Download Reflex Hemodynamic Responses Initiated from the Thoracic Aorta

Reflex Hemodynamic Responses Initiated from the Thoracic Aorta
By Franco Lioy, Alberto Malliani, Massimo Pagani, Giorgio Recordati, and Peter J. Schwartz
ABSTRACT
In anesthetized vagotomized cats with both carotid arteries occluded, stretch of the
walls of the thoracic aorta performed without obstructing aortic blood flow induced
reflex increases in arterial blood pressure (systolic: 136 ± 4 [SE] to 170 ± 7 mm Hg),
heart rate (230 ± 10 to 236 ± 1 1 beats/min), and maximum rate of rise of left ventricular
pressure (dP/dt max) (2,337 ± 256 to 3,155 ± 302 mm Hg/sec). In cats with spinal transection (C ( ), similar increases were observed. These responses were abolished by infiltrating the walls of the thoracic aorta with xylocaine. In adrenalectomized cats with intact central nervous systems, reflex responses were reduced but were still statistically significant. Phenoxybenzamine abolished the pressor response but not the increases in heart
rate and dP/dt max. Propranolol drastically reduced the increases in heart rate and dP/dt
max but not the pressor response. It is concluded that stretch of the thoracic aorta induced an increase in sympathetic activity affecting the heart, the peripheral vessels, and,
probably, the adrenal glands through a spinal reflex.
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KEY WORDS
dP/dt max
spinal cardiovascular reflexes
adrenal glands
vagotomy
• Experimental evidence for spinal reflex mechanisms contributing to the neural control of circulation has been progressively growing (1-8). A definitive resolution of this debated question (9, 10)
would result from identifying the cardiovascular
receptors projecting to the spinal cord, the stimuli
capable of affecting the receptors, the afferent and
efferent nervous pathways, and the cardiovascular functions which represent the target of the reflexes.
So far it has been proven that: (1) some cardiacsympathetic sensory endings are sensitive to specific hemodynamic events (6, 11), (2) natural
hemodynamic stimuli in spinal vagotomized preparations reflexly modify the electrical discharge of
sympathetic efferent fibers (6, 7), and (3) electrical
or chemical stimulation of afferent cardiac sympathetic fibers produces reflex cardiovascular responses (12-14). It remains to be demonstrated
that cardiovascular reflex responses can be induced
by mechanical stimuli in spinal preparations. In our
previous work on cardiocardiac reflexes (5, 6,
13-15), we could not find a mechanical stimulus
that acted on the heart without directly affecting
From the Istituto Ricerche Cardiovascolari, Universitii di
Milano, Centro Ricerche Cardiovascolari CNR, 20122 Milano,
Italy.
Dr. Lioy was a Research Scholar, Canadian Heart Foundation, and CNR Visiting Professor, on leave from the Department
of Physiology, University of British Columbia, Vancouver 8,
B.C., Canada.
Please address reprint requests to Dr. A. Malliani, Istituto
Ricerche Cardiovascolari, Via F. Sforza 35, 20122 Milano, Italy.
Received August 6, 1973. Accepted for publication October
25, 1973.
78
heart rate
arterial blood pressure
phenoxybenzamine
propranolol
carotid occlusion
cats
cardiac function. However, a recent observation
that numerous sympathetic sensory endings can be
functionally identified in the walls of the thoracic
aorta (unpublished observations) seems to offer a
possible solution to this problem. Therefore, we
decided to stimulate these vascular endings mechanically to ascertain whether such a stimulus
would produce reflex hemodynamic responses.
This procedure demonstrated that a stretch of the
thoracic aorta which did not interfere with aortic
blood flow induced significant increases in arterial
blood pressure, heart rate, and maximum rate of
rise of left ventricular pressure (dP/dt max) in
spinal vagotomized cats or vagotomized cats with
intact central nervous systems.
