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(Hypertension. 1995;26:363-368.)
© 1995 American Heart Association, Inc.
Articles |
Aortic Wall Properties in Normotensive and Hypertensive Rats of Various Ages In Vivo
From the Departments of Physiology (A.W. van G., R.S.R.), Pharmacology (D.S. van I.S., H.A.J.S.B., J.G.R. De M.), and Biophysics (A.P.G.H.), Cardiovascular Research Institute Maastricht (CARIM), University of Limburg, Maastricht, Netherlands.
Correspondence to Robert S. Reneman MD, PhD, Department of Physiology, Cardiovascular Research Institute Maastricht, University of Limburg, PO Box 616, 6200 MD Maastricht, Netherlands.
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Abstract |
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Abstract The distensibility of the arterial system, which is partly determined by arterial wall structure, smooth muscle tone, and actual pressure level, decreases with aging and hypertension. Our aim was to compare aortic wall properties in 3- and 6-month-old normotensive Wistar-Kyoto rats (WKY) and spontaneously hypertensive rats (SHR) at comparable blood pressures in vivo. During ketamine/xylazine anesthesia in rats we performed ultrasound arterial wall tracking and invasive pressure measurements to determine, at the level of the thoracic aorta, diastolic pressure, diastolic lumen area, changes in pressure and lumen area during the cardiac cycle, and indexes of compliance and distensibility. These observations were combined with histological measurements for determination of media cross-sectional area and thickness and the incremental elastic modulus under conditions as expected in situ. Anesthesia abolished the difference in diastolic pressure between SHR and WKY. Between 3 and 6 months of age in WKY, diastolic area and incremental elastic modulus increased significantly, distensibility decreased, and all other recorded variables were not modified. Between 3 and 6 months of age in SHR, diastolic area and incremental elastic modulus increased, distensibility of the aortic wall decreased, and all other mechanical and structural properties did not change significantly. At both ages, diastolic area and compliance were significantly smaller in SHR than WKY. The other mechanical and structural properties measured or calculated at comparable pressure did not differ between strains. Differences between the aorta of 3- and 6-month-old rats and between strains observed in vivo at comparable pressures can largely be attributed to differences in lumen caliber. These may represent the first findings concerning remodeling of the aorta in intact rats.
Key Words: arteries • aorta • rats, inbred WKY • rats, inbred SHR • age factors • compliance • remodeling
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Introduction |
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Arterial distensibility decreases with aging and hypertension.1 2 3 4 This increases aortic input impedance and decreases systemic arterial compliance and thus may adversely affect cardiac function in the long run by elevating cardiac afterload and reducing the energetic efficiency of the myocardium.2 5 6 7 Arterial distensibility is determined by the composition and organization of the arterial wall, the contractile tone of arterial smooth muscle cells, and the actual pressure level.8 The precise mechanism responsible for the alterations in distensibility with aging and hypertension is still largely unknown.
The aim of the present study was to determine the distensibility, compliance, and structure of the thoracic aorta in two age groups of normotensive and hypertensive rats at identical pressures in vivo. Distensibility and compliance were determined by ultrasound arterial wall tracking and invasive pressure measurements in 3- and 6-month-old Wistar-Kyoto rats (WKY) and spontaneously hypertensive rats (SHR) anesthetized with ketamine/xylazine. The structure was assessed by morphometry of cross sections.
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Methods |
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Study Design
Experiments were performed in 3- and 6-month-old male WKY and SHR of the Okamoto-Aoki strain9 (local inbred strains; Central Animal Facilities, University of Limburg, Maastricht, Netherlands); each group contained 12 rats. The rats were housed in individual cages, maintained on a 12-hour light/dark cycle, fed ad libitum (Hope Farms), and had free access to tap water. Experimental protocols were approved by the local Institutional Animal Care and Use Committee.
