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1 Department of Biological Sciences, University of North Texas, Denton, Texas 76203; and 2 Departament of Biology, Institute of Physics and Measurement Technology, Linköpings Universitet, SE-58183 Linköping, Sweden
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIAL AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Renewed interest in the use of
the embryonic chicken as a model of perinatal cardiovascular regulation
has inspired new questions about the control mechanisms that respond to
acute perturbations, such as hypoxia. The objectives of this study were
to determine the cardiovascular responses, the regulatory mechanisms
involved in those cardiovascular responses, and whether those
mechanisms involved the central nervous system (CNS) of embryonic
chickens. Heart rate (fH) and blood pressure were measured
in chicken embryos of different incubation ages during exposure to
different levels of hypoxia (15, 10, and 5% O2). At all
levels of hypoxia and at all developmental ages, a depression of
fH and arterial pressure was observed, with the exception
of day 20 embryos in 15 and 10% O2. The
intensity of the embryonic fH and blood pressure responses were directly related to the level of hypoxia used. Muscarinic and
-adrenergic receptor stimulation limited the hypoxic hypotension on
days 15-19 and 15-21,
respectively, as indicated after blockade with atropine and
phentolamine. During the final 3 days of incubation, the intensity of
the hypoxic hypotension was magnified due to -vasodilation caused by
-adrenergic and muscarinic receptor stimulation. In 19- to
21-day-old embryos, the fH response to hypoxia was limited
by -adrenergic receptor stimulation as indicated by the accentuated
bradycardia after blockade with phentolamine. Furthermore, on day
21, atropine limited the hypoxic bradycardia, indicating that
muscarinic receptors also play a role in the fH response at
this age. In addition, the muscarinic actions on the heart and the
adrenergic effects on the vasculature appeared to occur through a
hypoxic-induced direct release from chromaffin tissue and autonomic
nerve terminals. Thus, in embryonic chickens, the only cardiovascular
response to hypoxia that involves the CNS was the cholinergic
regulation of arterial pressure after day 15 of incubation.
Therefore, although embryonic chickens and fetal sheep, the standard
models of perinatal cardiovascular physiology, respond to hypoxia with
a similar redistribution of cardiac output, the underlying mechanisms
differ between these species.
catecholamine; autonomic; adrenergic; muscarinic; perinatal hypoxia
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIAL AND METHODS
RESULTS
DISCUSSION
REFERENCES
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EMBRYONIC CHICKENS EXPOSED to
hypoxia show an -adrenergic-mediated redistribution of cardiac
output with the preferential perfusion of the brain, heart, and
chorioallantoic membrane (CAM; 18, 20). This pattern of hypoxic
redistribution of cardiac output is similar to that seen in fetal
sheep, which is known to accompany redistribution of blood flow with
reflexive changes in heart rate and peripheral resistance
(12). In the sheep fetus, the neural reflex, a
vagal-mediated bradycardia, and an -adrenergic efferent-mediated hypertension are followed by numerous endocrine responses (12, 13). However, recent findings in embryonic chickens suggest that
cardiovascular regulation at the time of hatching is less developed in
chickens than in sheep at birth. This evidence includes the absences of
vagal tone throughout the prenatal period in chickens (10), the late (day 19) appearance of
baroreflexive responses (1), and the hypotension displayed
when exposed to hypoxia (10, 24). These three
characteristics of chicken development differ from those found in fetal
sheep during a similar period of gestation in response to similar
experimental conditions (11, 23).
Therefore it was hypothesized that embryonic chickens would rely on endocrine control mechanisms during acute periods of hypoxia. Furthermore, given the importance of adrenergic receptor stimulation in maintaining normal cardiovascular function in embryonic chickens (10), we also hypothesized that this would be the primary mechanism for regulating blood pressure and heart rate during hypoxic challenges (20). Thus the goal of this study was to determine the heart rate and arterial pressure responses, the regulatory mechanisms involved in those responses, and the role of the autonomic nervous system in regulating cardiovascular function during hypoxia in embryonic chickens.
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MATERIAL AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIAL AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects of study. Freshly laid chicken eggs, Gallus gallus (White Leghorn strain), were purchased from University of Texas A&M and shipped overnight to the University of North Texas, Department of Biological Sciences. On arrival, eggs were placed in incubation at 38 ± 0.5°C, 60-70% relative humidity and turned automatically every 3 h.