Methods
Nineteen cats were anesthetized with chloralose and
urethane (60 and 250 mg/kg, respectively, ip). In two
cats sodium pentobarbital (35 mg/kg, ip) was used. The
cervical vagi were cut, and then a carotid artery and a
femoral artery were cannulated with short, wide-bore
polyethylene catheters. After injection of a paralyzing
dose of gallamine triethiodide, positive-pressure respiration was initiated using a Harvard respirator connected to a tracheal cannula. The respirator was adjusted to maintain arterial gases and pH (measured on an
Astrup model RM 1304 blood acid-base analyzer) within
physiological limits. The guidelines of the American
Physiological Society regarding anesthetized, curarized
animals were observed.
In five cats the spinal cord was sectioned at Cx. In
another five cats hydrocortisone (20 nig, iv) was administered, and the adrenal glands were removed
through an abdominal midline laparotomy. Additional
hydrocortisone (30 mg/hour) was then administered
during the experiment by slow intravenous infusion.
Circulation Research, Vol. XXXIV, January 1974
79
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All cats were placed on their right side, and the left
hemithorax was widely opened from the fourth to the
tenth rib. A special cannula was used to stretch the walls
of the thoracic aorta without obstructing aortic blood
flow. It consisted of a stainless steel tube surrounded by
a thin rubber cylinder which could be inflated via
another small metal tube mounted perpendicular to the
tube close to one end of the cannula. The cat was heparinized (3 mg/kg), and, after clamping the aorta caudal
to the left subclavian artery, the vessel was completely
divided and the cannula inserted. Cannulas of different
dimensions (5-7 cm long, 3-5 mm, i.d.) were selected according to the cat's size so that they fit snugly into the
vessel. The two cut ends of the aorta were ligated
around the lower end of the cannula, the side tube passing out between them. The cannulation procedure took
between 1.5 and 2 minutes. The pressure drop across the
cannula measured by comparing the carotid and femoral
arterial mean pressures was between 5 and 15 mm Hg.
When the balloon was inflated the aortic walls were
stretched between the seventh and the tenth intercostal
arteries. The pericardium was opened, and a short (7
cm) no. 7 cardiac catheter was introduced into the left
ventricle via the left auricle and mitral valve.
Recorded Variables.—Arterial pressures were measured with Statham P23De strain gauges. The cathetermanometer systems had a flat ( ± 5 % ) frequency
response of 30 Hz as calculated by their responses to
step increases in pressure (16). Left ventricular pressure
was measured with a Statham P23De strain gauge connected to a specially built, high-frequency d-c operational bridge amplifier that was linear (-3 db) up to 15
kHz. The measured flat (±5%) frequency response of
the left ventricular catheter-manometer system was 60
Hz, and the phase lag was linear up to 110 Hz. The left
ventricular pressure signal was fed into an analog
differentiator which was linear up to 160 Hz. An
amplified record of left ventricular end-diastolic pressure was obtained using a Grass 7DAC driver amplifier.
We also recorded the electrocardiogram (ECG),
using a Grass 7P511 preamplifier, the heart rate, using a
Grass 7P4C tachograph, and the respiratory movements,
transduced by a crystal capsule connected to the side
arm of the tracheal cannula. These variables and the
blood pressures were registered on a multichannel inkwriting Grass P7 polygraph and simultaneously fed into
a Hewlett-Packard 3907C tape recorder. Five of these
variables could also be photographed by a Grass C4
camera from a Tektronix 565 oscilloscope.
Data were collected only from cats that had a systolic
blood pressure (carotid artery) above 100 mm Hg. Heart
rate was measured from the ECG for each group of ten
cardiac cycles during one control period (30-60 seconds) and during 30-60 seconds of stimulation (stretch
of the aortic walls). As a check on the validity of the
measurements of left ventricular dP/dt max, carotid and
left ventricular pressures along with dP/dt were displayed at fast speed on the oscilloscope to establish that
dP/dt max was always reached during the isovolumic
phase of ventricular contraction.
The control values and the maximum changes induced in each variable by stretch of the aortic walls
were averaged for each cat, and the resulting values
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LIOY, MALUANI, PAGANI, RECORDATI, SCHWARTZ
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were used to compute the means ± SE presented in the
tables.
