AMERICAN
JOURNAL
OF PHYSIOLOGY
Vol. 217, No. 5, November, 1969. Pn'ntedin
Baroreceptor
U.S. A.
functions
in the fetal lamb
C. R. BRINKMAN
III,
C. LADNER,
P. WESTON,
AND
Department
of Obstetrics and Gynecology, and Department
of Physiology,
Los Angeles, California
90024
BRINKMAN,
C. R. III,
C. LADNER,
in the fetal
pulmonary
and systemic
iosus; umbilicoplacental
lamb.
blood flows
circulation
and pressures;
ductus
arter-
MORPHOLOGIC
STUDIES have demonstrated
conclusively
that the baroreceptor
nerves located in the carotid
sinus and aortic arch are fully developed
in the near-term
fetus, the functional
activities
of these nerves remain
a
debatable
question
(1, 3, 5, 22, 27). The rise in arterial
pressure and the bradycardia
that follow interruption
of the
umbilical
cord have been suggested
by some authors
as
reflecting
baroreceptor
reflex activities
(3, 7). Recent
evidence, however,
has demonstrated
that the blood pressure
rise is related
to elimination
of the low vascular
resistance
of the placental
circulation
and not necessarily
to baroreceptor
reflexes; the cause of the bradycardia
is not totally
clear (1).
In the newborn
rabbit
and human,
evidence
of baroreceptor
activities
has been presented
by various
authors
(4, 6, 13).
In the present
studies,
the carotid
sinus baroreceptor
functions
were investigated
in terms
of their
effects on
systemic
and pulmonary
hemodynamics
of the near-term
fetal lamb.
A mathematical
model used for computer
simulation
of fetal baroreceptor
activities
and for testing
the
validity
of certain
hypotheses
derived
from
the animal
experiments
has been submitted
for publication.
ALTHOUGH
MATERIAL
AND
Experiments
of 17 near-term
METHODS
were carried
out to completion
on a total
pregnant
ewes of mixed
breed and their
fetuses. The
ewe was given
spinal
anesthesia
and her
respiration
was assisted with compressed
air using a Byrd
respirator;
the fetus was unanesthetized.
Maternal
arterial
pressure
and blood
respiratory
gases were monitored
as
previously
described
(1, 2, 18). The fetus was delivered
and
marsupialized
to the uterine
walls to protect
the umbilical
circulation.
Breathing
was prevented
by placing
a salinefilled
glove
over the fetal head.
These
procedures,
the
details
of which
have been reported
previously
(1, 2, 20,
25), were performed
in all experiments.
Further
surgery was
carried
out according
to the following
two experimental
protocols.
Decreasing
Pressure in Intact
Carotid
Sinus
This experiment
was carried
out on eight fetal lambs as
follows:
polyethelene
catheters
were placed
in the fetal
abdominal
aorta via the femoral
artery
and in the main
umbilical
vein through
an intercotelydonary
branch.
These
catheters
served to monitor
the fetal arterial
and umbilical
vein pressures and their respective
blood gases and pH. The
fetal chest was entered
through
the fourth
left intercostal
space. The pericardium
was opened
and the ascending
aorta, ductus arteriosus,
and main pulmonary
artery were
exposed
by blunt
dissection.
The left phrenic
nerve was
severed to facilitate
exposure
of the ductus,
but the vagus
and sympathetic
nerves were left intact.
In separating
the
main
pulmonary
artery
from
the
ascending
aorta,
small
veins surrounded
by connective
tissues were cut and ligated.
Although
this ligation
might
have involved
some nerve
fibers, it probably
did not affect seriously
the innervation
of
the large vessels. Previous
studies (2, 23, 25) using the same
dissection
technique
have shown that the pulmonary
and
systemic
vascular
response to a variety
of stimuli
was not
altered.
Catheters
were inserted
into the main
pulmonary
artery and the left atrium
for measurements
of their respective pressures.
