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Vol. 83, Issue 6, 2048-2054, December 1997
Departments of Medicine and Surgery, University of Wisconsin, and Middleton Memorial Veterans Hospital, Madison, Wisconsin 53706
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Katragadda, Srinivas, Ailiang Xie, Dominic Puleo, James B. Skatrud, and Barbara J. Morgan. Neural mechanism of the pressor
response to obstructive and nonobstructive apnea. J. Appl. Physiol. 83(6): 2048-2054, 1997.
Obstructive and nonobstructive apneas elicit
substantial increases in muscle sympathetic nerve activity and arterial
pressure. The time course of change in these variables suggests a
causal relationship; however, mechanical influences, such as release of
negative intrathoracic pressure and reinflation of the lungs, are
potential contributors to the arterial pressure rise. To test the
hypothesis that apnea-induced pressor responses are neurally mediated,
we measured arterial pressure (photoelectric plethysmography), muscle
sympathetic nerve activity (peroneal microneurography), arterial
O2 saturation (pulse oximeter),
and end-tidal CO2 tension (gas
analyzer) during sustained Mueller maneuvers, intermittent Mueller
maneuvers, and simple breath holds in six healthy humans before,
during, and after ganglionic blockade with trimethaphan (3-4
mg/min, titrated to produce complete disappearance of sympathetic
bursts from the neurogram). Ganglionic blockade abolished the pressor
responses to sustained and intermittent Mueller maneuvers (
4 ± 1 vs. +15 ± 3 and 0 ± 2 vs. +15 ± 5 mmHg) and breath
holds (0 ± 3 vs. +11 ± 3, all
P < 0.05). We conclude that the
acute pressor response to obstructive and nonobstructive voluntary
apnea is sympathetically mediated.
sympathetic nervous system; arterial pressure; obstructive sleep
apnea
INTRODUCTION SUSTAINED APNEA, with
and without intrathoracic pressure
change, causes an increase in arterial pressure that is coincident with
resumption of breathing. This apnea-induced pressor response is
preceded by an increase in sympathetic outflow to skeletal muscle; however,
a causal relationship between sympathetic activation and arterial pressure elevation has not been demonstrated in humans. Mechanical influences, such as release of highly negative intrathoracic pressure, may play a role in raising arterial pressure via
redistribution of blood volume. On the other hand, several lines of
evidence suggest that neural mechanisms are more important than
mechanical mechanisms in causing the pressor response to apnea.
O'Donnell and co-workers (10) showed that increases in arterial
pressure produced by experimental airway occlusion in sleeping dogs are abolished by autonomic blockade. The importance of chemoreflex stimulation was demonstrated in studies where supplemental
O2 greatly attenuated
apnea-induced increases in sympathetic vasoconstrictor outflow and
arterial pressure during voluntary apneas in awake subjects and during
episodes of sleep apnea (4, 5, 9, 17). Previous work from our
laboratory indicates that chemoreflex stimulation is more important
than negative intrathoracic pressure in causing apnea-induced
sympathetic activation and arterial pressure elevation during
wakefulness (9). In that study, peak increases in sympathetic outflow
and arterial pressure were comparable in obstructive and nonobstructive
apneas of the same duration.
The purpose of the present study was to test the hypothesis that
pressor responses to obstructive and nonobstructive apnea are neurally
mediated. Accordingly, we studied the hemodynamic responses to Mueller
maneuvers and breath holds during wakefulness in healthy subjects
before, during, and after reversible pharmacological blockade of the
autonomic nervous system.
METHODS Four women and two men, aged 21 ± 3 (SD) yr, served
as subjects. All subjects were normotensive and free from
cardiovascular, pulmonary, and neurological disease as evaluated by
history and physical examination. All subjects provided informed
consent, and the experimental protocol was approved by the University
of Wisconsin Health Sciences Human Subjects Committee.
-motoneuron or mechanoreceptor activity caused by
unintentional leg movements were excluded from analysis. For purposes
of quantification, muscle sympathetic nerve activity was expressed as
minute activity (bursts/min × mean burst amplitude) in arbitrary
units.
Sustained and intermittent Mueller maneuvers.