For measurement of arterial blood pressure the rats were equipped under ether anesthesia with an intra-aortic catheter filled with heparinized saline. The diameter of the intra-aortic catheter was 0.5 mm. The catheter was advanced from a femoral artery to just below the bifurcation of the left renal artery. The catheter was guided under the skin and exteriorized at the base of the skull. Two days later blood pressure was measured in the freely moving conscious rats through an external low volume displacement pressure transducer (CP-01, Century Technology Co). The time delay of the catheter and pressure transducer was 12 milliseconds and hence guaranteed a sample frequency greater than 50 Hz. The rats were subsequently anesthetized with ketamine/xylazine (10:50 µg/mL; 100 µL/100 g body wt), and blood pressure measurements were performed along with ultrasound wall tracking of the thoracic aorta. Experiments were terminated by exsanguination of the rats, after which the thoracic aorta was isolated for subsequent histological examination.
Ultrasound Assessment of Aortic Diameter and Wall
Movement
The diameter and change in diameter during the cardiac cycle
were assessed as a continuous function of time with the use of a vessel
wall tracking system (see below) attached to a conventional B-mode
ultrasound system (Pie480, 7.5-MHz linear array, Pie Medical). With
this ultrasonic technique we measured the internal diameter of the
aorta.10 The ultrasound probe was placed on the thorax
slightly to the left of the sternum. The thoracic aorta was then
visualized in B-mode (B, brightness), and an M-line was positioned
perpendicular to the vessel walls approximately 10 mm cranially from
the diaphragm. Thereafter the ultrasound system was switched to M-mode
(M, motion), and ultrasound was emitted and received along the selected
line of sight at a programmable emission trigger frequency.
The concept of the wall tracking system has been described in detail before.10 It is based on a data-acquisition system capable of capturing the received and amplified radio frequency (RF) signals synchronously with the emission trigger at a programmable sample frequency of up to 30 MHz and with a dynamic range of 48 dB (8 bits). The position and width of the range of interest are programmable (on average, 20 and 10 mm, respectively, in the present study). The size of the internal data memory is 1 megabyte, allowing for the temporary storage of, for example, 512 RF lines of 2000 data points each. At an emission frequency of 250 Hz the memory will then hold 2.5 seconds of data, corresponding to approximately 10 cardiac cycles (and three respiration cycles) under the present experimental conditions (Fig 1). The wall tracking system is also equipped with an acquisition system for reference signals such as blood pressure, which are sampled synchronously with the emission trigger, activating the capture of an RF line (Fig 2).
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After data acquisition is complete the data are transferred to a personal computer. The first line acquired is graphically presented and displayed, allowing manual identification of the anterior and posterior wall boundaries by placement of two markers representing the sample windows for data processing. Once the walls are identified the remaining data are transferred and processed on the fly (<10 seconds). To extract the change in position of either the anterior or posterior wall, averaged over a few RF lines, the approach based on the cross-correlation model for corresponding segments of subsequent RF lines was applied.11 This method has a low noise sensitivity and is insensitive to the RF carrier frequency. The estimates for the cross-correlation coefficients are based on a running average over a programmable number of RF lines (data window in time) to enhance the stability of the estimate for the mean displacement. To ensure that the signals were always returned by the same structure, we adjusted the position of the sample windows according to the observed displacements (tracking window). The difference between the displacement signal of the posterior and anterior walls yields the change in diameter as a function of time. From the observed distension waveform, in combination with the initial distance between the sample windows, the internal end-diastolic diameter, the peak-to-peak change in internal diameter, and the length of the cardiac cycle can be extracted for each cardiac cycle.
Measurements were started after blood pressure and heart rate had
stabilized with rats under anesthesia (20 minutes). In each
rat two observers performed three 2.5-second recordings. The
data obtained during these sessions were averaged. The ultrasound
system used is very accurate and can resolve displacements of only a
few micrometers.10 The reliability in
anesthetized rats is also good. The variabilities between four
consecutive measurements as performed on 1 day by one investigator
expressed as coefficients of variation varied between 3.2% and 6.5%
for the aortic diameter (Ddia) and between 7.9% and 11.0%
for the change in aortic diameter during the cardiac cycle (
D). The
variabilities between successive experimental days, also expressed as
coefficients of variance, were 4.6% for Ddia and 9.2% for
D. These values are comparable to the ones recently reported for
human carotid and femoral arteries.12
Relationship Between Lumen Diameter and Pressure
Since the wall tracking system and the intra-aortic catheter
display different time responses, we limited the analysis of
the relationship between aorta lumen caliber and intra-aortic pressure
to the situation at end diastole and to the maximal changes
in pressure and diameter that occurred during the cardiac cycle.
