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1 Hebrew Rehabilitation Center for Aged Research and Training Institute, 2 Beth Israel/Deaconess Medical Center Department of Medicine, and 3 Harvard Medical School, Boston, Massachusetts 02131; and 4 Bikur Cholim Hospital, Jerusalem, 91004 Israel
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Lipsitz, Lewis A., Raymond Morin, Margaret Gagnon, Dan
Kiely, and Aharon Medina. Vasomotor instability preceding
tilt-induced syncope: does respiration play a role? J. Appl. Physiol. 83(2): 383-390, 1997.
This study
aimed to determine whether alterations in cardiovascular dynamics
before syncope are related to changes in spontaneous respiration.
Fifty-two healthy subjects underwent continuous heart rate (HR),
arterial blood pressure (BP), and respiratory measurements during
10-min periods of spontaneous and paced breathing (0.25 Hz) in the
supine and 60° head-up tilt positions. Data were evaluated by power
spectrum and transfer function analyses. During tilt, 27 subjects
developed syncope or presyncope and 25 remained asymptomatic. Subjects
with tilt-induced syncope had significantly greater increases in
low-frequency (0.04-0.15 Hz) systolic BP, diastolic BP, and HR
power during tilt than the asymptomatic subjects
(P 
0.01). This difference was
present during spontaneous but not paced breathing. However, average
tidal volume, respiratory rate, minute ventilation, proportion of
breaths below 0.15 Hz, and low-frequency respiratory power during tilt did not differ between syncopal and nonsyncopal subjects. Transfer magnitudes between low-frequency respiration and BP, and between BP and
interbeat interval, were also similar between groups. Thus vasomotor
instability before syncope is not related to alterations in respiration
or the cardiovagal baroreflex but may reflect oscillating central
sympathetic outflow to the vasculature.
Mayer waves; power spectral analysis; neurally mediated; arterial
pressure; heart rate; variability; dynamics
INTRODUCTION NEURALLY MEDIATED SYNCOPE is a common and potentially
dangerous abnormality in blood pressure (BP) regulation that often can be provoked in healthy individuals by the orthostatic stress of head-up
tilt (13). We and others have observed high-amplitude low-frequency
heart rate (HR) (13, 27) and arterial BP (Mayer wave) (11, 29)
oscillations preceding the onset of neurally mediated syncope. These
observations suggest that alterations in beat-to-beat HR and arterial
BP dynamics may be indicative of maladaptive arterial BP control
mechanisms that predispose people to syncope.
Low-frequency Mayer wave and HR oscillations (centered at 0.1 Hz) are
thought to represent baroreflex-feedback control of vasomotor activity
or cardiac chronotropy, respectively (2). However, there may be several
mechanisms capable of producing these oscillations, none of which is
currently well understood. For example, respiratory cycles can
influence low-frequency arterial BP and cardiac interval (R-R)
fluctuations (9, 12, 19).
Many years ago, several investigators observed that subjects frequently
yawned, sighed, and hyperventilated before the development of neurally
mediated syncope (5, 8, 31). In 1968, Epstein and colleagues (5)
observed phasic oscillations in arterial BP at a frequency of 4-9
oscillations/min before the development of syncope during head-up
tilt. Furthermore, they demonstrated that the amplitude of
these oscillations could be enhanced by increasing the depth of
respiration. Therefore, we asked whether arterial BP Mayer wave
oscillations during upright tilt are affected by controlled breathing
in subjects who subsequently develop syncope and whether alterations in
vasomotor control in these subjects may be related to changes in
spontaneous respiration. If vasomotor instability before syncope were
related to abnormal respiratory cycles, specific breathing exercises
might be designed to avert syncope in susceptible patients.
METHODS
) [respiratory rate × average tidal volume
(VT)] was calculated
during 3 min of spontaneous breathing during supine rest and was
subsequently held constant during periods of paced breathing by having
the subject adjust his or her depth of respiratory excursion according
to a marker on an oscilloscope screen. During paced breathing,
respiratory frequency was controlled by having subjects follow a
tape-recorded auditory signal and line on the oscilloscope screen.
Experimental protocol.