Balanced
field-electromagnetic
flow transducers (26) were placed around
the ascending
aorta or the
main pulmonary
artery and around
the ductus arteriosus
to
monitor
blood
flows in these vessels. In three additional
fetuses, total
umbilical
blood
flow was measured
with a
flow transducer
placed
around
the main
umbilical
vein.
The techniques
for the surgical procedures
and for recording
simultaneously
pressures and flows from these vascular
beds
have been reported
elsewhere
(1, 2, 18, 2 1, 23, 25).
Next, both carotid arteries were exposed proximal
to their
bifurcation
through
a midline
incision in the neck and were
freed from the vagus nerves which were kept intact.
One of
the carotids was ligated while pressures and flows were being
1346
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P. WESTON, AND N. S. ASSALI.
Am. J. Physiol.
217(5) :
1346-l 351.
1969.-The
influence
of carotid
sinus baroreceptor
functions
on systemic and pulmonary
circulations
was investigated
in near-term
unanesthetized
fetal lambs. Experimental
preparations used were intact carotid
sinus and isolated
carotid
sinus
pouch cross perfused
with maternal
arterial
blood. Decreasing
carotid sinus pressure resulted in a rise in systemic
and pulmonary
artery pressures
without
significant
changes in ascending
aortic
and main pulmonary
artery
flows;
ductus
arteriosus
flow decreased
consistently.
Increasing
pressure
in the carotid
sinus
pouch led to a fall in systemic arterial pressure.
These circulatory
alterations
are related to a baroreceptor
reflex action originating
in the carotid sinus. Neither
the chemoreceptors
nor the decrease
in carotid
conductance
played any role. The umbilicoplacental
circulation
must have taken a part in the rise in systemic vascular
resistance produced
by carotid occlusion,
even though the changes
in umbilical
vein flow and pressure were minor.
Baroreceptor functions
N. S. ASSALI
UCLA School of Medicine,
BARORECEPTORS
IN FETAL
LAMB
1347
Increasing
or Decreasing
Pressure in Carotid
Sinus Pouch
This procedure
was carried
out on the remaining
nine
animals.
The two carotid
arteries
and the trachea
were
exposed low in the neck through
a midline
incision.
The
trachea
was ligated
so that the saline-filled
glove used to
prevent
breathing
could be removed
to facilitate
the dissection. An oblique
incision
just below the angle of the jaw
was made and carried down to the area of the carotid
sinus
on the left side. To improve
exposure,
the angle of the
mandible
was resected and branches of the jugular
vein and
one carotid
artery were ligated.
Silver clips were placed on
the branches
of the other carotid
artery, except the internal
carotid.
This latter was cannulated
with a short piece of
polyethylene
tubing,
the tip of which was directed
toward
the sinus. The common
carotid
was ligated,
well below the
area of the sinus, and was catheterized
with a short polyethylene
tubing
directed
cephalad.
In this way, the carotid
sinus was isolated
and transformed
into a pouch with one
inlet and one outlet.
Both of these were connected
to pressure transducers
so that the pressure gradient
across the
sinus pouch could be monitored.
The pressure gradient
was
regulated
to the desired level with the use of thumb
screws
placed around the inlet and outlet tubings.
The inlet tubing
was then connected
to a catheter
which had been inserted
The outlet
previously
into the maternal
carotid
artery.
tubing
was connected
to a catheter
in the maternal
jugular
vein. This type of cross perfusion
provided
the fetal carotid
sinus pouch
with
a constant
circulation
with
a highly
oxygenated
maternal
blood. By manipulating
the thumbscrews on the inlet and outlet,
the perfusing
pressure in the
sinus was adjusted
to the level of the fetal arterial
pressure.
Continuous
heparinization
of the ewe was accomplished
with a Harvard
pump.
A control
period
(30-40
min) was first observed
during
which
the fetal carotid
sinus pouch
was perfused
with
maternal
blood but at the fetal arterial
pressure. Periods of
increasing
or decreasing
fetal pulsatile
carotid
sinus pressure
then followed
and were accomplished
by merely
releasing
or tightening
the thumbscrew
on the inlet tubing.