Surgical procedures. Before each experimental series, eggs were removed from the incubator, candled to locate a chorioallantoic artery, and placed in a holder thermostatically controlled at 38 ± 0.5°C. A 1-cm2 portion of the eggshell was then removed, exposing the previously located artery. This artery was then occlusively catheterized with heat-pulled PE-90 tubing filled with heparinized 0.9% saline under a dissection microscope (Wild M3Z). Once the catheter was in place, it was fixed to the shell with cyanoacrylic glue. Subsequently, the egg was placed in the experimental chamber that consisted of a water-jacketed glass container fitted with a glass lid. The lid had three ports, providing an avenue for externalizing the arterial catheter as well as routes for inflow and outflow of different gas mixtures. During the experiments, all eggs were maintained at 38 ± 0.5°C in water-saturated air.
Signal recording and calibration. The arterial catheter from each egg was attached to a pressure transducer (WPI, type BLPR), and this was connected to a bridge amplifier (CB Sciences, model ETH-400). Pressure signals were stored in a computer using PowerLab data-acquisition software. Heart rate was continuously calculated from the pressure signal via an acquisition software tachograph. Reference zero pressure was set at the top of the experimental bath, and all values were corrected after the experiment as previously described (1).
Experimental protocol.
The study consisted of six different experimental series. The number of
embryos used in each series at each incubation age is indicated in
Table 1. All embryos were only used in
one experimental series. All series began with a control period of 30 min postsurgery to allow blood pressure and heart rate to reach stable
values. Embryos that failed to do so were removed from the study. For all series that involved pharmacological manipulations, drugs were
administered via a T connector in the arterial catheter line. Each drug
injection was followed by a saline flush with double the volume of the
drug solution. Total injection volumes were always <5% of the total
blood volume. This volume had no significant effect on cardiovascular
function as previously reported (1). For all experimental
series, 20-day-old embryos were defined as internally pipped eggs
verified by candling. Twenty-one-day-old embryos were defined as
embryos externally pipped. The sequence of experimental series
described represents the flow of the investigation from the general
hypoxic response to the determination of the receptors involved and
then the contribution of any reflexive responses.
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-adrenergic antagonist
propranolol (3 mg/kg) and the -adrenergic antagonist phentolamine (1 mg/kg). The antagonists were always given in the same order with a
stabilization period after the injection of 30-60 min.
In series III, embryos were catheterized on days
18, 19, 20, and 21 of incubation
and allowed 30 min to reach control blood pressures and heart rates.
Subsequently, a control blood sample (200 ml) was taken from the
arterial catheter and immediately spun down to separate the plasma. The
erythrocytes were then suspended in 0.9% saline to the original
volume, withdrawn, and injected back into the embryo via the arterial
catheter. Plasma samples were then mixed with 5 µl of an
EGTA-glutathione solution (0.2 M-0.2 M) to prevent catecholamine
oxidation. A second blood sample (200 ml) was taken after a 5-min
exposure to 10% O2 and prepared as described. Plasma
epinephrine and norepinephrine concentrations in the normoxic and
hypoxic samples were determined using HPLC techniques previously
described by the authors (10).
Series IV and V were carried out to distinguish
between neural and humoral catecholamine actions during hypoxia. This
differentiation was accomplished using chemical sympathectomy with
6-hydroxydopamine (6-OH). In fetal sheep, sympathectomy is carried out
over a period of days (serial injections) to ensure the total
destruction of sympathetic terminals (4). In this series,
tyramine was used as a selective norepinephrine-releasing agent
(29). Injections before and after treatment with 6-OH were
used to test for the presence of functional sympathetic nerve terminals
and to verify the degree of chemical sympathectomy achieved 60 min
after a bolus injection of 6-OH. Thus, in series IV, after
the catheterization and a 30-min control period, a single injection of
tyramine (10 mg/kg) was given to embryonic chickens on days
12, 15, 18, 19, 20,
and 21 of incubation. After a 30-min recovery period,
chemical sympathectomy was conducted with 6-OH (20 mg/kg) only on
days 15, 18, 19, 20, and
21 of incubation because tyramine showed no effects on
day 12. After 60 min, the injection of 6-OH was followed by
a second administration of tyramine (10 mg/kg) for comparisons of the
cardiovascular response to tyramine before and after 6-OH treatment.