After equipment hook up and calibration, subjects rested supine for 30 min to reach equilibrium. Continuous ECG, BP, and respiratory data were
then collected during 30 min of supine rest, and 45 min of 60°
head-up tilt. During a 10-min supine period, and between minutes 5 and
15 after the initiation of tilt,
subjects were instructed to breathe at a fixed rate of 15 breaths/min
(0.25 Hz), as described above. While they were in the upright position,
subjects were carefully observed and questioned for signs and symptoms
such as dizziness, nausea, sweating, other discomfort, yawning, or near
syncope. If subjects became symptomatic or hypotensive (SBP <80 mmHg)
during tilt, they were returned immediately to the supine position.
Data processing.
All data were digitized at 250 Hz and displayed in real time by using
commercially available data acquisition software (Windaq, Dataq
Instruments, Akron, OH) on a personal computer. Continuous ECG and BP
data recorded before and during tilt were visually inspected and edited
offline for artifact and ectopy, with the use of an automated program
to detect arrhythmias. Eight-minute segments of stationary data
(without trends or abrupt changes in the mean over time) during paced
and spontaneous breathing in the supine and tilted positions were used
for analysis. Data segments obtained during the tilt were analyzed from
the initial 5-15 min while subjects were performing paced
breathing and from 15-25 min while they were breathing
spontaneously. Because 13 subjects developed syncope
before the spontaneous breathing segment could be obtained, and 5 fainted before completion of paced breathing, their data were not
available for the tilt component of the analysis. All data segments
used in the analysis for syncopal subjects were obtained while the
subjects were asymptomatic, at least 1 min before the onset of
symptoms.
Beat-to-beat R-R intervals were determined from the R-wave of the ECG,
and SBP and diastolic BP (DBP) were derived from the maximum and
minimum of the arterial BP waveform. HR was calculated as the
reciprocal of the R-R interval (in s), multiplied by 60. The means ± SD for R-R interval, HR, SBP, and DBP were calculated from the
beat-to-beat values averaged over 30 s. Each R-R interval, HR, SBP,
DBP, and respiratory time series was resampled at 2 Hz to obtain
equidistant time intervals. The resampled series were analyzed by using
a fast Fourier transform algorithm as previously described (18). The
areas under the power spectra in the Mayer wave and respiratory
frequencies (defined as 0.04-0.15 and 0.15-0.50 Hz,
respectively) were integrated and used for statistical comparisons.
Data analysis.
Baseline characteristics of the two groups of subjects were compared by
using analysis of covariance (ANCOVA) and Student's t-tests. Supine and tilt
cardiovascular variables and spectral powers were compared between the
groups by using two different methods to handle missing data. The first
was a two-way repeated-measures ANCOVA (to examine group and time
effects), removing those subjects with incomplete data. The second
analysis employed an unbalanced repeated-measures model with structured
covariance matrixes (proc mixed; see Ref. 24) that is useful in
unbalanced repeated-measures experiments in which there are missing
observations. Because both methods yielded the same results, only the
proc-mixed analysis is reported. All spectral data were natural log
transformed to normalize their distributions and were adjusted for age
effects. Data are expressed as untransformed means ± SE.
The respiratory time series was further analyzed by computing
histograms of breathing frequencies (breaths/min) and
VT (ml) for each subject during
upright tilt. The means of these distributions were compared between
groups of subjects using Student's
t-tests. We also compared
(average frequency × volume) and the
percentage of breaths below 0.15 Hz.
To identify a possible linear relation, and the strength of that
relation between respiratory (input signal) and arterial BP (output
signal) fluctuations and between arterial BP (input) and R-R interval
(output) fluctuations in the low-frequency range (0.04-0.15 Hz)
during upright tilt, we calculated the coherence and transfer
magnitudes between the signals by using the technique of Saul et al.
(25). All analyses were performed with DaDisp software on a personal
computer. Coherence was calculated from the cross spectra and
autospectra of the time series, according to the formula
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RESULTS
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Power spectral analysis of spontaneous breathing segments of the study showed that both symptomatic and asymptomatic subjects had similar low-frequency (0.04-0.15 Hz) SBP and DBP power in the supine position, and increased both systolic and diastolic power significantly during tilt (P = 0.0001, time effect for both pressures; Figs. 2 and 3). However, subjects with subsequent syncope had significantly greater increases in low-frequency systolic and diastolic power during tilt than the asymptomatic subjects (P = 0.01, time by group interaction, Figs. 2 and 3). This difference was not present during the paced breathing segments of the study.