Results
Cats with Intact Central Nervous Systems.—In
eight vagotomized cats with both their common
carotid arteries occluded, stretch of the walls of
the thoracic aorta induced marked increases in
systolic, diastolic, and pulse arterial pressures, left
ventricular systolic pressure, and dP/dt max. Heart
rate increased only a few beats per minute, and left
ventricular end-diastolic pressure increased by less
than 1 mm Hg. All these changes were statistically
significant (Table 1). Figure 1A shows one of these
experiments: blood pressures, left ventricular dP/
dt max, and heart rate rose soon after inflation of
the balloon and remained elevated throughout the
period of stimulation. These hemodynamic effects
were not due to obstruction of the thoracic aortic
blood flow caused by the experimental maneuver,
since a parallel pressure increase was observed
both above and below the cannula. In several experiments, as in the one presented in Figure 1A, a
second late increase in blood pressure was
recorded after the initial rise. When the balloon
was deflated, aU variables decreased toward control levels, which were reached after different
periods of time (30-230 seconds).
These cardiovascular responses were much less
evident if one common carotid artery was not oc-
eluded, thus allowing the full operation of that
baroreceptive area.
Cats with Spinal Section.—In six vagotomized
cats with their spinal cord sectioned at C,, the aortic stretch produced similar circulatory responses
(Table 1). Figure 2 shows one of these experiments.
All variables returned to control 30-120 seconds
after cessation of the stimulus.
Reflex Nature of the Response.—In four cats
with intact central nervous systems and in one with
spinal section, 1% xylocaine was infiltrated under
the adventitia of that portion of the thoracic aorta
which was stretched by the balloon. Table 2 shows
the very significant reduction or abolition of all of
the responses to aortic stretch induced by this procedure. The small decrease in dP/dt max shown in
Table 2 was not due to the stimulus; it probably
resulted from some absorption of the anesthetic
into the bloodstream. After administration of xylocaine, however, the cat's reactivity was still perfectly preserved, as shown by the cardiovascular
responses to a strong nociceptive stimulus (clamping of the paw). Light nociceptive stimuli did not
elicit cardiovascular responses because of the level
of anesthesia. These experiments showed that the
effects of aortic stretch were initiated from receptors located in the aortic walls.
Peripheral Mechanisms of the Reflex Responses.—To assess the contributions of cardiac
and peripheral vascular mechanisms to the
responses elicited by aortic stretch, adrenergic
blockade and cardiac denervation were carried out
in some cats.
Propranolol (l mg/kg, iv) was injected over a
period of 30 minutes in four cats with intact central
nervous systems. Left ventricular dP/dt max and
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FIGURE 1
Effects of stretching the thoracic aorta in a vagotomized cat
with an intact central nervous system and both common carotid
arteries occluded. CAP - carotid artery pressure (recorded
proximal to the point of occlusion), FAP —femoral artery pressure, LVP - left ventricular pressure (all in mm tig), LV dP/
dt — rate of change of left ventricular pressure (mm Hglsec),
and HR — heart rate (beats/min). On the left of each section are
fast-speed records of each variable. The aortic stretch in this
and following figures is indicated by a bar. A: Control: B: After
administration of propranolol (1 mg/kg, iv).
HR
FIGURE 2
30..C
Effects of stretching the thoracic aorta in a vagotomized cat
with spinal section (Ci). Abbreviations are the same as they are
in Figure 1. A: Control. B: After administration of phenoxybenzamine hydrochloride (5 mg/kg, iv).
Circulation Research, Vol. XXXIV, January 1974
81
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heart rate were decreased by the drug. Aortic
stretch induced a smaller but clear increase in arterial and left ventricular pressures; heart rate remained constant, and left ventricular dP/dt max increased only very slightly and slowly during the
period of stimulation (Fig. IB).
After slow intravenous injection of phenoxybenzamine hydrochloride (5 mg/kg) in four spinal
cats, the increase in systolic pressure induced by
aortic stretch was drastically reduced; arterial
diastolic pressure was somewhat decreased, and
pulse pressure was increased. There were slight
decreases in left ventricular end-diastolic pressure.
The response of dP/dt max was not significantly
altered, but heart rate increased much more than it
did in the control period (Table 2). The cardiac
effects (heart rate, dP/dt max) of the aortic stretch
were prolonged and continued after cessation of
the stimulus (Fig. 2B).
