(Hypertension. 1998;32:180-185.)
© 1998 American Heart Association, Inc.
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Third Workshop on Structure and Function of Large
Arteries: Part I |
Differences in the Mechanical Properties of the Rat Carotid Artery In Vivo, In Situ, and In Vitro
Anne Zanchi;
Nikos Stergiopulos;
Hans R. Brunner;
; Daniel Hayoz
From the Division of Hypertension and Vascular Medicine, University
Hospital, and Medical Engineering, EPFL (N.S.), Lausanne, Switzerland.
Correspondence to Daniel Hayoz, Division of Hypertension and Vascular Medicine, CHUV, 1011 Lausanne, Switzerland. E-mail daniel.hayoz{at}chuv.hospvd.ch
Abstract
Abstract—The elastic properties of
carotid arteries of spontaneously hypertensive rats (SHR) and
normotensive controls (Wistar-Kyoto rats [WKY]) were examined in
vivo, in situ, and in vitro. The changes of internal diameter were
measured with a high-resolution A-mode echo-tracking device
simultaneously with the intra-arterial pressure
at the carotid. The internal diameter at mean arterial
blood pressure (MBP) was substantially smaller in vitro than in vivo in
SHR (-33.8%) and WKY (-48.3%). The arterial
distensibility was lower in vitro in all arteries compared with in vivo
conditions (SHR, -30.1%; WKY, -60.4%; at MBP) despite a reduced
incremental elastic modulus in vitro (SHR, -56.9%; WKY, -45.1%; at
MBP). However, the in vitro and in vivo measurements show
consistent elastic behavior of the carotid arteries between
both strains of rats. Carotid arteries from WKY were also examined in
situ. Although no significant reduction in internal diameter could be
observed in situ, distensibility was dramatically decreased (-87% at
MBP). These results emphasize the importance of considering the
original vascular geometry when determining elastic properties of
arteries. We conclude that experimental conditions are likely to be a
critical determinant for the assessment of the mechanical properties of
conduit vessels.
Key Words: arterial distensibility • elasticity • carotid arteries
Resistance arteries
have the capacity to adapt to increased wall stress by reorganization
of the components of the media (remodeling) and/or by thickening of the
media (hypertrophy).1 2 3 In contrast
to resistance arteries, conductance arteries hardly contribute to
peripheral resistance, but their buffering capacity
contributes to the pulsatile component of blood pressure, and they are
a major determinant of cardiac afterload. The adaptation of large
arteries to hypertension is associated with hypertrophy of
the media. Recent studies have been carried out to examine whether the
hypertrophic process may alter the mechanical properties of the
arterial wall.4 5 6 7 8 9 There has been
evidence that arteries demonstrate increased passive
stiffness10 and decreased
compliance11 during hypertension. However, the
development of new methods for in vivo assessment of the mechanical
properties of the arterial wall led to controversial
findings. In humans, the majority of in vivo assessments of
arterial compliance was derived from pulse-wave velocity
measurements and demonstrated a reduced compliance in hypertensive
subjects.12 In contrast, direct measurements of
the diameter-pressure relationship of the radial artery in hypertensive
subjects did not show a reduction of distensibility in hypertensive
subjects.4 5 13 Some of these discrepancies may
be related to the heterogeneity of the
arterial tree. The elastic properties of carotid arteries
measured in hypertensive rats, however, were not significantly
modified6 7 when compared with those of control
animals. These results differed from those obtained either by in situ
measurements in anesthetized
animals8 14 15 or by in vitro
experiments.11
The objective of this study was to assess the influence of the
experimental conditions (in vivo, in situ, in vitro) on the mechanical
properties of the common carotid artery in the rat and to examine in
which way the differences in mechanical properties observed so far
between normotensive and hypertensive animals could be affected by the
experimental conditions in which the measurements are performed.
