Arterial hemodynamics and mechanical properties after circulatory intervention in the chick embryo
Division of Pediatric Cardiology, Department of Pediatrics, Children's Hospital of Pittsburgh of UPMC, Rangos Research Center Room 3320E, 3460 Fifth Ave, Pittsburgh, PA 15213, USA
* Author for correspondence (e-mail: jennifer.lucitti{at}chp.edu)
Accepted 8 March 2005
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Summary |
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Key words: chick embryo, cardiovascular development, impedance, compliance, arterial load
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Introduction |
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While the impact of hemodynamic alterations on cardiac functional
development has been well studied, the compensatory responses of the
vasculature are less well characterized. Chick embryos and Xenopus
larvae quickly alter arterial resistance and stroke volume in response to
acute changes in circulating blood volume
(Yoshigi et al., 1996;
Warburton and Fritsche, 2000
).
Within 5 h of right lateral vitelline vein ligation, embryos normalize the
ligation-induced reductions in dorsal aortic blood flow
(Stekelenburg-de Vos et al.,
2003
) even though ventricular dynamics may be altered. These
studies suggest that the regulation or maintenance of certain hemodynamic
parameters may be critical for surviving circulatory perturbations and
continuing embryogenesis.
We hypothesize that the regulation of embryonic hemodynamics is a critical factor for embryo survival and that there are specific hemodynamic patterns associated with adaptation to altered circulation. Therefore, the objective of this study is to determine which hemodynamic parameters are maintained or altered as the chick embryo adapts to altered flow or altered resistance. In the present study we used microsurgical ligation techniques to acutely alter arterial flow or arterial resistance. At three successive time points, we measured dorsal aortic pressure and flow and calculated arterial impedance, compliance, and hydraulic power to assess a range of hemodynamic parameters. Knowledge of these patterns provides insight into the regulatory capacity of the embryonic cardiovascular system.
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Materials and methods |
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For LAL, embryos were gently repositioned to their left side and the embryonic membranes above the developing left atrium were resected. A loop of 10-0 monofilament suture was positioned around the atrium and tightened, reducing effective chamber size by at least 50%. If the ligation visually appeared to reduce the chamber size by 50% or less or cause any blood loss, the embryo was immediately discarded. After successful ligation, the embryo was then repositioned, the egg was sealed with stretched parafilm and returned to the incubator. Overall survival rate was approximately 65% from ligation to time of measurement.
For VAL, membranes above the right lateral vitelline artery were gently resected and a length of 10-0 monofilament was passed below the artery and tied in an occlusive overhand knot with minimal disruption to the vitelline membrane. Venous return from this bed was not directly affected by arterial ligation. Eggs were sealed and reincubated. Overall survival rate was approximately 68%.
For CON, egg shells were windowed, the membranes were resected above the embryo, and eggs were sealed and reincubated. Survival was approximately 90%. After approximately 1 h of post-intervention recovery (HH21), 14 h (HH24) or 32 h (HH27), embryos were prepared for hemodynamic measurements. After measurements were taken, each embryo was discarded.
Hemodynamic measurements
We measured simultaneous dorsal aortic blood pressure with a servo-null
system (900A, WPI, Sarasota, FL, USA) and dorsal aortic blood velocity with a
pulsed-Doppler velocimeter (Triton, San Diego, CA, USA) and a 0.5 mm custom
mounted probe (Iowa Doppler Products, Iowa City, IA, USA) as previously
described (Tobita et al.,
2002; Yoshigi et al.,
1996
) (Fig. 1A).
Dorsal aortic diameter was imaged for individual HH21 and HH24 embryos using a
video camera (model 70, Dage-MTI, Michigan City, IN, USA) mounted on a
dissecting microscope. We calibrated the image analysis software (Scion Image,
Scion Corp, Frederick, MD, USA) using an etched glass standard. Diameters were
determined at two magnifications, compared with each other to verify accuracy,
and then averaged to yield one diameter per embryo. After correction for the
Doppler probe angle, flow was calculated as the product of the instantaneous
velocity and the cross sectional area. Because the increasingly opaque body
wall hampered dorsal aortic imaging at HH27, we imaged the dorsal aortas of
separate groups of embryos using a high resolution ultrasound system equipped
with a 40 MHz probe (Vevo 660, VisualSonics, Toronto, Ontario, Canada).