Sympathetic denervation of the heart was performed in some cats by cutting the cardiac nerves
or by bilateral stellectomy. Although the cardiac
effects of aortic stretch were reduced, they could
not be abolished by denervation. Since the residual
effects could have been mediated by a reflex increase in catecholamine output from the adrenal
glands, the experiments were repeated in a group
of adrenalectomized cats.
Adrenalectomized Cats.—After removal of the
adrenal glands, the aortic stretch still induced all
the described cardiovascular effects in five cats
with intact central nervous systems (Table 1). The
magnitude of the responses was smaller than it was
in the cats with adrenal glands, although the
difference was statistically significant only for the
arterial pressure effects. The maximum changes
were observed soon after the onset of the stimulus,
and the late rise in blood pressure was never seen
in this group of cats (Fig. 3). Moreover, when the
balloon was deflated, all variables returned to control levels after short periods of time (4-15 seconds).
In two of these cats, section of the left inferior
cardiac nerve and the pericoronary nerve completely abolished the cardiac effects of the stimulation. It is therefore very likely that in cats with
adrenal glands the residual cardiac effects of aortic
stretch after cardiac denervation are due to a reflex
increase in the adrenal output of catecholamines.
Effect of an Afterload Increase on Left
Ventricular dP/dt max. —In six cats, an increase in
systolic arterial pressure comparable to that
elicited by aortic wall distention was induced by
82
LIOY, MALLIANI, PAGANI, RECORDATI, SCHWARTZ
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FIGURE 3
Effects of stretching the thoracic aorta in an adrenalectomized
vagotomized cat with an intact central nervous system and both
common carotid arteries occluded. Abbreviations are the same
as they are in Figure 1.
partially obstructing the aorta with a tourniquet.
The average percent rise in dP/dt max obtained in
this way (+12%) was much smaller than that induced by aortic stretch (+32%). This difference
was statistically significant (P < 0.05V
Effect of Different Anesthetics.—The reflex
effects obtained in two cats anesthetized with
sodium pentobarbital (one with an intact central
nervous system and one with spinal cord section)
were similar to those obtained in the other cats
anesthetized with the chloralose-urethane mixture.
Adequacy of the Stimulus. — All the cardiovascular responses that have been described
were clearly evident with stretches that increased
aortic diameter, measured with a precision caliper
at the point of maximum distention, only 10%. This
change in aortic radius was of the same magnitude
as that observed when the mean pressure of the
thoracic aorta was mechanically increased (aortic
stenosis) 50-60 mm Hg. A similar extensibility of
the aortic walls has been reported in the dog (17).
The stimulus we used was therefore comparable to
changes that can be observed in physiological
situations.
Discussion
A mechanical stretch of the walls of the thoracic
aorta induced significant increases in systemic arterial blood pressure, heart rate, and left ventricular dP/dt max. These cardiovascular responses
were not due to some direct interference with aortic blood flow caused by the experimental
maneuver; they represented neurally mediated
phenomena, since they all disappeared after infiltration of the aortic walls with a local anesthetic.
The same responses were present in spinal preparations, and, therefore, the integration of the
reflex appears to take place in the spinal cord. It is
probable that supraspinal baroreceptive mechanisms exert an inhibitory influence on these reflex
responses, because the effects of aortic stretch
were greatly attenuated unless both common
carotid arteries were occluded in vagotomized cats
with intact brains.
Gruhzit et al. (18) have observed that a rise in
aortic pressure, produced in dogs by intravenous
injection of epinephrine, induces a reflex hind-limb
vasodilatation initiated by receptors which are probably located in the thoracic aorta and mediated
by spinal afferent pathways. It is difficult to compare their results with ours because of the
differences in the stimuli and the preparations.
Furthermore, the fact that we always observed a
rise in arterial blood pressure does not rule out the
possibility that some vasodilatation occurred in
some vascular territories.