Each one
of these periods lasted 3-4 min. A recovery
period followed
during
which the pressure in the carotid
sinus pouch was
brought
back to fetal levels.
In some experiments,
the pulsation
of the perfusing
pressure of the carotid
sinus pouch was damped
by introducing
a large syringe
containing
saline and air into the
inflow tubing.
This procedure
attenuated
the pressure pulse
without
changing
its mean.
RESULTS
Efects
of Surgical
Procedure
and Ligation
of One Carotid
Artery
The effects of the surgical
procedure
on both mother
and
fetus were no different
from those observed
in other series
previously
reported
from these laboratories
(2, 20, 25). Fetal
pulmonary
and systemic
blood
flows and pressures
and
blood
respiratory
gases during
the control
period
were
within
the range of values previously
reported
(1, 2, 20, 23,
25).
Ligation
of one fetal carotid
artery with the other intact
had no appreciable
effect on fetal systemic
and pulmonary
artery pressures and on any of the blood flows that were
measured.
The mean pressure in the carotid
sinus on the
ligated
side averaged
35 mm Hg as compared
to an average
of 65 mm Hg in the descending
aorta. This finding
indicates
the presence of collateral
circulation.
Decreasing
Pressure in Intact
Carotid
Sinus
Efects on systemic circulation.
Partial
reduction
in carotid
sinus pressure through
50 % decrease in its blood flow rate
had insignificant
effects on fetal systemic
and pulmonary
circulations.
Profound
reduction
in sinus pressure through
total carotid
artery occlusion,
however,
elicited
a prompt
rise in fetal
systemic
arterial
pressure which lasted for the duration
of
the occlusion
(Fig. 1 and Table
1). Ascending
aortic flow
did not change appreciably
but ductus arteriosus
flow decreased consistently
(Table
1). Fetal effective cardiac output
(ascending
aortic + ductus flow) decreased
by an average
of 12 % mainly
because of the fall in ductus flow (Fig. 2).
Systemic
vascular
resistance
increased
significantly
during
carotid
occlusion
(Fig. 2).
Pressure in the carotid sinus of the ligated
artery decreased
by about 50 % from its control
values during
carotid
occlusion; this indicates
that even with cessation of flow in both
carotid
arteries,
the carotid
sinus of the fetal lamb
still
receives blood from other sources. Fetal heart rate did not
change appreciably
during
or after carotid
occlusion.
Efects on pulmonary
circulation.
Figure
3 shows the effects
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monitored
continuously.
A catheter
was passed through
the
distal end of this artery and served to measure
the pressure
in the carotid
sinus on the ligated
side. This procedure
served to test the existence
of collateral
circulation.
The
other main carotid
artery was fitted with an electromagnetic flow transducer.
A segment
of this artery distal to the
transducer,
well below the carotid
sinus, was placed in a
Blalock
clamp which served for graded carotid
occlusion.
The studies comprised
the following
three periods:
I) A
control
period lasting
3040
min during
which blood flows
and pressures were monitored
every 3-4 min while blood
respiratory
gases from mother
and fetus were analyzed
at
frequent
intervals.
2) A period
of carotid
occlusion
during
which the Blalock
clamp
was progressively
closed around
the artery until its blood flow, as monitored
with the flowmeter, reached
zero. The average duration
of total carotid
occlusion
was about
1 min.
Pressures and flows were recorded
continuously
during
and after the occlusion
for
about
lo-15
min.
Fetal
blood
respiratory
gases were
analyzed
once or twice during this time. Two to five episodes
of carotid
occlusion
were carried
out in each experiment.
3) A recovery
period
lasting
20-30 min during
which the
Blalock
clam p was released
and flows and pressures were
monitored
as in the control
period.
Flows and pressures were recorded
on an Offner Dynograph and Ampex
magnetic
tape recorder.
Blood respiratory gases in mother
and fetus were analyzed
by techniques
in current
use in our laboratories
(17, 18). Fetal effective
cardiac
output,
net pulmonary
blood flow, and systemic
and pulmonary
vascular
resistances
were computed
by
formulas
previously
described
(1, 2).