In series V, after a 30-min control period, chemical
sympathectomy with 6-OH (20 mg/kg) was carried out as in
series IV in embryos on days 15,
18, 19, 20, and 21 of
incubation. After a 60-min recovery period, 6-OH-treated embryos were
exposed to hypoxia (10% O2), and cardiovascular response
was recorded as in series II.
In series VI, after the surgical recovery period (30 min),
embryonic chickens at days 15, 18, 19,
20, and 21 were exposed to a 5-min hypoxic (10%
O2) period. A recovery period was then allowed (60 min)
before an injection of the ganglionic blocking agent hexamethonium (25 mg/kg) was conducted. After the injection, arterial pressure and heart
rate stabilized within 30 min. This was followed by a second 5-min
hypoxic (10% O2) exposure and recovery.
At the completion of all series, embryos were euthanized with an
overdose of pentobarbital sodium and KCl. The eggs were then frozen to
determine the heart position needed for correction of the blood
pressure values (1).
Statistical analysis. A matched-pairs Wilcoxon nonparametric test was used to assess statistical differences in heart rate and blood pressure before and after exposure to hypoxia with or without drugs. A U-Mann-Whitney comparison nonparametric test was conducted between adjacent days of incubation to determine changes in the cardiovascular response to 10% O2 as well as the responses to various blocking agents. A Bonferroni correction was applied for data used more than once in a given analysis. All data are presented as means ± SE.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIAL AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Series I: effects of hypoxia.
Chicken embryos responded to all levels of hypoxia (15, 10, and 5%
O2) with a significant (P < 0.05)
hypotensive bradycardia up to day 19 of incubation. This
pattern differed on days 20 and 21 of incubation
as illustrated by the representative traces in Fig.
1. Before day 20 of
incubation, changes in mean arterial pressure (MAP) and heart rate were
related to the severity of the hypoxic challenge, with significant
differences between hypoxic responses. MAP dropped an average of 12%
(15% O2), 18% (10% O2), and 26% (5%
O2), whereas heart rate dropped an average of 9% (15% O2), 19% (10% O2), and 34% (5%
O2) during this period of study (Fig.
2). On day 20 there was no
pressure response to 15% and 10% O2, but 5%
O2 resulted in a drop in MAP and heart rate. Day 21 embryonic chickens reverted to the hypoxic hypotensive
bradycardia to all levels of hypoxia shown in earlier days of
incubation (P < 0.05).
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Series II: hypoxic responses after muscarinic and adrenergic
antagonists.
The cardiovascular responses to muscarinic as well as - and
-adrenergic blockade were similar to those previously described (10) and will not be discussed further.
1 to a postatropine
hypoxic bradycardia of 10 ± 6 min1
(P < 0.05; Fig. 3).
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-Blockade
produced a significant (P < 0.05) decrease in MAP
during hypoxia compared with the response after atropine and
propranolol injection on days 15, 19,
20, and 21 of incubation (Fig. 4C).
The average hypoxic change in MAP after phentolamine increased with
development: 0.06 kPa on day 12, 0.21 kPa on day
15, 0.26 kPa on day 18, 0.74 kPa on day 19, 1.44 kPa on day 20, and 1.66 kPa on day 21. In
addition, during the final 3 days of incubation, phentolamine resulted
in an increased hypoxic bradycardia that was significantly different
(P < 0.05) from that of embryos treated with atropine
and propranolol alone on days 19 and 20 (Fig.
4D). Large differences between embryos on day 21 may account for the nonsignificant change in hypoxic heart rate
response on this day of incubation (P < 0.06) (Fig. 4D).
Series III: catecholamine release during hypoxia.
A marked release of catecholamines occurred during exposure to 10%
O2 in day 18 embryos and older (Table
2). Norepinephrine release peaked on
day 19 (a 16-fold increase above normoxic levels), whereas
epinephrine release was maximal on day 20 (a 15-fold
increase).
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Series IV and V: hypoxic response after chemical sympathectomy.