The subject breathed through a mouthpiece that was attached to a
two-way valve. After stable respiration, arterial pressure, and heart
rate were observed for at least 1 min, the subject paused momentarily
at end expiration while the valve on the mouthpiece assembly was closed
to occlude the airway. The subject then generated 40 mmHg of
pressure (measured at the mouth) and maintained this level of negative
pressure for 20 s. A visual display of mouth pressure was provided to
assist the subject in maintaining the required level of pressure. The
subject was instructed to exhale immediately after the opening of the
valve at the end of the Mueller maneuver so that an end-tidal sample
could be acquired for CO2 analysis. To perform intermittent Mueller maneuvers, the subject made
brief, repetitive inspiratory efforts (1-3 s in duration) against
the closed valve every 5 s for a total of 20 s.
Breath holds.
The subject breathed through the mouthpiece and valve described in
General procedures. After a stable
baseline was achieved, the subject stopped breathing at end expiration
for 20 s. At the end of the breath hold, the subject was instructed to
exhale so that an end-tidal sample could be acquired for
CO2 analysis.
Experimental protocol.
Each subject underwent several practice trials of each of the breathing
maneuvers before data collection began. During the data-collection
period the subjects performed breath holds, sustained Mueller
maneuvers, and intermittent Mueller maneuvers in duplicate or
triplicate before, during, and after intravenous infusion of trimethaphan (3-4 mg/min). The presence and absence of ganglionic blockade were confirmed by the presence and absence, respectively, of
bursts of postganglionic sympathetic activity on the peroneal neurogram. Postdrug measurements were made at least 20 min after discontinuation of the trimethaphan infusion.
Data analysis.
Five-second averages of mean arterial pressure (
pulse
pressure + diastolic pressure), muscle sympathetic nerve activity
(bursts/min × mean burst amplitude), and heart rate during
sustained Mueller maneuvers and breath holds were computed. The change
in arterial pressure, heart rate, and tidal volume caused by the apnea
was determined by calculating the difference between the peak value
observed after the apnea and the mean of the preapnea control period.
The change in muscle sympathetic nerve activity was determined by
expressing the mean minute activity observed in each 5-s period during
apnea as a percentage of the preapnea baseline. Differences in these
variables before, during, and after ganglionic blockade were compared
by repeated-measures analyses of variance with Newman-Keuls post hoc
tests (23). Peak changes in these variables caused by intermittent Mueller maneuvers were computed and compared in the same manner. To
determine the equivalency of chemical stimuli produced by Mueller maneuvers and breath holds in the intact and ganglionically blocked conditions, changes in arterial O2
saturation and end-tidal CO2 tension were compared by repeated-measures analyses of variance. P < 0.05 was considered
statistically significant. Unless otherwise noted, values are means ± SE.
RESULTS
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) in mean arterial pressure
(A) and heart rate
(B) during and after sustained
Mueller maneuvers in intact condition and during ganglionic blockade.
In the absence of ganglionic blockade, breath holds caused a progressive increase in arterial pressure (Figs. 4 and 5, Table 1). This increase was abolished by ganglionic blockade. Muscle sympathetic nerve activity increased to 809% of the baseline value during breath hold in the intact condition. During ganglionic blockade, muscle sympathetic nerve activity was absent at rest, and no increase was elicited by breath hold. In the unblocked condition, heart rate decreased by an average of 1 beat/min during the breath hold (Fig. 5, Table 1). During ganglionic blockade, heart rate increased 4 beats/min.
Mueller maneuvers and breath holds produced equivalent chemical stimuli and similar increases in tidal volume in the intact and ganglionically blocked conditions (Table 1). After discontinuation of the trimethaphan infusion, the neurocirculatory responses to both types of apnea were restored (Table 1). Effects of intermittent Mueller maneuvers on mean arterial pressure with and without ganglionic blockade. In the intact condition, each period of negative intrathoracic pressure caused a small decrease in arterial pressure, but there was an overall increase in arterial pressure over the duration of the 20-s apneic period (Fig. 6). Ganglionic blockade abolished the overall increase in arterial pressure but not the intermittent decrease that accompanied each inspiratory effort (Fig. 6, Table 1).