Methods
In Vivo Versus In Vitro Conditions
Twenty-four-week-old male SHR (n=6) and normotensive WKY (n=6)
control rats were obtained from Iffa-Credo (Lyon, France). The animals
were housed in a conditioned environment, with constant temperature and
humidity and regular light/dark cycles (ie, light from 7 AM
to 7 PM). Ordinary rat chow (UAR, AO4,
Ville- moisson-sur-Orge, France) containing 100 µmol sodium
per gram and drinking fluid were provided ad libitum. The procedures
used in this study were approved by the governmental ethics committee
for animal experiments.
On the day of the experiment, anesthesia was induced and
maintained with halothane (Arovet AG) at a concentration of 1.5%. The
right common carotid artery was cannulated with a catheter (PE-50,
Portex) filled with heparinized 0.9% saline solution.
Intra-arterial pressure and heart rate were monitored as
described previously with a computerized data acquisition
system.16 The frequency response of the
transducer (Micro Switch, Honeywell) is >1 KHz, and the transducer
system is automatically zeroed with respect to atmospheric pressure.
The ID of the left common carotid artery was measured
simultaneously with an A-mode ultrasonic echo-tracking
device (NIUS 02, Asulab). This device, which has a dynamic precision
close to 1 µm, has been used previously in both animal
experiments and human studies.4 17 18 Briefly,
the ultrasonic echoes generated by a 17-MHz probe placed
perpendicularly over the artery without direct contact with the skin
are reflected by the interfaces between blood and both anterior and
posterior walls (RF echo line). They are sampled at 100 MHz and stored
at 500-Hz pulse repetition frequency (PRF). The vascular interfaces are
subsequently selected by the operator on the RF echo line and
automatically tracked to obtain the diameter and its variation over
time. The exact position of each selected interface is obtained by
calculation of the real-time position of the maximum of the
corresponding peak in the RF line, thus increasing the initial
resolution given by the 100-MHz sampling frequency (corresponding to a
spatial depth of 7.5 µm) to approximately 1 µm.
Doppler mode was used to guide the probe, and ultrasonic gel was
used for signal transmission. The built-in postprocessing allows
immediate calculation of the diameter-pressure relationship from the
simultaneous arterial diameter and blood
pressure measurements stored at 50 Hz. This diameter-pressure
relationship is subsequently converted into cross-sectional compliance-
and distensibility-pressure curves. These curves are fitted best with
an arctangent function.19 Cross-sectional
compliance (C) is expressed by C=dS/dP, where C is the slope of the
CSA-pressure curve, and S is the lumen cross section.
Arterial distensibility (D) is the compliance value
normalized by the cross section (S). It is expressed as
D=(1/S)xdS/dP.
Once the measurements were completed, the animal was killed with a
lethal dose of pentobarbital (90 mg/kg IA). The heart was dissected,
squeezed, and weighed. A segment of the left common carotid artery was
precisely measured in situ and after excision. The artery was then
immersed in an oxygenated (95%
O2-5% CO2), warmed
(37°C) isotonic solution of the following composition (mmol/L): NaCl
119, KCl 4.7, KH2PO4 1.17,
NaHCO3 25, MgSO4 1.17,
CaCl2 2.5, glucose 5.5. Both ends of the artery
were mounted on needles (0.5-mm diameter) and stretched to the initial
in situ length. One needle was connected to a piezo-element for the
determination of intraluminal pressure while the other was connected to
a catheter filled with the isotonic solution bath. Pressure was
manually altered to obtain a pulsatile variation in intraluminal
pressure corresponding to the systolo-diastolic blood
pressure measured in vivo and with a frequency close to 0.2 Hz. A
diameter-pressure relation was calculated from the
simultaneous arterial diameter and blood
pressure recordings and was subsequently converted into
cross-sectional compliance- and distensibility-pressure curves as
described above. The rate-dependent changes of the mechanical
properties of the carotid arteries were assessed by submitting isolated
carotid arteries to a peristaltic pump–generated pulsatile flow whose
frequency was adjusted from 1 to 4 Hz at a mean blood pressure of
100 mm Hg.
Carotid arteries were then fixed at the mean blood pressure found in
vivo during 30 minutes with a 4% paraformaldehyde
solution. Paraffin-embedded tissue blocks were sectioned at a thickness
of 5 µm and stained with hematoxylin and eosin.