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We used common hemodynamic measures as a gauge of arterial wall
characteristics. Arterial impedance describes the opposition of the
vasculature to both the steady and pulsatile aspects of blood flow and
determines how much work the heart must perform to produce given pressure and
flow pulse contours. Total vascular resistance (TVR) represents the
steady opposition to blood flow (Nichols
and O'Rourke, 1998). Characteristic impedance
(ZC) quantifies impedance in the absence of reflected
waves, a situation that is not physiological but can yield information
regarding the site of measurement, such as relative stiffness
(Nichols and O'Rourke, 1998
).
Impedance at the first harmonic (Z1) refers to the
impedance modulus that corresponds to the most prominent oscillatory
frequency, the heart rate. Total arterial compliance (CA)
describes arterial wall distensibility. Total hydraulic power
(WT) is an index of the energy required by the heart to
maintain pressure and flow pulsations while both expanding distensible vessels
with blood (oscillatory component, WO) and distributing
blood to the periphery (steady component, WS). Factors
that influence these parameters include arterial diameter, the elastic
properties of the arterial wall, wall thickness and vascular tone. Of note,
the above measurements assess the arterial system at/peripheral to the dorsal
aorta and do not include the cranial circulation or pharyngeal arch
arteries.
Data analysis
We calculated basic hemodynamic parameters in a customized LabVIEW
(National Instruments, Austin, TX, USA) environment. Cycle length and waveform
features were determined manually. Input impedance spectra were generated as
previously described (Yoshigi et al.,
1996) (Fig. 1B,C).
We defined TVR as the impedance modulus at 0 Hz,
Z1 as the impedance modulus at the first harmonic, and
ZC as the average of the impedance moduli from the third
harmonic up to 10 Hz. Global CA was calculated using the
area under the pressure waveform as:
![]() | (1) |
where VS is stroke volume, PN and
PD are pressure at the dicrotic notch and end diastole,
respectively, and AS and AD are the
areas under the aortic pressure waveform during systole and diastole,
respectively. Steady power (WS) was calculated as:
![]() | (2) |
where and
are mean pressure and flow,
respectively. Oscillatory power (WO) was calculated as:
![]() | (3) |
where |Qn|,
|Zn| and n are the flow
modulus, the impedance modulus, and the impedance phase angle at the
`nth' harmonic. Oscillatory fraction of hydraulic power is:
![]() | (4) |
Total power (WT) was calculated as:
![]() | (5) |
Statistics
Data are reported as mean ± S.E.M.
Heart rate, blood pressure, stroke volume, and changes in vascular impedance
and hydraulic power were first analyzed by ANOVA followed by Tukey
post-hoc analysis. Statistical significance was determined at a level
of 5% alpha error between groups for a single measure
(P<0.05).
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Results |
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HH24
All pressure parameters were similar to controls. Stroke volume and
remained depressed. Although
ZC normalized at this stage, TVR became elevated,
reflecting a more global change in arterial resistance. Global compliance and
WS power normalized by HH24 while WT
and WO remained lower than CON values (P=0.08 and
P=0.07, respectively).
HH27
Pressure parameters were similar to both CON. Stroke volume,
and fH also
normalized to CON values. Compliance, all impedance and all hydraulic power
parameters were similar to CON values.
Vitelline artery ligation HH21
One hour after ligation, all pressure parameters were similar to CON values
(Table 1). However,
VS and declined
(Table 2). Total vascular
resistance and Z1 both significantly increased while
characteristic impedance was unaffected
(Fig. 2A-C). The
CA decreased (Fig.
3). The WT and WS were
similar to controls although WO was reduced
(Fig. 4A-C). Percent
oscillatory power was similar to controls
(Fig. 5).
HH24
Dicrotic notch pressure and pulse pressure were elevated although other
pressure parameters mirrored CON values. Total vascular resistance and
Z1 remained elevated and ZC became
elevated as well. Arterial compliance remained low. Total, steady and
oscillatory power became low. Since WO and
WT changed proportionally, %WO
remained similar to CON values.
HH27
Although pressure parameters normalized, VS and
remained low. Similarly,
CA remained low and TVR, Z1 and
ZC remained elevated. All hydraulic power parameters were
similar to CON values.
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Discussion |
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Basic hemodynamics following LAL and VAL
Increasing arterial resistance with VAL caused a drastic decrease in
VS and .