DISCUSSION
To investigate the relative contributions of neural and mechanical influences on the arterial pressure fluctuations caused by obstructive and nonobstructive apneas, we studied neurocirculatory responses to Mueller maneuvers and breath holds in healthy subjects before, during, and after pharmacological blockade of the autonomic nervous system. Our findings point to a major role for sympathetic activation in causing apnea-induced arterial pressure elevations, at least during wakefulness. In contrast, mechanical influences, such as negative intrathoracic pressure, appear to have little, if any, independent effect on the arterial pressure rise that follows apnea.
Critique of methods. A limitation of this study is that we recorded sympathetic discharge only in postganglionic neurons that innervate vascular structures in leg muscle. During trimethaphan infusion in our experiments, no muscle sympathetic nerve activity was detectable on the peroneal neurogram under resting conditions and none was elicited by apneas. Although this discharge is representative of sympathetic outflow to skeletal muscle vascular beds elsewhere in the body (11), our measurements do not allow inferences about the effects of trimethaphan on neural outflow to other organs and vascular beds. However, because trimethaphan abolished the pressor response to apnea, it is likely that the drug, in the doses we used, provided nearly complete blockade at all sympathetic ganglia. We are less confident that trimethaphan caused complete blockade at parasympathetic ganglia. In our subjects, heart rate increased with breath holds during ganglionic blockade and decreased during breath holds in the intact condition. Our interpretation of these findings is that the predominant effect of apnea on heart rate in the intact condition was a decrease that occurred because baroreceptors were stimulated by a rise in blood pressure. In the blocked condition, no baroreceptor stimulation occurred (blood pressure did not rise) and a less powerful mechanism that produced parasympathetic withdrawal was unmasked. These findings suggest that parasympathetic control of sinus node activity was at least partially intact in our ganglionic blockade experiments and that the dose of trimethaphan we used was not sufficient to produce complete autonomic blockade. This inability to confirm complete autonomic blockade would have complicated the interpretation of our data if we had seen only small attenuations of the apnea-induced pressor response during trimethaphan infusion; however, ganglionic blockade completely abolished this pressor response in our subjects. Therefore, the inability to demonstrate complete parasympathetic blockade should not limit our interpretation of the findings. We assume that trimethaphan had no effect on chemoreceptor function. In the present study our only means of testing this assumption was to examine the ventilatory responses following termination of apneas. Ventilation and tidal volume increased after apneas under control conditions and during ganglionic blockade. This finding indicates that the ventilatory control system remained responsive to apneic events during ganglionic blockade. However, in three of six subjects the ventilatory responses following apnea were smaller in the blocked than in the intact state, perhaps because of removal of the mild, modulatory influence of sympathetic activity on carotid body function (2). We cannot determine whether these decreased responses to voluntary apnea in the awake state represent altered chemoreceptor function or the overriding effects of behavioral inputs, which can be highly variable (16). Potential mechanical influences on arterial pressure during and after apnea. The role of mechanical influences in causing the pressor response following an obstructive apnea has been a matter of controversy. Although the negative intrathoracic pressures generated during inspiration temporarily augment venous return by increasing the pressure gradient between the extrathoracic veins and the right atrium (7), increasingly negative pressures may actually limit venous return by collapsing the great veins at their point of entry into the thorax (14). Previous studies in experimental animals have shown that negative intrathoracic pressure, produced by inspiratory loading or airway occlusion, causes a decrease in stroke volume that is thought to be caused by alterations in preload and afterload (13, 14, 19). A similar decrease in stroke volume has been observed during obstructive sleep apnea in humans (3, 18, 20). Thus it is possible that the release of negative intrathoracic pressure at apnea termination could, via removal of this constraint on cardiac output, result in a pressor response of purely mechanical origin. The present data do not support this concept. In our ganglionically blocked subjects, arterial pressure, which had fallen during the Mueller maneuver, returned slowly to the control level on release of the inspiratory strain. We did not observe the characteristic overshoot in arterial pressure that normally occurs after voluntary Mueller maneuvers and obstructive apneas during sleep. We considered the possibility that repetitive