Histomorphometric measurements were performed under a microscope
(Diaphot, Nikon). The IMT and ID measurements were performed with
200-fold magnification in a blinded fashion. The measurements carried
out on 2 carotid sections and on 6 fields per section were averaged.
The intima-media CSA of the fixed arteries was determined according to
the following formula: CSA=
[(internal
radius+IMT)2-(internal
radius)2].
To have an estimation of the incremental modulus of elasticity in vivo
and in vitro, the arterial wall thickness was derived for
each level of blood pressure from the CSA measured in vitro and the ID
(d) measured in vivo and in vitro. This was done assuming that the CSA
remains constant in vivo and in vitro and is not influenced by the
changes in diameter.17 20 The in vitro
experiments on the excised arteries were carried out at in situ length.
Thus, the length between 2 arbitrarily chosen anatomic markers was set
to the same level as before excision and kept for the entire inflation
experiment protocols. Therefore, despite large changes in pressure, the
length of the segment as well as the longitudinal stretch ratio were
kept constant. This means that the local wall CSA, by virtue of the
incompressibility condition, remained constant. The wall thickness (h)
was calculated according to the following formula: h= 214
[(CSA+ (d/2)2)/]-d/2. The
circumferential stress (
) for each level of blood pressure (p) and
ID (d) was derived from the following formula: =pd/2h. Finally, the
incremental modulus of elasticity was defined as
Einc=
/strain=[(n+1)-n]/[d(n+1)-dn]
and was calculated for each increase in intra-arterial
blood pressure of 2.5 mm Hg within the operational blood pressure
range.
In Vivo Versus In Situ Conditions
Twenty-four-week-old male normotensive WKY controls were housed
in a conditioned environment as described above. On the day of the
experiment, anesthesia was induced and maintained with
halothane (Arovet AG) at a concentration of 1.5%. The right internal
carotid artery was cannulated with a catheter (PE-50, Portex) filled
with heparinized 0.9% saline solution. A loose knot was carefully
placed around the proximal common carotid artery.
Intra-arterial pressure and heart rate were monitored as
described previously. The ID of the right common carotid artery was
measured simultaneously with a 10-MHz A-mode ultrasonic
echo-tracking device (NIUS 02, Asulab). For the recordings, the
probe was placed perpendicularly over the artery at 8 mm away from
the knot. Doppler mode was used to guide the probe, and warmed
ultrasonic gel was used for signal transmission. The
simultaneous arterial diameter and blood
pressure measurements allowed calculation of a diameter-pressure
relation, which was subsequently converted into cross-sectional
compliance- and distensibility-pressure curves. After the measurements
performed in vivo, the knot was tightened and the catheter was filled
with an oxygenated (95% O2-5%
CO2), warmed (37°C) physiological
salt solution identical in composition to that used in vitro and
described above. The intraluminal pressure was again manually altered
similarly to the experiment performed in vitro over the
systolo-diastolic pressure range measured in vivo after 10
to 15 minutes of preconditioning. After completion of the measurements,
the rat was killed with a lethal dose of pentobarbital (90 mg/kg IA);
immediately afterward, the intraluminal pressure was again modified as
described above. The positions of the electronic trackers on the RF
lines yielding both proximal and far-wall signals were not altered
during all these procedures.
Statistics
Between-group comparisons of body weight; heart weight index;
CSA; IMT; ID at histology; and mean, diastolic, and
systolic blood pressures were made by Scheffé's test.
The diameter, distensibility, and Einc curves
were established within operating pressures, the upper and lower limits
representing the mean systolic and mean
diastolic values for each group, respectively. For the
statistical evaluation of the diameter-, distensibility-, and
Einc-pressure curves, the areas under the curves
for operating blood pressures were compared using Scheffé's
test. Results are given as mean±SEM.
Results
In Vivo Versus In Vitro
Table 1
summarizes the
characteristics of the study groups at the age of 24 weeks. The SHR
were slightly heavier than the control WKY. Systolic,
diastolic, and mean blood pressures were significantly
higher in the SHR than in the control WKY. Pulse pressure was not
different among the 2 groups. The presence of cardiac
hypertrophy in the SHR was demonstrated by a higher heart
weight index [heart weight (mg)/body weight (g)] when compared with
controls.