High-frequency (0.15-0.50 Hz) SBP and DBP power also increased significantly during tilt (P = 0.0001), but only the diastolic power response was significantly greater in syncopal subjects than asymptomatic subjects (P = 0.04). Again, this difference was not seen during paced breathing (Figs. 2 and 3). R-R and HR dynamics. Low-frequency R-R interval power was unchanged during tilt, whereas high-frequency power decreased significantly (P = 0.0001) in both the symptomatic and asymptomatic groups of healthy subjects (Fig. 4). There were no differences in responses between the two groups of subjects. In contrast, low-frequency HR power increased to a significantly greater extent in syncopal subjects than in asymptomatic subjects (P = 0.008; Fig. 5). There were no differences in high-frequency HR power.
During paced breathing, both high-frequency R-R interval (Fig. 4) and HR (Fig. 5) power decreased in response to tilt (P = 0.0001 for both). There was no difference in responses between the two groups. Low-frequency R-R and HR powers during paced breathing were unchanged by tilt in both groups. Respiratory dynamics. As shown in Table 1, average VT, respiratory rate, and
during tilt did not differ
significantly between symptomatic and asymptomatic subjects.
Furthermore, the proportion of breaths in the low-frequency range
<0.15 Hz (Table 1) and both low- and high-frequency respiratory power
under all conditions were similar between these two groups of subjects.
Low- and high-frequency respiratory power during spontaneous breathing
increased to a similar extent in response to tilt in subjects with and
without syncope (Fig. 6). There was no
relationship between the change in SBP power and change in respiratory
power for either group of subjects.
Paced breathing at 0.25 Hz reduced low-frequency respiratory power (P = 0.0001) and increased high-frequency power (P = 0.0001) for both groups, but it did not distinguish symptomatic from asymptomatic subjects. Potential influence of respiration on arterial BP dynamics. Although respiratory dynamics were similar between groups, it was possible that high-amplitude low-frequency breaths had a greater influence on arterial BP in syncopal than in nonsyncopal subjects. Therefore, we examined the transfer functions between respiration and SBP in subjects with and without syncope during tilt (Table 2). Eight-minute segments of artifact-free tilt data were available from 21 healthy nonfainters and 14 healthy fainters.
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DISCUSSION
There are three principal findings from this study. 1) Healthy individuals who develop neurally mediated syncope during head-up tilt demonstrate exaggerated low-frequency arterial BP and HR oscillations before the onset of syncope while they are still asymptomatic. 2) Although the difference in these oscillations between syncopal and nonsyncopal subjects disappears during paced breathing, the oscillations do not appear to be related to respiration. 3) The oscillations are not associated with alterations in the cardiovagal baroreflex. What is the origin of these low-frequency oscillations and their physiological significance?
Rhythmic fluctuations of systemic arterial BP were described as early
as 1733 by the physiologist Stephen Hales (6). Subsequent investigators, including Traube in 1865 (30) and Hering in 1869 (7),
attributed these "blood pressure waves" to respiration. In 1876, Sigmund Mayer (17) described in rabbits spontaneous low-frequency
arterial BP waves that were independent of the respiratory rhythm.
Since that time, there has been considerable controversy over the
origin of low-frequency arterial BP oscillations. This controversy has
been fueled in part by differences in nomenclature and oscillation
period for the pressure waves, different stimuli used to evoke them,
and the different animal models used to study them. Proposed mechanisms
are of two types: 1) phasic feedback loops from peripheral baro- or chemoreceptors to brainstem centers that
produce oscillating sympathetic output to the vasculature and
2) a central rhythm generator that
operates independently of phasic feedback (22). High-amplitude arterial
BP oscillations with a frequency between 0.04 and 0.15 Hz can be
generated in mammals by hypotensive hemorrhage (22), coronary artery
occlusion (14), upright posture (4, 21), and intravenous nitroglycerin infusion (21), suggesting that they represent the vasomotor response to
sympathoexcitation. This notion is supported by the fact that this
response can be prevented by bilateral stellectomy (21), peripheral
-adrenergic blockade with phentolamine mesylate (22), or sympathetic
vasomotor blockade by epidural anesthesia (26).
