predisposition. In addition, they are undoubtedly independent of the level of sodium in the diet. Finally, the disturbed mechanical properties of the carotid artery are prevented by the diuretic compound indapamide in a manner that cannot be explained exclusively on the basis of the drug-induced natriuretic and/or antihypertensive effect.
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Acknowledgments |
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This study was performed with a grant from the Institut National de la Santé et de la Recherche Médicale (INSERM U337), the Association Claude Bernard, the Ministère de la Recherche, and the Ministère de la Santé, Paris, France. We thank Annette Seban for her excellent assistance.
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Footnotes |
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Reprint requests to A. Benetos, MD, Service de Médecine Interne 1, Hôpital Broussais, 96, rue Didot, 75014 Paris, France.
Received May 5, 1994; first decision June 28, 1994; accepted October 3, 1994.
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