A single administration of tyramine (series IV) induced a
significant hypertension in embryonic chickens at day 15 of
incubation and older, producing an average elevation in pressure
ranging from 0.16 to 0.75 kPa (Table 3).
In addition, day 19 and 21 embryos showed a
significant tachycardic response to tyramine injection (Table 3).
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Series VI: hypoxic response after ganglionic blockade.
Hexamethonium injections triggered changes in MAP and heart rate
that were similar to those previously shown over the same period of
chicken incubation (10). The hypoxic response
posthexamethonium was significantly different during the late stages of
embryonic development (Fig. 5). An
enhancement of the hypoxic hypotension was observed on days
18 (a 31% greater pressure drop) and 19 (a 84%
greater pressure drop), with no difference on day 20. On
day 21, the effects of hexamethonium were reversed compared
with previous days with a reduction in the hypoxic hypotension after
hexamethonium (72% reduction in the pressure drop; Fig. 5). These
changes in arterial pressure to 10% O2 after hexamethonium
were not accompanied by differences in the heart rate response to
hypoxia (Fig. 5).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIAL AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Throughout the second half of incubation, embryonic chickens
of the White Leghorn strain exhibited a clear depression of heart rate
and arterial pressure when exposed to hypoxia as previously reported
(24). The intensity of this response was directly related to the intensity of the hypoxic exposure, with the largest effects observed in all embryos that were exposed to 5% O2 (Fig.
2). Early in development (day 12 of incubation), the hypoxic
bradycardia appeared to be primarily caused by the direct action of low
O2 on the cardiac muscle. By the end of the incubation,
this response appeared also to be due to stimulation of cholinergic
receptors (day 21). In addition, the hypoxic hypotension
found in embryonic chickens was limited by both an -adrenergic- and
a cholinergic receptor-stimulated vasoconstriction from days
15 to 19 in embryonic chickens. During the final 3 days
of incubation, a third regulatory element was present, namely a
-adrenergic-stimulated vasodilator tone. At the same time, a
reversal of the cholinergic response (from vasoconstrictor to
vasodilator) appeared on day 21. The pharmacological
evidence suggests that the cholinergic receptor stimulated action on
pressure during hypoxia originated above the ganglionic level.
Conversely, the adrenergic receptor-stimulated pressure changes were
predominantly derived from the humoral catecholamine response,
with a neural contribution during the last days of incubation. Thus, in
embryonic chickens, hypoxia appeared to directly stimulate chromaffin tissue and sympathetic nerve terminals to release
catecholamines. This then stimulates adrenergic receptors, causing
changes in heart rate and arterial pressure. Furthermore, the
cholinergic receptor-stimulated changes in arterial pressure alone
originated above the ganglionic level, possibly indicating a reflexive
mechanism controlling pressure in embryonic chickens.
Effects of hypoxia in embryos up to 18 days of incubation.
Until day 18 of incubation, the hypoxic bradycardia evident
in embryonic chickens was not due to a reflexive (neural) response. This statement is based on the persistent hypoxic bradycardia after
ganglionic blockade with hexamethonium (Fig. 5). In addition, the
cholinergic and adrenergic receptor stimulation contributed little to
the chronotropic response to hypoxia in embryos as was evident in the
persistent hypoxic bradycardia after - and -adrenergic blockade
(Fig. 4). Therefore, at these early developmental stages (
18 days),
the most relevant finding was the existence of a muscarinic-dependent regulation of systemic arterial pressure during hypoxia. Such a
cholinergic vasomotor control is absent in mammals but is present in
adult birds (3). Thus, on day 15, cholinergic
receptors are involved in a vasoconstrictor response during hypoxia,
lessening the severity of the hypoxic hypotension.
Effects of hypoxia in embryos older than 18 days.
Compared with earlier days of incubation, cardiovascular regulation
during the last 3 days of chicken incubation became complex. This
increased complexity was caused by the appearance of a muscarinic, -adrenergic, and -adrenergic receptor stimulation action on the
heart as well as the vasculature during hypoxia. Therefore, these
receptors may be paramount to maintaining cardiovascular function in
the chicken through the late perinatal and hatching periods.