1348
BRINKMAN,
MATERNAL
ARTERIAL
PRESSURE
mmHg
PULMONARY
PRESSURE
mmHg
I25
EN”o”
. N
CAROTID
T
63
53
32
39
61
73
61
45
50
VEIN
50
AORTA
Flow r
ml/kg per
min
T
C
Flow,
ml/kg per
min
T
T
T
Mean
22
=tl
SE
69
57
38
43
62
81
69
47
68
73
1 115 1105
32
43
62
78
63
51
38
55
65
86
70
54
4
1
1
2
2
2
53 58 56
zt3 *3
*4
142
70
89
80
65
103
88
54
79
62
60
76
78
104
62 13 87
zJz4
zt4
73
&4
127 126
*7
*7
<O.OOl
91
198
152
165
78
200
152
158
161
*15
159
H8
>0.5
<O.Ol
>O.OOl
average of several readings
taken
Values
under C represent
those under T represent
average readprior to carotid occlusion;
ings taken at the peak response
to carotid
occlusion.
Mean & 1
SE of all experiments
is presented;
N = number of tests.
ARTERIOSUS
FLOW
ml/mln
+40
RELEASE
FIG. 1. Segment of a record illustrating
effects of total carotid occlusion on mean fetal arterial, pulmonary
artery, and umbilical vein
pressures, and mean blood flows in carotid artery, ascending aorta,
and ductus arteriosus.
Note slow increase in fetal arterial and pulmonary artery pressures on carotid occlusion and prompt return after
occlusion had been released.
of total carotid occlusion
on fetal pulmonary
hemodynamics.
Pulmonary
artery pressure increased
promptly
in a parallel
fashion to the increase in systemic
arterial
pressure (Fig. 3
and Table
1). Ductus
blood flow again decreased
as in the
previous
experiments,
while main
pulmonary
artery flow
remained
unchanged
(Table
1). The
pressure
gradient
across the ductus either
remained
the same or increased
slightly
during
carotid
occlusion.
Net pulmonary
blood
flow
(main
pulmonary
arteryductus
flow)
increased
slightly.
Effects on umbilical
circulation.
Umbilical
vein blood flow
and umbilical
vein pressure
did not change
significantly
during
carotid
occlusion.
Efects on blood respiratory gases. Carotid
occlusion
did not
alter the Paz, Pcoz, and pH of the blood in the umbilical
vein, abdominal
aorta, and the carotid
sinus of the ligated
side (Table 2).
Pressure in Carotid
r
+30-
I mm/set
or Decreasing
Aszo;$;g
ier
N ml/kg
min
C
<O.OOl
OCCLUSION
Increasing
ASSALI
Sinus Pouch
This series of experiments
yielded
variable
results largely
because of technical
difficulties
in the experimental
preparation.
In the first four experiments,
a rise in fetal arterial
pressure occurred
on increasing
the pressure in the carotid
sinus pouch
by perfusing
it with
maternal
blood.
This
+20-
1
PAP
-lO-
Dcp
(IDA
EC0
‘I
LJ-SW
-2o-3o-4oFIG. 2. Percent
change (mean Z!Z 1 SE) from control during carotid
occlusion of fetal arterial pressure (FAP), pulmonary
artery pressure
(PAP), distal carotid pressure (DCP), ductus arteriosus flow @DA),
effective cardiac output (ECO, algebraic sum of ascending aortic and
ductus arteriosus flows) and the systemic vascular resistance (SVR).
response was contrary
to what is expected
from this type of
stimulus.
Autopsy of these animals
revealed several branches
in the posterior
aspect of the carotid arterial
system that had
not been ligated.
The rise in pressure was then obviously
caused by overloading
the fetal circulation.
In two other experiments,
an attempt
was made to ligate
these posterior
branches,
but, in the dissection,
several of
the carotid
sinus nerves were destroyed.