inspiratory efforts, similar to those that occur during episodes of obstructive sleep apnea, might have a cumulative mechanical effect on arterial pressure. However, in our ganglionic blockade experiments, brief repetitive Mueller maneuvers also failed to produce an overshoot in arterial pressure (Fig. 6, Table 1). Taken together, these findings suggest that mechanical factors play no independent role in causing the pressor response to apnea. Neural mechanism of the pressor response to apnea. The present findings, which are consistent with the previous observation that hexamethonium prevents the pressor response to airway obstruction in sleeping dogs (10), suggest that during apnea an increase in sympathetic vasoconstrictor outflow raises arterial pressure via increased peripheral vascular resistance. However, because trimethaphan blocks transmission at parasympathetic as well as sympathetic ganglia, we also considered the possibility that parasympathetic withdrawal contributed to the rise in arterial pressure via heart rate acceleration and increased cardiac output. Previous investigators demonstrated that atropine blunts the arterial pressure fluctuations associated with apneas in patients with central and obstructive sleep apnea (15). Arousal-induced tachycardia has been shown to augment the pressor response to obstructive apnea in sleeping dogs (10). In contrast, the pressor response to the Mueller maneuver is unaffected by vagotomy in anesthetized dogs (13). We consider it unlikely that a parasympathetically mediated increase in cardiac output contributed importantly to the apnea-induced pressor response in our subjects for several reasons. First, the pressor response to breath hold was accompanied by a decline in heart rate (1 beat/min), and the pressor response to Mueller maneuvers was
accompanied by an increase in heart rate (+5-6 beats/min). Even if
combined with a sympathetically mediated increase in myocardial contractility and stroke volume, it is unlikely that such a small increase in heart rate could raise cardiac output. This concept is
supported by the previous clinical finding that cardiac output does not
increase after obstructive apneas in patients with sleep apnea
syndrome. In these patients, postapneic tachycardia is accompanied by a
reduction in stroke volume (3, 18). Second, in one subject in whom
incomplete parasympathetic blockade was suspected even though
trimethaphan caused complete disappearance of sympathetic activity from
the neurogram, heart rate increased by an average of 19 beats/min
during Mueller maneuvers. Despite this more substantial increase in
heart rate, arterial pressure did not rise. Most importantly, the
apnea-induced increases in heart rate were as large or even larger in
the blocked than in the intact condition; nevertheless, the pressor
responses to breath holds and Mueller maneuvers were completely
abolished during trimethaphan infusion. These findings strongly suggest
that sympathetic activation is the primary cause of the arterial
pressure rise that accompanies apnea through an increase in peripheral
vascular resistance and/or an increase in myocardial
contractility.
What is the trigger for sympathetic activation during apnea? Our
previous work and that of other investigators point to chemoreflex stimulation as a key feature of this neural response (4, 9, 22). In all
these previous studies the pressor response to apnea was greatly
attenuated by administration of supplemental
O2. These observations of
experimental apneas during wakefulness are in good agreement with
clinical observations of obstructive apneas during sleep (5, 17);
however, we recognize that voluntary apneas performed during
wakefulness fail to reproduce all the respiratory and neurocirculatory
disturbances that occur during sleep. Most importantly, these maneuvers
fail to reproduce the effect of sleep state. Many aspects of
cardiovascular regulation are known to vary with sleep state (6), and
the arousal that occurs at the termination of sleep apneas is likely to
contribute importantly to the pressor response, in an additive or a
synergistic manner (12).
In conclusion, the pressor response to obstructive and nonobstructive
apneas in awake humans is mediated by the autonomic nervous system,
because it is abolished by ganglionic blockade. Our data indicate that
this arterial pressure rise is caused by sympathetically mediated
increases in peripheral vascular resistance and/or
sympathetically mediated increases in stroke volume. In contrast,
parasympathetically mediated increases in cardiac output do not play an
important role in causing this pressor response, because heart rate
responses to apnea were unaffected by ganglionic blockade. We further
conclude that the mechanical influence of highly negative intrathoracic
pressure has little or no independent effect on the acute pressor
response to voluntary apnea.
ACKNOWLEDGEMENTS
The authors thank Patricia Mecum for secretarial assistance.
FOOTNOTES
Address for reprint requests: B. J. Morgan, Dept. of Surgery, 1300 University Ave., 5175 MSC, Madison, WI 53706-1532.
Received 20 May 1997; accepted in final form 15 August 1997.
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