-adrenoceptors on the heart cannot be excluded as previously
reported in fetal lambs (8). If a positive -adrenergic
stimulation of heart rate occurred during hypoxia it was likely due to
the direct hypoxic induced release of norepinephrine from sympathetic
terminals. This is based on the chemically sympathectomized embryos,
which displayed a greater hypoxic bradycardia on day 19 and
20 of chicken incubation (Table 5). Given that -blockade
did nothing to the hypoxic heart rate response (Fig. 4B),
the adrenergic limitation of the bradycardic intensity must originate
from -adrenergic stimulation. Furthermore, that the hypoxic
bradycardia was magnified after partial sympathectomy (Table 5) but not
after hexamethonium (Fig. 5) suggests that the adrenergic receptor
stimulation of the heart was caused by a direct hypoxic-induced release
of catecholamines from the sympathetic nerve terminals. This type of
nonreflexive hypoxic heart rate response was also present in externally
pipped (day 21) embryos.
In externally pipped embryos (21 days), hypoxic bradycardia could be
eliminated via muscarinic blockade with atropine (Fig. 2) but not via
ganglionic blockade with hexamethonium (Fig. 5), indicating that the
cholinergic response on day 21 was not reflexive. The
effects of atropine on day 21 contrast with those of a prior study (10) and could be attributed to the less-precise
determination of embryonic age in an earlier study by the authors.
However, when combined, the atropine and hexamethonium data indicate
that the hypoxic depression of heart rate in embryonic chickens occurs without an increase in vagal activity and thus was due to the direct
effects of hypoxia.
As previously reported, tonic regulation of the total embryonic chicken
vasculature (embryonic plus extraembryonic: yolk sac and
chorioallantois) is based on a -adrenergic vasodilation superimposed on an -adrenergic vasoconstriction (10). During hypoxia
the -adrenergic tone was elevated, limiting the fall in CAM arterial pressure in embryos during the last third of incubation (Fig. 4). On
days 15 and 18, however, the -adrenergic
stimulation was insufficient to offset the overriding hypoxic reduction
in arterial pressure. Later (days 19-21) the
-adrenergic response was sufficient to cause a general hypoxic
hypertension that is overridden by a -adrenergic vasodilation (Fig.
4). The main site of -adrenergic vasodilation appeared to be the
chorioallantoic vascular bed, as shown in preliminary experiments with
in vitro perfusion of this isolated vascular bed (Crossley, unpublished
results). The CAM also shows a limited vasoconstriction after
-adrenergic stimulation with phenylephrine. Therefore, systemic
release of catecholamines (Table 3) during hypoxia in late-stage
embryonic chickens would result in a vasodilation of the CAM vessels
via -adrenoceptors while producing a vasoconstriction in some of the
intraembryonic vessels via -adrenergic receptors. With an estimated
CAM blood flow of 20-50% of total cardiac output (2, 18,
21, 26, 27), CAM vasodilation could account for the global
hypotension that occurred during hypoxia. Interestingly, the hypoxic
pressure response to mild and moderate levels (15 and 10%
O2) was much less accentuated in internally pipped embryos
(day 20). Taking into account that effective lung
ventilation starts on day 20, the differences in responses
to mild and moderate hypoxia could be attributed to a transient
resetting of the sensitivity to hypoxia. The change in function of the
cholinergic pressure control system from a hypoxic vasoconstriction (up
to day 20) to a vasodilation (on day 21) may also
contribute to the different response found on day 20.
Adrenergic activation: neural vs. humoral contribution.