Figure 1 illustrates the
diameter-pressure curves for the 2 groups obtained in vivo and in vitro
over the systolo-diastolic range of pressure. As
demonstrated, the ID was significantly smaller in vitro than in vivo in
all groups, and this was more pronounced in the WKY
(P<0.001). The distensibility-pressure curves differed
substantially and in a similar fashion in vivo and in vitro in the 2
groups (Figure 2). The distensibility
observed in vitro was dramatically reduced when compared with in vivo
conditions.
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Figure 1. Line plots show the relation between
intra-arterial pressure and diameter of the common carotid
artery in vivo and in vitro in WKY and SHR. In vivo vs in vitro: WKY,
P<0.001; SHR, P<0.001. Lines
represent means; shadows, SEM.
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Figure 2. Line plots show the relation between
intra-arterial pressure and distensibility of the common
carotid artery in WKY and SHR. In vivo vs in vitro: WKY,
P<0.001; SHR, P<0.01. Lines
represent means; shadows, SEM.
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The calculated Einc was markedly lower in vitro
than in vivo in the SHR (P<0.005) and WKY
(P<0.05) (Figure 3).
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Figure 3. Line plots show the relation between
intra-arterial pressure and Einc of the common
carotid artery in WKY and SHR. In vivo vs in vitro: WKY,
P<0.05; SHR, P<0.005. Lines
represent means; shadows, SEM.
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The morphometric characteristics were measured first with the
ultrasonic device in vitro to assess thickness and diameter of the
artery and subsequently by histology after perfusion fixation with
paraformaldehyde (Table 2). The CSA of the carotid artery was
significantly increased in the SHR compared with the WKY controls when
estimated in vitro and by histology. There was a strong positive
correlation between the values of CSA obtained in vitro and by
histology, demonstrating that histological processing
induced proportionally the same changes in all arteries
(r=0.92, P<0.001).
The rate-dependent changes in vascular mechanics in vitro is shown in
Figure 4, where an inverse relationship
between frequency of the pulsatile pressure and distensibility of the
common carotid artery was observed.
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Figure 4. Line plots show the effect of pulse pressure
frequency on the distensibility-pressure relationship of isolated
carotid arteries in Krebs buffer at 37°C (n=5; mean±SEM).
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In Vivo Versus In Situ
At 24 weeks, the WKY weighed 372±4 g, and their mean
systolic and diastolic blood pressures were 106±4
and 82±3 mm Hg, respectively. The changes in ID in the
systolo-diastolic pressure range of the WKY are shown in
Figure 5. The pulse-induced variations in
diameter were most evident in vivo. In situ, the diameter was similar
at 80 mm Hg, but it barely increased with rising pressures,
whereas in situ postmortem, the artery showed a substantial
vasoconstriction (P<0.001 versus in vivo) in addition to
very low pulsatile-induced changes. As a consequence of the preceding
findings, the distensibility-pressure curves did not differ between the
2 types of in situ measurements. However, both were dramatically lower
than the in vivo measurements (P<0.001) (Figure 6).
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Figure 5. Line plots show the relation between
intra-arterial pressure and diameter of the common carotid
artery in vivo, in situ, and in situ postmortem in WKY. In vivo vs in
situ: P<0.001; in vivo vs in situ postmortem:
P<0.001; in situ vs in situ postmortem:
P<0.05. Lines represent means; shadows,
SEM.
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Figure 6. Line plots show the relation between
intra-arterial pressure and distensibility of the common
carotid artery in vivo, in situ, and in situ postmortem in WKY. In vivo
vs in situ: P<0.001; in vivo vs in situ postmortem:
P<0.001; in situ vs in situ postmortem:
P>0.05. Lines represent means; shadows,
SEM.
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Discussion
These results clearly demonstrate that the elastic properties of
the rat carotid artery differ substantially between in vivo and in
vitro conditions. Furthermore, when compared with intact in vivo
conditions, the differences are still significant when the artery is
examined in situ in the alive animal. Although death of the animal is
associated with a constriction of the artery, the distensibility in
situ did not depend on whether the animal was alive.