In these animals,
no blood pressure response could be elicited
to either fall or
rise in sinus pressure. In the remaining
three animals,
most
of the carotid
artery branches
were ligated
with minimal
injury
to the sinus nerves. In these experiments,
a total of
10 tests of increasing
pressure and 10 of decreasing
pressure
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DUCTUS
AND
011
ARTERY
FLOW
ml /min
ASCENDING
FLOW
ml/mln
Ductus
Ax-F,yus
Aortic
Pressure,
mm Hg
C
ARTERY
0
UMBILICAL
PRESSURE
mm Hg
WESTON,
TABLE
I. Efects of carotid artery ocdusion on systemic and
pulmonary
artery pressures and on ductus, ascending aortic,
and main pulmonary artery Cpaws
FETAL
ARTERIAL
PRESSURE
mmHg
FETAL
LADNER,
BARORECEPTORS
DISTAL
CAROTID
PRESSURE
mmHg
FETAL
IN FETAL
LAMB
1349
DISCUSSION
ARTERY
ARTERIAL
PRESSURE
mm Hg
PULMONARY
PRESSURE
mmHg
ARTERY
FLOW
ml /min
130
0
RELEASE
OCCLUSION
3. Segment of a record illustrating
effects of total carotid
occlusion
on systemic
arterial and pulmonary
artery pressures on
ductus and main pulmonary
artery flows. Distal carotid artery pressure refers to that in sinus of ligated side. Note prompt increase in pulmonary and systemic pressures and decrease in ductus flow. Pressure
in carotid sinus of ligated side did not reach zero despite bilateral
carotid occlusion.
FIG.
2. Blood gas tensions and pH in umbilical
aorta and carotid sinus before and during carotid
TABLE
Period
Parameter
Umbilical
Vein
1
~~‘~~(&
I
vein, descending
occlusion
1 Carotid
Sinus
I
Control
Paz, mm Hg
Pco~, mm Hg
PH
45Zl.Z3
231k3
7.3111~0.05
25Zt3
30*3
7.26xtO.03
26&O .4
25Zt4
7.25rfiO.03
Carotid
occlusion
POZ, mm Hg
PCOZ, mm Hg
PH
44&4
201k3
7.3O~tO.03
27&l
24&3
7.26~tO.04
28&Z
319x4
7.27~~0.03
Values
are means rt SE.
in the carotid
sinus pouch was performed.
The results were
as follows:
control
fetal arterial
pressure
(mm
Hg) was
87 & 3 (SE) systolic and 63 I+ 1.5 diastolic;
during increasing
pressure, fetal arterial
pressure fell to an average of 83 =t 3
systolic and 60 =t 1 diastolic;
during
decreasing
pressure,
arterial
pressure rose to an average of 94 rt 2.5 systolic and
66 rt 1 diastolic.
Control
heart rate averaged
180 beats/min,
and decreased to an average of 148 during increasing
carotid
sinus pouch pressure;
during
lowering
of the pouch pressure, heart rate changed
inconsistently.
An example
of this
experiment
is illustrated
in Fig. 4. Since the maternal
blood
perfusing
the sinus pouch had a Pea of about 90 mm Hg,
the chemoreceptors
could not have been involved
in this
fetal blood pressure response.
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CAROTID
ARTERY
The classical response to a fall in carotid
sinus pressure
in the adult animal
is an increase in the arterial
pressure
and heart rate. These circulatory
changes
are related
to
enhanced
vasomotor
sympathetic
activities
brought
about
by decreased
baroreceptor
activities
of the carotid
sinus
nerves
(14). Increased
carotid
sinus pressure
yields
the
opposite results, namely
arteriolar
vasodilatation
and bradycardia ( 14).
The reports on the influence
of carotid sinus baroreceptors
on the cardiac
output
and pulmonary
circulation
are controversial
(8). Although
an increase
in the cardiac
output
has been observed
during
carotid
occlusion
in the nonanesthetized
animals
(12, 16, 24), the changes in pulmonary
vascular
resistance have been inconsistent
(10, 11). Difficulties in experimental
techniques
and in separating
the action
of the baroreceptors
from that of the chemoreceptors
might
have contributed
to the controversy.