In fetal sheep, adrenergic stimulation brought about by acute hypoxia
is made up of a combination of increased nervous adrenergic drive and
adrenal release of catecholamines (7, 9, 14, 17). Both
mechanisms are possible in embryonic chickens given the effects of
-blockade (Fig. 4) and the increased titers of catecholamines in the
plasma during hypoxia (19). However, using field
stimulation, release of norepinephrine from sympathetic terminals has
been shown to occur only during the last day of incubation
(22). This suggests that in embryonic chickens the humoral
adrenergic response is of greater importance during hypoxia than the
neural adrenergic response. In an effort to isolate the origin of the
catecholamine response to hypoxia in embryonic chickens, 6-OH was used
to eliminate the neural originating catecholamines. Unfortunately,
complete chemical sympathectomy with 6-OH was not fully achieved in
this work given that the effects of tyramine were lowered but not
abolished. Thus conclusions based on the response to hypoxia after 6-OH
treatment must be viewed with caution. Acknowledging this
consideration, the hypoxic pressure response of day 20 embryos was altered by treatment with 6-OH (Table 5). Thus day
20 embryonic chickens release catecholamines from sympathetic terminals to maintain arterial pressure during hypoxia challenges. Therefore, the sympathetic terminals are capable of releasing catecholamines during hypoxia before they were previously suggested to
be functional and may contribute to the pressure response on this day
of incubation (22). To further clarify the source of the
hypoxic catecholaminergic and muscarinic response in embryonic chickens, hexamethonium, an antagonist of nicotinic receptors, was
administered. Hexamethonium blocks autonomic transmission at the
ganglionic level of both cholinergic and adrenergic fibers. Thus it
blocks the centrally mediated release of catecholamines from adrenergic
nerve terminals and adrenal glands. Few changes in the cardiovascular
response to hypoxia were evident after hexamethonium, with those
effects seen mimicking the effects previously determined with atropine.
This indicates that hexamethonium did not affect the adrenergic humoral
response. Thus the adrenergic response was triggered by the direct
action of low oxygen on the chromaffin cells of the adrenal tissue as
well as sympathetic terminals and did not involve an autonomic nervous
system-originating reflex.
Perspectives
Upon exposure to hypoxia, chicken embryos display both similar features and unique regulatory mechanisms compared with fetal sheep, the standard model in the study of perinatal cardiovascular regulation. Embryonic chickens exhibit a greater bradycardic response to reduced O2 levels than do fetal sheep at a corresponding developmental age (based on percentage of gestation) (13). In chickens, the autonomic nervous system seems to play only a limited role, with the direct effect of oxygen levels on the heart as well as other local systems dominating the response to hypoxia. A contributing factor to the differing hypoxic heart rate and arterial pressure responses between these species may be the presence of a greater resistance to oxygen diffusion in chicken embryos. In chickens, this larger resistance to gas flux (the eggshell through pores and the shell membranes) causes a low oxygen saturation of systemic blood (as low as 27%) (25) compared with the 60% saturation reported in fetal sheep (15). Thus small changes in environmental O2 could result in larger changes in blood PO2 levels in chicken embryos producing a greater sensitivity to hypoxic exposure compared with fetal sheep.Fetal sheep and embryonic chickens also differ in terms of their
regulation of the hypoxic response. This was evident in the hypoxic
hypotension of embryonic chickens instead of the reflex hypertension
displayed by fetal sheep (13). This difference may be due
to the existence of an important -adrenergic receptor-dependent vasodilation of the CAM vasculature in chickens, a character not shared
by its mammalian analog, the placenta, which has been found to be
catecholamine insensitive (5, 28). This CAM dilation in
chickens may counteract the -adrenergic-stimulated vasoconstriction found in both species during hypoxia derived from catecholamines originating from the adrenal medulla and sympathetic nerves in later
embryonic development. Thus this possibly accounts for the differing
hypoxic pressure responses between embryonic chickens and fetal sheep.
Furthermore, there is evidence that cholinergic receptors are involved
in the vascular control in chicken embryos, which again differs from
fetal sheep. Thus the redistribution of cardiac output during hypoxia
is similar between chicken and sheep (18); however, it
appears to be achieved via differing mechanisms. This implies that the
maintenance of blood flow to the heart, the brain, and exchange organ
(CAM or placenta) is not dependent on the same regulatory mechanisms
between these species.
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ACKNOWLEDGEMENTS |
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We are greatly indebted to G. Rydgren for catecholamine analysis.
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FOOTNOTES |
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The work was supported by National Science Foundation Grant 1BN-9616138 to W. W. Burggren.
Address for reprint requests and other correspondence: D. A. Crossley II, Dept. of Ecology and Evolutionary Biology, Univ. of California at Irvine, Irvine, CA 92697 (E-mail: dcrossle{at}uci.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
September 27, 2002;10.1152/ajpregu.00654.2001
Received 5 November 2001; accepted in final form 14 August 2002.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIAL AND METHODS
RESULTS
DISCUSSION
REFERENCES
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