The mechanical properties of the arteries were examined in vivo, in
situ, and in vitro by deriving the cross-sectional distensibility from
the diameter-pressure curve without trying to match vascular strain by
either pharmacological or physical means. The measurements were
performed on the assumption that the common carotid artery is a
cylindrical vessel, and since changes in arterial volume
are mainly due to changes in cross section, distensibility is thus
defined as the cross-sectional changes induced by pulse
pressure.21 22 The length of the exposed carotid
artery has been reported recently to vary with
pressure.23 Assuming that the ligature of the
artery does not affect the changes in length of the exposed segment of
artery, the differences between the in situ and in vivo measurements in
cross-sectional distensibility must be related to other mechanisms than
the changes in length per se. Indeed, the artery was mounted on a 5-mm
needle, so there was no significant collapse. From a solid mechanical
point of view, the "end effects" are created by the local bending
moments, which in the present case of a relatively thin artery,
dissipate very fast, in the order of 1 to 2 diameters. Since the
segment under study was typically 10 mm long, this implies that at
the middle of the segment where measurements were carried out,
interference of "end effects" was negligible. The main advantage of
cross-sectional analysis of the mechanical properties of the
carotid artery is that it allows for the first time, in contrast to
volume-pressure measurements, the comparison of in vivo, in situ, and
in vitro measurements using the same method.
The lack of hemodynamically generated shear stress at
the intima, the difference in the quality of the perfusate, the
absence of blood-borne vasoactive substances and of circulating
elements, and the low frequency of blood pressure
oscillations (0.2 Hz) were conditions prevailing both in
the in vitro and in situ measurements that could be responsible for
some of the differences found with the in vivo measurements. This may
indeed affect to different extents the arterial diameter of
the carotid arteries of WKY and SHR, in part due to a possible
alteration of the endothelial function (Table 2
) as
discussed below. However, the manually generated low-frequency
oscillations should increase the distensibility of the
vascular wall by virtue of a reduced
viscoelasticity,24 although the velocity of
stretching was not taken into consideration. Figure 4 shows an inverse
relationship between the frequency of pulsations and the distensibility
of excised rat carotid arteries. Furthermore, the arterial
wall viscosity differs significantly between in vivo and in vitro
conditions, and an active modulation of the viscous component of the
arterial wall seems to depend on the integrity of the
endothelial function.25 The high
oxygen concentration (95%) used in vitro instead of air may be
responsible for the generation of an increased reactive oxygen species
that can interfere with smooth muscle tone.
Strong evidence exists that mechanical strain modulates the secretion
of various vasoactive factors by the endothelial
cells.26 27 28 29 30 31 Pressurization produces
simultaneous strains and stresses in all directions that
are associated with insignificant flow rate in situ and in vitro
because of the presence of a ligature around the artery. Shear stress
increases as a function of the product of flow rate and fluid
viscosity. Both parameters are very low in the in situ and
in vitro measurements, and consequently shear stress is abnormally low.
A reduced release of nitric oxide and
endothelium-derived hyperpolarizing factor related to
low shear stress, and conversely an increased release of endothelin,
may favor a constriction of the vessel and presumably be partially
responsible for the decreased diameter found in vitro in the SHR and
WKY.28 29 31 32 33 However, the fact that the ID in
situ in the alive animal was close to the ID values in vivo illustrates
that factors other than flow-induced and blood-borne substances may
participate in the dilation of the vessel, in particular the central
nervous system via the ß-adrenergic system. Nevertheless, whatever
the differences in diameter in situ, in vitro, and in vivo,
arterial distensibility was dramatically decreased in the
arteries of WKY when examined in situ in the alive animal or
immediately after death and in vitro in all arteries obtained from
normotensive or hypertensive animals. This experiment did not allow us
to discriminate the effects linked to different mechanical
environments, ie, low shear stress or pattern of variation in blood
pressure, from those related to the absence of blood-borne vasoactive
factors. Indeed, further studies are needed to investigate the
importance of shear stress in the mechanical properties of the carotid
artery and also the influence of cyclic stretch, its amplitude, and its
frequency. Modulation of the arterial tone in vitro should
also give an indication of the influence of this parameter
on the mechanical properties of the artery.