The present
data indicate
that in the near-term
fetal
lamb the carotid sinus baroreceptors
are active. The prompt
rise or fall in systemic
arterial
pressure when the carotid
sinus pressure
was decreased
or increased
is definitely
related
to alterations
in the systemic
vascular
resistance
caused by a baroreceptor
reflex; surgical
destruction
of the
sinus nerves eliminated
the pressure response.
It could be argued
that the rise in fetal arterial
pressure
resulted
not from a baroreceptor
reflex but rather from a
decrease in conductance
of the systemic vascular bed caused
by total occlusion
of the carotid circuit.
This hypothesis
was
ruled
out with computer
simulation.
The results of this
simulation
show that decreasing
carotid
conductance
to
zero results in only 9 % increase in systemic vascular
resistance as compared
to 29 % observed
in the animal
experiments
(unpublished
observations).
This
estimation
is
rendered
more meaningful
by the fact that in the animal
experiment,
because of collateral
circulation,
carotid
conductance
never reached
zero even with bilateral
carotid
occlusion.
The site of the increased
vascular
resistance
during
fetal
carotid
occlusion
cannot
be determined
with
absolute
certainty.
On physiological
ground
and computer
simulation, the umbilicoplacental
circulatory
system must have
shared in the increase in systemic vascular
resistance,
since
its blood
flow rate amounts
to about
two-thirds
of the
effective
fetal cardiac
output
(1). On the other hand, the
umbilical
vessels are generally
thought
to be devoid of nerve
supply,
but Jacobsen
(15) has recently
demonstrated
the
existence of nerve fibers along the cotelydonary
vessels, and
the ductus venosus is known
to possess a rich supply
of
sympathetic
and parasympathetic
nerves (3, 19). So, although
the changes
in umbilical
vein pressure
and flow
during
carotid
occlusion
were minor,
alterations
in compliance or resistance
in the placental
vascular
bed must have
occurred
to permit
the observed increase in systemic arterial
pressure. These alterations
are probably
within
the error of
flow and pressure
measuring
methods,
and,
therefore,
cannot be detected
easily.
The presence of the umbilicoplacental
circuit
as a lowresistance
system in parallel
with the fetal systemic circuit
has a damping
effect on the pressor response
to carotid
occlusion.
This is demonstrated
by the smaller
fetal pressor
1350
FiTAL
AR7-,-LR/AL
CAROUD
1Omm
S/AUS
PREssI/RE
Pf.TRf-USING
PRESSURf
/set
10 mm/mln
0 L-
CONTROL
LOW
INCREASED
PRESSURE
PRESSURE
RECOVERY
pressure during perfusion at low pressure,
when perfusing pressure was increased.
and fall in fetal pressure
response when compared
to that of adult
animals.
Also,
computer
simulation
has shown that the increase in blood
pressure
and systemic
vascular
resistance
in response
to
carotid
occlusion
is significantly
greater
after eliminating
the umbilicoplacental
circulation
(unpublished
observations).
Further
evidence
of the damping
effects of the
placenta
is provided
by the smaller
response
of the fetal
circulation
to vasoactive
substances;
the fetus requires
10-l 5 times the adult dose per kilogram
of body weight of
any vasoactive
substance to elicit the same degree of arterial
pressure response
(1, 23). We believe
that this damped
circulatory
response
might
have been responsible
for the
reports that have denied the existence of fetal baroreceptor
activities.
The increase
in pulmonary
artery pressure observed
in
the fetal lamb during
carotid
occlusion
is similar
in magnitude and pattern
to that of the systemic arterial
pressure. It
is unlikely
that the changes
in pulmonary
circulation
are
due to a specific
response
to carotid
sinus baroreceptor
activities.
They are probably
secondary
to the changes in
systemic circulation
transmitted
through
the ductus arteriosus.