Diameters and diameter changes were converted to lumen areas and
changes (A and A), assuming a perfect circular cross section of the
vessel. With the additional assumption that the vessel segment length
remains constant, the absolute and relative changes in aortic lumen
area noted during the cardiac cycle and expressed per unit of pressure
provide information about the compliance and distensibility of the
vessel, respectively.10 11 12 Below A/P and
(A/A)/P will be referred to as the compliance coefficient and
distensibility coefficient, respectively.10 11 12
Aortic Wall Structure
A 10-mm supradiaphragmatic segment of the thoracic aorta was
isolated, fixed in 4% neutral buffered formaldehyde, and embedded in
paraffin, after which 4-µm-thick sections were obtained. These were
stained with Lawson's solution, which highlights elastic laminae, and
the cross-sectional area of the media was determined with an axioplan
microscope (Zeiss) equipped with a standard CCD camera
(Stemmer).13 14 Digitized images were analyzed
with commercial software (JAVA, Jandell Scientific). The
area enclosed by the external and internal elastic laminae was
considered to represent the ex vivo cross-sectional area of the
media (CSAe). This was converted to in vivo media
cross-sectional area (CSAi) by the formula
CSAi=(Le/Li) · CSAe,
in which it was assumed that aortic wall volume remains constant after
isolation and fixation and in which Li and Le
refer to the length of the thoracic aorta before and after isolation,
respectively. To this end, a segment of 10 mm (Li) halfway
between heart and diaphragm was marked on the aorta and subsequently
removed from the rat and cleaned of adhering fat and connective tissue,
after which the ex vivo length of the segment (Le) was
again measured under a stereomicroscope with a precision of ±5 µm.
Le/Li averaged 0.75±0.02 and 0.75±0.01
in 3- and 6-month-old WKY and 0.72±0.01 and 0.79±0.01 in 3- and
6-month-old SHR, respectively. Media thickness (Mt) in
diastole was calculated from the ultrasound measurement of
diastolic diameter (Ddia) and from
CSAi using the formula
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which can be rewritten as
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In these calculations it is assumed that the cross section of the aorta was circular in situ.
Measurements of mechanical properties and dimensions were combined to calculate the incremental elastic modulus or Young's modulus (Einc):
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where DC is the distensibility coefficient.
Statistics
Each age group of WKY and SHR consisted of 12 rats. In each rat
six consecutive 2.5-second recordings of pressure, internal
lumen diameter, and distension were obtained and derivatives calculated
for each individual cardiac cycle. Mean values were calculated for each
recording session, and these values then were averaged for each
individual rat; ultimately, a group mean was obtained for each
strain-age group.
Data are shown as mean±SEM. Comparisons between age groups were performed with the Wilcoxon-Mann-Whitney rank sum test.15 Comparisons between strains were performed with the unpaired Student's t test.15 A value of P<.05 was considered to denote statistical significance of differences.
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Results |
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Between 3 and 6 months of age, body weight and blood pressure increased in both WKY and SHR (Table 1). At both ages, body weight was significantly lower and blood pressure, determined in conscious, freely moving conditions, was significantly higher in SHR than WKY (Table 1).
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Anesthesia with ketamine/xylazine hardly affected diastolic pressure in 3- or 6-month-old WKY (Table 2). In SHR on the other hand anesthesia markedly lowered blood pressure. During anesthesia the original difference in diastolic pressure between SHR and WKY was abolished, as was the difference in pulse pressure at 3 months of age (Table 2). Pulse pressure remained significantly elevated in 6-month-old anesthetized SHR.
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Table 2 summarizes findings with respect to aortic wall properties in anesthetized 3- and 6-month-old WKY and SHR. In WKY between 3 and 6 months of age diastolic pressure, pulse pressure, and heart rate as well as media cross-sectional area, media thickness, and aortic compliance were not modified. However, aortic lumen area at diastole was increased, and distensibility of the aortic wall was reduced (Table 2). The increase in lumen area and decrease in distensibility resulted in a significant elevation of the elastic modulus. In SHR, comparable changes were observed between 3 and 6 months of age, except for pulse pressure, which rose significantly. Also in this strain aortic lumen area increased and distensibility decreased, and media mass and aortic compliance were not modified (Table 2).