Conversely, reducing VS and
via LAL caused an increase in
resistance parameters. Regardless of intervention, systolic, diastolic and
mean pressures were maintained 1 h after both LAL and VAL and at subsequent
stages. These observations indicate that maintaining mean and pulsatile
pressure, as opposed to arterial flow or resistance, is essential for embryo
survival. Forces associated with intraluminal pressures, such as cyclic
stretch and strain, are known to modulate vascular smooth muscle cell
proliferation, phenotype, and a variety of signaling cascades in both vascular
smooth muscle and endothelial cells
(Birukov et al., 1995
;
Sackin, 1995
;
Reusch et al., 1996
;
Xu et al., 1996
;
Birukov et al., 1997
;
Hishikawa and Luscher, 1997
;
Cheng et al., 1998
;
Lehoux and Tedgui, 1998
;
Iwasaki et al., 2000
). Since
the arterial vasculature undergoes rapid growth and differentiation at these
stages (i.e. only a thin layer of vascular smooth muscle cells surround the
proximal arteries and many ECM proteins, such as elastin, are not yet present
(Hughes, 1943
;
Bergwerff et al., 1996
),
precise regulation of these processes may be critical to embryo survival.
Because vascular tone is not centrally regulated during these early stages of
avian embryogenesis (Altimiras and
Crossley, 2000
; Crossley and
Altimiras, 2000
) arterial responses must be exerted via
local control of tone and/or passive tissue properties.
Although all pressure values were similar to CON values 1 h after ligation,
most were different between VAL and LAL groups. In HH24 chick embryos,
infusion and withdrawal of vascular volume causes immediate dose-dependent
increases and decreases, respectively, in mean and peak arterial pressure that
were countered by changes arterial impedance within the 30-100 s observation
period (Yoshigi et al., 1996).
Similarly, bolus injections of saline and a volume expander increase arterial
pressure by 6-15% in the relatively older Nieuwkoop-Faber
(Nieuwkoop and Faber, 1994
)
stage 49-51 Xenpous laevis larvae
(Warburton and Fritsche,
2000
). Larvae quickly attenuated arterial pressure changes
via changes in stroke volume and arterial resistance and most
restored arterial pressure to pre-injection levels within 15 min. In the
present study, it is possible that arterial pressure decreased immediately
after LAL and increased immediately after VAL but normalized within the one
hour period between ligation and measurement. Regardless, it is evident that
the rapid restoration of arterial pressure is a primary directive of the
embryonic vascular system.
An essential role of blood flow is the delivery of oxygen to tissue and the
removal of metabolic waste products. Burggren et al.
(2000) completely occluded the
outflow tract of approximately HH18-HH25 chick embryos and observed that
ligated embryos grew at the same rate as control embryos for the 4-8 h
observation period. The authors speculated that embryonic oxygen requirements
were likely met through diffusion and that blood flow was not immediately
critical for survival at these stages. This same group partially occluded
conotruncal flow in the HH18 chick embryo. This treatment did not affect body,
eye or chorioallantoic membrane growth in the subsequent 36 h (to HH24)
(Burggren et al., 2004
). The
authors propose that, at these stages, arterial flow may occur in advance of
the need for convective flow to tissues to ensure adequate vascular
performance at the time when convective flow becomes critically important to
survival. It is well established that blood flow stimulates cellular
activities via shear stress responsive elements associated with
endothelial cells and the extracellular matrix and that arterial flow patterns
may be important for normal vascular expansion and wall maturation. Thus, the
relatively simple embryonic cardiovascular system may tolerate certain
functional deficits that could become problematic in fetal and post-natal
life. The long-term consequences of developing under conditions of low
arterial flow are not known. In light of the present data, we propose that,
during these stages of embryogenesis, reducing arterial flow, rather than
arterial pressure, is the preferred mechanism employed to balance circulation
deficiencies.
Impedance and compliance following LAL and VAL
Infusion and withdrawal of peripheral blood volume in HH24 chick embryos
causes immediate compensatory changes in peripheral impedance and
Z1 but not ZC
(Yoshigi et al., 1996).
Although we did not remove blood volume, we reduced aortic flow by reducing
VS via LAL. Acutely reduced aortic flow may have
triggered local vasoconstriction within the large arteries and account for the
observed change in ZC, Z1 and
CA but not TVR at HH21. Continually low
may cause volume to shift from the
embryonic arterial system to the compliant venous system. Reduced arterial
volume, potentially coupled with associated changes in vascular structure, may
then be responsible for inducing peripheral vasoconstriction, as noted by the
increase in TVR by HH24. However, adaptive cardiac remodeling is
known to occur after LAL (Sedmera et al.,
1999
) and presumably, once VS and
recovered, ZC,
Z1 and TVR and CA
normalized.