The excision of vessels with resulting retraction followed by
elongation and distension has been reported to change the intrinsic
properties of the arterial wall.34
This procedure alone cannot explain the differences found in vitro and
in vivo because during the in situ measurements the artery length
remained unchanged. Nevertheless, striking differences between in situ
and in vivo measurements were also observed. Surgical exposure of the
artery might also alter its properties. Thus, to obtain similar
conditions in vivo and in situ, exposure of the artery was performed
before the in vivo measurements.
With a more constricted artery as found in vitro, the connective tissue
retracts and the load is borne by more elastic components. In WKY and
SHR, the reduced diameter in vitro was associated with a decreased
elastic modulus, ie, a low stiffness. Although the intrinsic
characteristics of the arteries were less stiff in vitro than in vivo
in the WKY and SHR, the distensibility of the arteries was dramatically
decreased. This clearly illustrates that the mechanical properties of
the artery are not solely dependent on the intrinsic properties of the
artery. The Einc gives an indication of the
stiffness of the arterial wall material independent of
vessel geometry. However, distensibility depends both on the geometry
of the artery and the intrinsic properties of the arterial
wall. Between the 2 conditions, in vitro and in vivo, the
Einc changes because of a modification of the
smooth muscle tone leading to changes in geometry. The decrease in
passive stiffness found in vitro was evidently exceeded by the change
of arterial geometry, ie, wall thickening and reduction in
diameter. It is possible to mathematically represent the
relationship between the distensibility of an artery, its material
properties, and its geometry by the following formula (d, diameter; h,
thickness):
 |
where the following formula for the incremental modulus was
used35 :
For a given artery, the CSA remains constant (incompressibility of
the wall) and the incremental modulus becomes proportional (assume
h<<d) to:
The above relation explains the seemingly controversial
finding where the arteries in vitro have lower
Einc (softer material) but are still less
distensible (lower D). This is due to the severe reduction in diameter,
which, being raised to the second power, overrides the change in
Einc and yields a lower distensibility. The above
can be demonstrated using the values for WKY at 120 mm Hg as an
example (Figures 1 through 3).
This simple calculation predicts a 2-fold decrease in the
distensibility in vitro, which is in good agreement with the values
shown in Figure 2.
There was a strong positive correlation between the CSA obtained in
vitro by ultrasonography with the 17-MHz probe and the CSA obtained at
histology. This demonstrates that histological
processing induces a similar and consistent degree of volume
reduction in all arteries. It also indicates that with the 17-MHz
ultrasonic probe, it is possible to determine accurately an
arterial wall thickness as small as 70 µm. However,
this was only possible in vitro in the dissected artery and not in vivo
in the presence of the surrounding structures.
In conclusion, the mechanical properties of the carotid artery
substantially differ in vivo, in situ, and in vitro. However, the data
from WKY and SHR show consistent elastic behavior in vitro and
in vivo in both strains of rats. Cross-sectional distensibility is
dramatically decreased in vitro in hypertrophic and normal arteries,
and this phenomenon is not related to an increased stiffness of the
arterial wall but rather to a change in geometry of the
artery in situ and in vitro. These results demonstrate that in vitro
and/or in situ measurements cannot automatically be extrapolated to in
vivo conditions.
Selected Abbreviations and Acronyms
| CSA |
= |
cross-sectional area |
| Einc |
= |
incremental modulus of elasticity |
| ID |
= |
internal diameter |
| IMT |
= |
intimal-medial thickness |
| RF |
= |
radio frequency |
| SHR |
= |
spontaneously hypertensive rats |
| WKY |
= |
Wistar-Kyoto rats |
|
Acknowledgments
This work was supported by the Fonds National Suisse de la
Recherche Scientifique, grant 3200-042515.94/1. Dr Hayoz is supported
by a career award from the Max Cloetta Foundation.
Received January 24, 1998;
first decision February 24, 1998;
accepted April 3, 1998.
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