Table 2 also illustrates differences between the aortic wall properties observed during anesthesia in WKY and SHR at both ages. At 3 months of age under conditions of comparable diastolic and pulse pressures, diastolic lumen area and compliance were significantly lower and the elastic modulus significantly smaller in the aorta of SHR than in that of WKY. These differences can be appreciated from the relationships between intra-aortic pressure and aortic lumen area shown in Fig 3. The slope of the line connecting observations during diastole and peak systole corresponds to the compliance coefficient. At 3 months of age media area did not differ between SHR and WKY. However, in view of the smaller lumen at comparable pressure, media thickness was significantly larger in SHR than WKY (Table 2). At 6 months of age differences between SHR and WKY with respect to aortic lumen area and aortic compliance persisted (Table 2, Fig 3). Differences in terms of media thickness and elastic modulus, however, were no longer significant at 6 months of age (Table 2).
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) and
spontaneously hypertensive rats (
). The slope of the lines
connecting minimal and maximal values refers to the compliance
coefficient discussed in the text and shown in Table 2 |
Discussion |
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We determined in vivo aortic wall properties by ultrasound techniques at comparable pressures in 3- and 6-month-old SHR and WKY. The main change with aging and hypertension consisted of an alteration of the lumen caliber of the vessel. Cross-sectional compliance was reduced in SHR compared with WKY.
Mechanical and structural properties of arteries and their interactions have been studied extensively with respect to the development and treatment of hypertension. In recent years primarily small resistance-sized arteries were addressed in this respect, in view of the elevated total peripheral vascular resistance that characterizes essential hypertension.16 17 At this level both wall hypertrophy and a reduction of lumen diameter (remodeling) may be involved.17 18 The situation is less clear in more proximal parts of the circulation such as the aorta. Reduction of the distensibility of this vessel can adversely affect cardiac function in the long run and thus promote the development of various cardiac disorders.1 2 3 4 5 6 7 In this respect hypertension may accelerate the changes that occur during normal aging.4 However, the exact nature of the changes in the aortic wall that lead to a reduction of aortic distensibility and compliance with aging and hypertension remains largely unknown. In general, the mechanical properties of a vessel such as the aorta are determined by its structure, the activity of its smooth muscle, and the actual pressure level.8 Studies of arterial wall mechanics in hypertension have been performed in both humans and animals with the use of in vivo and in vitro methods. Many of these studies addressed static rather than dynamic mechanical properties. In general, these studies have resulted in the conclusion that an increase in stiffness or elastic modulus of arteries exists in hypertension (for review see References 17 and 1917 19 ). Using an ultrasound system connected to a wall tracking system, Hayoz et al20 measured in vivo the cross-sectional compliance and distensibility of the carotid artery of SHR and found an increase in both. These results are contradictory to our findings. No clear-cut explanation can be given for this discrepancy. It is possible that the carotid artery behaves differently from the aorta (our study) under these circumstances.
In the present investigation we attempted to study aortic wall
properties in vivo in two age groups of normotensive and hypertensive
rats. We used ultrasound techniques to record internal minimal
(diastolic) lumen diameter and diameter changes during the
cardiac cycle. Combined with invasive blood pressure measurements this
allowed us to estimate wall distensibility and compliance. The
analysis was restricted to maximal changes in diameter and
pressure because aortic wall displacement and pressure were not
determined at identical locations. Consequently, we could not
dissociate between the contributions of elastic and viscous wall
properties to the observed aortic wall displacement. For obvious
reasons the measurements could not be obtained in freely moving,
conscious rats. We deliberately performed the experiments during
ketamine/xylazine anesthesia in an attempt to
compare findings under comparable hemodynamic
conditions. Xylazine is well known for its 
2-adrenergic
agonistic properties. The compound thereby (1) inhibits the activity of
the vasomotor center in the central nervous system,21 (2)
reduces peripheral adrenergic neurotransmission by a
prejunctional inhibitory action,22 and (3)
dilates the aorta through a local endothelium-dependent
mechanism.23 The low heart rates and unpublished
observations are in line with this scenario. After administration of
ketamine/xylazine, circulating catecholamine levels
were reduced by 80% to 90%, and unlike in conscious, restrained WKY,
prazosin and sodium nitroprusside failed to dilate the aorta in vivo
(J.G.R. De M., D.S. van I.S., P.M.H. Schiffers, unpublished
observations, 1995). That the blood pressure–lowering effect of
ketamine/xylazine was far more marked in SHR than WKY is
compatible with other evidence that indicates hyperactivity of the
sympathetic nervous system in SHR.24 25 26 27 The
anesthesia used abolished the difference in
diastolic pressure between both strains and reduced
interstrain differences in pulse pressure.