Of interest
is the consistent
diminution
of blood
flow
through
the ductus arteriosus
that occurred
during
carotid
occlusion.
This decrease cannot be caused by alteration
in
any of the three major
factors that control
ductus circulation, namely,
the POT of the fetal blood, the pressure gradient
across the ductus, and the right ventricular
output,
since all
of these factors remained
practically
unchanged.
The decrease, however,
could be due to either an alteration
in the
asynchronic
ejection
of the two ventricles
(1, 2 1) or to an
active reflex constriction
stimulated
by the carotid occlusion.
Whatever
its cause, the decrease in ductus flow was responsible for the slight fall in effective fetal cardiac output,
since
left ventricular
output
as reflected
by ascending
aortic
flow was not altered
by carotid
occlusion.
The absence of tachycardia
represents
another
difference
between
fetal and adult
baroreceptor
response to carotid
occlusion.
Although
the, exact reason for the lack of chronotropic
action
is obscure,
it is possible
that,
because the
heart rate of the fetal lamb
is between
160 and 200 under
normal
conditions,
the control
mechanisms
responsible
for
cardioacceleration
are nearly “saturated.”
This hypothesis
receives support
from the fact that, when the carotid
sinus
pressure was increased,
bradycardia
occurred
along with
the hypotension.
Further
evidence
of this concept
is provided
by the fact that the fetal heart responds
with deceleration
to a variety
of stimuli
which in the adult cause
cardioacceleration.
This study was supported
by National Heart Institute
Grant HE
01755, and National Institute for Child Health and Human Development Training Grant 5 Tl HD 38-07.
C. R, Brinkman
III,
C. Ladner,
and P. Weston
were United
States Public Health Trainees in Reproductive
Physiology.
Received
for publication
10 February
1969.
REFERENCES
II. The Fetus and Neonate.
Academic,
1968, p. 51-142.
ASSALI,N. S., T. H. KIRSCHBAUM, AND P. V. DILTS, JR. Effects of
hyperbaric
oxygen on uteroplacental
and fetal circulation.
Circulation Res. 22 : 573-588, 1968.
BARCROFT, J. Researches on Prenatal Life. Oxford : Blackwell,
1945.
BLOOR, C. M. Aortic baroreceptor
threshold
and sensitivity
in
rabbits at different ages. J. Physiol., London 174 : 163-l 7 1, 1964.
BOYD, J. D. The inferior aortico-pulmonary
glomus. Brit. Med.
Bull. 17: 127-131, 1961.
BRADY, J. P., AND W. H. TOOLEY. Cardiovascular
and respiratory reflexes in the newborn.
Pediat. Clin. North Am. 13 : 801-82 1,
1966.
CALDEYRO BARCIA, R., J. J. POSEIRO, C. NEGREIROS DE PAIVA,
C. GOMEZ ROGERS, A. FAGWDES LATHAM, M. A. ZAMBTANA, A.
ARELLANOHERNANDEZ,G.BEAUGUIS,
P. PENA ORTEZ, F. AGIJERO
New
2.
3.
4.
5.
6.
7.
AND
W. FILLER, JR. Effects of abnormal uterine conon a human fetus. Bibliotheca Paediat. 81: 267-295, 1963.
CORCONDILAS, A., D. E. DONALD, AND J. SHEPHERD. Assessment
by two independent
methods of the role of cardiac output in the
pressor response to carotid occlusion.
J. Physiol., London 170:
250-262, 1964.
CROSS,
K. W., AND J. L. MALCOLM. Evidence of carotid body and
sinus activity in new-born
and foetal animals. Proc. Physiol. Sot.
4-5: 10-11 P, 1952.
DALY, M., AND C. P. LUCK. The effects of carotid sinus baroreceptor reflexes on pulmonary
arterial pressure and pulmonary
blood flow in dog. J. Physiol., London 143 : 343-368, 1958.
DALY, I., AND M. DALY. The effects of stimulation
of the carotid
body chemoreceptors
on the pulmonary
vascular bed in the dog:
the vasosensory
controlled
perfused living animal preparation.