Alpha-receptor blockade suppressed the rise in
blood pressures induced by the aortic stretch but
not the increase in heart rate and left ventricular
dP/dt max. Actually a much larger increase in
heart rate was observed after administration
of phenoxybenzamine. This increase probably resulted from inhibition of norepinephrine reuptake or interference with catecholamine metabolism by the drug (19), which would result in greater
availability of adrenergic transmitter for betastimulating effects. The decrease in arterial
diastolic pressure observed under these conditions
was presumably due to some beta-adrenergic (20)
or sympathetic cholinergic (21) vasodilatation induced by the stimulus. Thus, the experiments with
alpha-receptor blockade showed that the blood
pressure increase was mainly due to peripheral
vasoconstriction and that the rise in dP/dt max was
largely independent of the increase in afterload
and could actually occur even when aortic diastolic
pressure decreased during stimulation (Fig. 2B).
The modest influence of increases in afterload on
dP/dt max was further proven by comparing the
effects of similar rises in aortic pressure during
Circulation Research. Vol. XXXIV. January 1974
83
HEMODYNAMIC RESPONSES TO AORTIC STRETCH
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reflex responses and during mechanical constriction of the aorta (see Results).
The administration of a beta-receptor blocking
agent did not affect the increases in blood pressure
but completely abolished the tachycardia and
drastically reduced the increase in dP/dt max. The
very small residual effect on dP/dt max probably
depended mostly, if not exclusively, on the rise in
afterload (22, 23).
The validity of left ventricular dP/dt max as an
index of myocardial contractility was supported in
these experiments by the fact that its maximum
value was always attained before the opening of
the semilunar valves (23). However, before assuming that the increase in dP/dt max was the result of
an increase in sympathetic discharge to the heart,
other factors should be ruled out, i.e., changes in
afterload, preload, heart rate, and circulating catecholamines (13, 22, 23). The role of afterload has
already been discussed. The influence of changes in
preload on dP/dt max (23) must have been
minimum, since left ventricular end-diastolic
pressure remained practically constant during aortic stretch. It also seems unlikely that the rise in dP/
dt max resulted primarily from a staircase
phenomenon (23) caused by the simultaneously
elicited tachycardia, because heart rate only increased a few beats per minute even though dP/
dt max increased much more substantially (in average 30% over control values).
Another point that should be discussed is the
contribution of the adrenal glands to the observed
cardiovascular responses. On purely theoretical
grounds, an increase in afferent nervous activity involving several spinal segments (T7-Ti0) in part corresponding to those from which the splanchnic
nerves originate should reflexly stimulate adrenal
secretion. This supposition was supported by the
fact that the cardiac effects of aortic stretch could
not be completely suppressed by cardiac denervation. This last observation contrasts with results
found when cardiovascular responses are elicited
through afferent cardiac sympathetic fibers projecting to higher segments of the spinal cord (13,
14). However, the persistence of all the reflex
responses in adrenalectomized cats proved that
they were only partly due to increased cateeholamine output from the adrenal glands. As predicted, in these cats cardiac denervation completely abolished the reflex increases in heart rate
and dP/dt max.
In conclusion, our experiments indicate the existence of spinal cardiovascular reflexes initiated by
Circulation Research. VoL XXXIV, January 1974
mechanical stimuli acting on vascular sensory endings. We are not suggesting that the thoracic aorta
represents another reflexogenic area in the classical sense: on the contrary, it is likely that nervous
control of circulation is obtained through a variety
of neural circuits (1, 3, 4) and that spinal reflexes
represent diffuse, elementary mechanisms. The
spinal reflex discussed in the present paper appears
to operate by a positive feedback mechanism: a
stimulus likely to duplicate the effects of an increase in aortic blood pressure produces a further
increase in blood pressure, heart rate, and dP/dt
max. Thus, the conception that nervous control of
the circulation is exerted exclusively through negative feedback mechanisms seems to be in conflict
with some of the experimental evidence.
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Circulation Research, Vol. XXXIV, January 1974
Reflex Hemodynamic Responses Initiated from the Thoracic Aorta
FRANCO LIOY, ALBERTO MALLIANI, MASSIMO PAGANI, GIORGIO RECORDATI and
PETER J. SCHWARTZ
Downloaded from http://circres.ahajournals.org/ by guest on May 7, 2017
Circ Res. 1974;34:78-84
doi: 10.1161/01.RES.34.1.78
Circulation Research is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
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