To analyze the contribution of structural wall properties to the mechanical properties observed by ultrasound wall tracking, we corrected histological findings with respect to media cross-sectional area for the changes that occurred during vessel isolation, and we took into account the in vivo measurements of diastolic lumen diameter to calculate media thickness. Thus, the experimental approaches used allowed us to compare aortic wall properties in two age groups of WKY and SHR under dynamic in vivo conditions at comparable levels of (diastolic) blood pressure and possibly during relaxation of the aortic smooth muscle.
Between 3 and 6 months of age, aortic lumen caliber at diastole increased in both WKY and SHR. This change may account for the significant reduction of the distensibility and for the significant increase of the elastic modulus with aging. Other variables, such as the area and thickness of the media, tended to increase, but these changes did not reach statistical significance. Compliance did not change either with increasing age in both SHR and WKY. The loss of distensibility is apparently compensated for so that increases in systolic pressure, an independent risk factor,28 29 are limited. The mechanism by which aortic caliber increased between 3 and 6 months of age cannot be deduced from our findings. However, it may be of interest that the rats gained more than 30% body weight and are known to exhibit a significant increase in cardiac output during this time interval.26 It has been reported that chronic increases in flow increase arterial lumen diameter.30 31
At both 3 and 6 months of age aortic lumen diameter at diastole was considerably smaller in SHR than WKY. This together with the unaltered distensibility may account for the significantly lower compliance of the aorta of SHR than that of WKY. At 3 months of age the smaller lumen caliber and increased wall thickness culminate in a significantly lower elastic modulus in SHR. Surprisingly, the encroachment of the aortic wall on the lumen in SHR was not due to increased media mass. This lack of aortic wall hypertrophy in SHR contrasts with several earlier reports (for review see References 27 and 3227 32 ). This may be due to our attempts to estimate aortic wall structure at the pressure, lumen diameter, and vessel segment length corresponding to the conditions during the recording of wall elasticity in vivo. The structural narrowing of the SHR aorta at comparable pressure is analogous to observations in resistance-sized arteries from SHR, renin-transgenic rats, and essential hypertensive patients.18 33 34 35 36 This suggests that what is now generally referred to as vascular remodeling in hypertension18 is not restricted to distal small arteries.
It is of interest to note that in SHR aorta, compared with WKY aorta, the incremental elastic modulus or Young's modulus was reduced (suggesting increased distensibility) despite the lower compliance and comparable distensibility measured. This was statistically significant at 3 months of age and showed an insignificant trend at 6 months of age. It has previously been reported that in the human radial artery the incremental elastic modulus is not increased with hypertension.37 However, the validity of Young's modulus to estimate elastic properties under these circumstances may be questioned. It treats the arterial wall as a homogeneous and mere elastic structure. We based its calculation on media thickness rather than wall thickness because of the poor delineation of the outer vessel wall boundary. However, the relative contributions of media and adventitia to vessel wall mechanics in situ are poorly understood. Furthermore, both layers are composed of diverse components including cells, collagen, elastin, and other extracellular matrix components. The relative importance of each of these and their interactions require further investigation.
In conclusion, in the present study we were able to evaluate mechanical and structural properties of the thoracic aorta in two age groups of normotensive and hypertensive rats under dynamic in vivo conditions and at comparable diastolic pressures. We observed an increase in lumen diameter between 3 and 6 months of age in both strains. Differences between SHR and WKY included at both ages a reduction of aortic lumen diameter. This is compatible with earlier findings in resistance-sized arteries that have been attributed to remodeling of the arterial wall. Future analysis of underlying mechanisms will require detailed analysis of arterial wall components.