J. Physiol., London 148: 201-219, 1959.
LUGONES,
1. A~SALI, N. S. Biology of Gestation. Vol.
tractions
York:
8.
9.
10.
11.
Downloaded from http://ajplegacy.physiology.org/ by 10.220.33.4 on June 18, 2017
4. Segment of a record illustrating
effects of cross perfusing a
fetal carotid sinus pouch with maternal blood at low and high pressures. Note overall increase in fetal systemic
(particularly
systolic)
FIG.
BARORECEPTORS
IN
FETAL
LAMB
20. LUCAS, W., T. KIRSCHBAUM, AND N. S. ASSALI. Cephalic circulation and oxygen consumption
before and after birth. Am. J.
Physiol. 2 10’: 287-292, 1966.
21. MORRIS, J. A., G. A. BEKEY, N. S. ASSALI, AND R. BECK. Dynamics
of blood flow in the ductus arteriosus. Am. J. Physiol. 208: 471476, 1965.
of chemoreceptor
22. PURVES, M. J., AND T. J. BISCOE. -Development
activity. Bit. Med. Bull. 22: 56-60, 1966.
23. SMITH, R. W., J. A. MORRIS, AND N. S. ASSALI. Effects of chemical
mediators of the pulmonary
and ductus arteriosus circulation
in
the fetal lamb. Am. J. Obstet. Gynecol. 89: 252-260, 1964.
24. TUCKMAN, J., S. R. SLATER, AND M. MENDLOWITZ. The carotid
sinus reflexes. Am. Hear-t J. 70: 119-l 35, 1965.
25. VAUGHN, D., T. H. KIRSCHBAUM, T. BERSENTES, AND N. S. A~SALI.
Effects of autonomic blockade on pulmonary
and systemic circulation before and after birth. Am. J. Physiol. 2 12 : 436-443, 1967.
26. WESTERSTEN, A., E. RICE, C. BRINKMAN, AND N. S. ALKALI. A
balanced field-type
electromagnetic
flowmeter.
J. A&@. Physiol.
26: 497-500, 1969.
In: Handbook of
27. YOUNG, M. The fetal and neonatal circulation.
Physiology. Circulation. Washington,
D.C. : Am. Physiol.
Sot.,
1963, sect. 2, vol. II, chapt. 46, p. 1619-1650.
Downloaded from http://ajplegacy.physiology.org/ by 10.220.33.4 on June 18, 2017
12. DELAUNOIS, A. L., AND P. J. BERNARD. Cardiac output during
carotid sinus reflexes. In : Baroreceptors and Hypertension, edited by
P. Kezdi. New York : Pergamon, l967, p. 181~185.
13. DOWNING, S. E. Baroreceptor
reflexes in newborn
rabbits.
J.
Physiol., London 150: 201-2 13, 1960.
14. HEYMANS, C., AND E. NEIL. Reflexogenic Areas of the Cardiovascular
System. London : Churchill,
1958.
innervation
of
15. JACOBSON, H. N., AND F. K. CHAPLER. Intrinsic
the human placenta. Nature 214: 103-104, 1967.
sinus
16. KENNEY, R. A., E. NEIL, AND A. SCHWEITZER. Carotid
reflexes and cardiac output in dogs. J. Physiol., London 114: 27-40,
1951.
N. SHAPIRO, AND N. S.
17. KIRSCHBAUM, T. H., J. C. DEHAVEN,
A~SALI. Oxyhemoglobin
dissociation characteristics
of human and
sheep maternal and fetal blood. Am. J. Obstet. Gynecol. 96: 741759, 1966.
AND N. S.
18. KIRSCHBAUM, T. H., W. E. LUCAS, J. C. DEHAVEN,
ASSALI. The dynamics of placental oxygen transfer. Am, J. Obstet.
Gynecol. 98: 429-443, 1967.
19. LIND, J., L. STERN, AND C. WEGELIUS. Human Foetal and Neonatal
Circulation. Springfield,
Ill. : Thomas,
1964.
1351