Total vascular resistance and impedance parameters generally decrease as
the embryo develops due to the rapid growth and expansion of the arterial
circulation (Zahka et al.,
1989; Yoshigi et al.,
1996
). Resistance parameters followed this trend in both CON and
LAL embryos. By contrast, these parameters, as well as compliance, did not
change between HH21 and HH24 in VAL embryos. Considering that dicrotic notch
and pulse pressure, which are indices of arterial stiffness, also increased at
this stage, arterial stiffness increased appreciably by HH24 without
observable detrimental effects to morphogenesis. It is worth noting that
although aortic valve leaflets have not yet developed, outflow tract cushions
appear to function as valves (VanMierop
and Bertuck, 1971
; Keller et
al., 1990
), though they may not be fully competent
(Ursem et al., 2001
). As
ventricular pressure exceeds aortic pressure, blood is ejected into the aortic
sac until sac pressure exceeds ventricular pressure. We assume that wave
reflection occurs in the viscoelastic, branching embryonic arterial system and
that, similar to mature cardiovascular systems, summation of reflected
pressure waves terminates ventricular ejection earlier in the cardiac cycle
(thus, at a higher pressure) in stiffer conduit arteries due to a faster
transit time. Although resistance and impedance were still elevated at HH27,
they became much closer to CON values. We speculate that between HH24 and
HH27, adaptive vascular remodeling within the embryo and/or accelerated
expansion of the extra-embryonic vascular systems occurred to reduce
opposition to blood flow. These embryos showed a remarkable ability to
maintain a normal growth trajectory while experiencing a marked increase in
arterial stiffness and arterial flow opposition.
The observation of an increase in fH after LAL was
unexpected because, in general, the early embryo does not adjust
fH to compensate for moderate changes in cardiac function
(Keller et al., 1997). At
HH21, pacemaker depolarization occurs in the region of the sinus venosus and
the depolarization front travels through the ventricular area to the outflow
tract at varying velocities, depending on the cardiac segment
(de Jong et al., 1992
).
Ligating a large percentage of the left atrium may significantly deform the
atrium and while bringing the sinus venosus and atrioventricular canal closer
together at the inner curvature of the heart. This deformation of the atrium
may have increased the resting stretch on pacemaking cells within the atrium
with a subsequent alteration in stretch-sensitive ion channels and decay in
membrane potential, resulting in more rapid triggering of myocyte
depolarization. By HH24, fH in LAL embryos was similar to
CON and VAL embryos, consistent with a return to normal depolarization
rates.
Hydraulic power following LAL and VAL
Left atrial ligation caused an acute decrease in hydraulic power parameters
and increase in HR. Theoretically, increased HR favors steady power at the
expense of oscillatory power. However, percent oscillatory power was
unaffected by LAL. In fact, %WO did not change in any
experimental group at any stage. Hydraulic power parameters were altered after
acute alteration of blood volume in chick embryos
(Yoshigi et al., 1996).
However, %WO remained stable except at the highest level
of volume alterations. Often referred to as `wasted' energy, oscillatory
energy produces cyclic stretch. Cyclic stretch impacts cellular activities
via mechanotransducers and affects many functions that are essential
to arterial growth (Birukov et al.,
1995
; Wilson et al.,
1995
). In the adult circulation, %WO is
approximately 10% (O'Rourke,
1967
) and is much lower than the approximately 23-33% observed
over three developmental stages in this study and the approximately 25%
observed by Yoshigi et al.
(1996
) in HH24 chick embryos.
A precise balance between oscillatory and steady hydraulic power may be
required for normal embryonic growth, despite changes in absolute values.
In conclusion, we found that arterial pressure is maintained at the expense of stroke volume and blood flow at all stages observed. Additionally, the %WO was conserved in all groups at all stages regardless of changes in other hydraulic power parameters. Together, these data suggest that the maintenance of arterial pressure and oscillatory vascular stretch is necessary for short-term embryogenesis while arterial flow is not, although the long-term consequences of this compensatory mechanism are not known.
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Acknowledgments |
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