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Acknowledgments |
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This work was supported by grants from the Netherlands Scientific Research Organization (NWO, 518-291 PGC) and from the Dutch Heart Foundation (NHS, 91.098).
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 P. Lacolley, P. Challande, S. Boumaza, G. Cohuet, S. Laurent, P. Boutouyrie, J.-A. Grimaud, D. Paulin, J.-M. D. Lamaziere, and Z. Li Mechanical properties and structure of carotid arteries in mice lacking desmin Cardiovasc Res, July 1, 2001; 51(1): 178 - 187. [Abstract] [Full Text] [PDF]
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S. Boumaza, S. M. Arribas, M. Osborne-Pellegrin, J. C. McGrath, S. Laurent, P. Lacolley, and P. Challande Fenestrations of the Carotid Internal Elastic Lamina and Structural Adaptation in Stroke-Prone Spontaneously Hypertensive Rats Hypertension, April 1, 2001; 37(4): 1101 - 1107. [Abstract] [Full Text] [PDF]
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 C. E. Magyar, Y. Zhang, N.-H. Holstein-Rathlou, and A. A. McDonough Proximal tubule Na transporter responses are the same during acute and chronic hypertension Am J Physiol Renal Physiol, August 1, 2000; 279(2): F358 - F369. [Abstract] [Full Text] [PDF]
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C. Bussy, P. Boutouyrie, P. Lacolley, P. Challande, and S. Laurent Intrinsic Stiffness of the Carotid Arterial Wall Material in Essential Hypertensives Hypertension, May 1, 2000; 35(5): 1049 - 1054. [Abstract] [Full Text] [PDF]
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G. Zalba, F. J. Beaumont, G. S. Jose, A. Fortuno, M. A. Fortuno, J. C. Etayo, and J. Diez Vascular NADH/NADPH Oxidase Is Involved in Enhanced Superoxide Production in Spontaneously Hypertensive Rats Hypertension, May 1, 2000; 35(5): 1055 - 1061. [Abstract] [Full Text] [PDF]
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G. Marano, M. Grigioni, S. Palazzesi, and A. U Ferrari Endothelin and mechanical properties of the carotid artery in Wistar-Kyoto and spontaneously hypertensive rats Cardiovasc Res, March 1, 1999; 41(3): 701 - 707. [Abstract] [Full Text] [PDF]
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O. Lichtenstein, M. E. Safar, E. Mathieu, P. Poitevin, and B. I. Levy Static and Dynamic Mechanical Properties of the Carotid Artery From Normotensive and Hypertensive Rats Hypertension, August 1, 1998; 32(2): 346 - 350. [Abstract] [Full Text] [PDF]
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 Y. Bezie, J.-M. D. Lamaziere, S. Laurent, P. Challande, R. S. Cunha, J. Bonnet, and P. Lacolley Fibronectin Expression and Aortic Wall Elastic Modulus in Spontaneously Hypertensive Rats Arterioscler. Thromb. Vasc. Biol., July 1, 1998; 18(7): 1027 - 1034. [Abstract] [Full Text] [PDF]
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M. Takemoto, K. Egashira, H. Tomita, M. Usui, H. Okamoto, A. Kitabatake, H. Shimokawa, K. Sueishi, and A. Takeshita Chronic Angiotensin-Converting Enzyme Inhibition and Angiotensin II Type 1 Receptor Blockade : Effects on Cardiovascular Remodeling in Rats Induced by the Long-term Blockade of Nitric Oxide Synthesis Hypertension, December 1, 1997; 30(6): 1621 - 1627. [Abstract] [Full Text]
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H. A.J. Struijker-Boudier, H. van Essen, G. Fazzi, J. G.R. De Mey, H. Y. Qiu, and B. I. Levy Disproportional Arterial Hypertrophy in Hypertensive mRen-2 Transgenic Rats Hypertension, November 1, 1996; 28(5): 779 - 784. [Abstract] [Full Text]
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