Respiration also modulates HR and arterial BP (9, 19). Periodic breathing caused by congestive heart failure, sleep apnea, and high-altitude exposure has been shown to influence low-frequency HR oscillations (12). The attenuation of Mayer wave oscillations in healthy syncopal subjects during paced breathing at 0.25 Hz suggested to us that low-frequency respiratory cycles before syncope might be responsible for the vasomotor fluctuations we observed. However, after comparison of respiratory rates, VT, spectral powers, and respiratory-to-arterial BP transfer magnitudes in fainters and nonfainters, this did not appear to be the case. The damping effect of paced breathing on low-frequency arterial BP oscillations may have been due to partial entrainment of arterial BP rhythms at the higher breathing frequencies (9) or to suppression of sympathetic activity by the relaxation response. Alternatively, it is possible that enhanced Mayer wave amplitude occurs only at a time more proximal to syncope and, therefore, was not present during the initial phase of tilt when paced breathing was performed. We did not randomize the order of paced and spontaneous breathing because we wanted to maximize the chance of acquiring controlled breathing data during tilt, before subjects became symptomatic. If subsequent studies confirm that paced breathing not only reduces vasomotor instability but also prevents the development of syncope, paced breathing may prove to be a useful intervention in otherwise healthy individuals who are at risk of fainting during prolonged standing.
We also explored the possibility that an exaggerated Mayer wave response to tilt represented impaired cardiovagal baroreflex buffering of arterial BP. To investigate the cardiovagal baroreflex, we examined the transfer magnitudes between SBP and R-R intervals and found that they did not differ between healthy subjects with and without symptoms during tilt. This analysis implies a causal direction of change from low-frequency arterial BP to R-R interval. Although it is possible that a causal change can occur in the opposite direction, the analysis was limited to the tilted position, which increases low-frequency arterial BP variability, even when R-R interval variability is eliminated by cardiac pacing (28). The negative phase relation between these signals also supports the notion that arterial BP led R-R interval changes.
It is notable that the analysis of R-R variability yielded different results depending on whether HR or interbeat interval was used as the unit of measure. R-R interval is linearly related to cardiac vagal outflow, whereas HR is inversely related to R-R interval and reflects minute-to-minute systemic hemodynamic adjustments to physiological stimuli (1, 10). The finding that R-R interval variability during tilt did not differ between symptomatic and asymptomatic subjects, but that HR variability did, suggests that vasomotor instability in the syncopal subjects was probably not related to alterations in cardiovagal activity preceding syncope but was related to abnormalities in hemodynamic control of the circulation. Hemodynamic alterations that would predispose healthy subjects to syncope include inadequate cardiac output or systemic vascular resistance during upright tilt. A recent study (20), showing large-amplitude, low-frequency arterial BP oscillations when cardiac output was held constant by computer control of cardiac rate, suggests that our findings probably reflect beat-to-beat changes in systemic vascular resistance rather than cardiac output.
If Mayer waves indeed reflect sympathetic outflow to the vasculature, then a heightened sympathetic response to tilt might be the cause or effect of hemodynamic changes associated with syncope. One possible physiological explanation for our findings is that an excessive reduction in venous return during tilt in subjects prone to syncope resulted in heightened sympathetic activity, vigorous contraction of a relatively empty cardiac ventricle, stimulation of afferent vagal C fibers in the ventricular wall, and subsequent provocation of the Bezold-Jarisch reflex (16). This is consistent with the observation that Mayer wave oscillations increased before the onset of hypotension and bradycardia. Unfortunately, we were unable to measure venous return or stroke volume in the present study.
Limitations. There are several limitations to the present study. As discussed above, we did not randomize the sequence of paced and spontaneous breathing data collection periods during upright tilt. Therefore, we cannot be certain that lower Mayer wave amplitude during paced breathing was not due to a temporal effect. However, this limitation would not affect the principal analysis of respiratory dynamics during periods of spontaneous breathing when Mayer wave amplitude was heightened. Also, this study did not examine hemodynamic changes associated with syncope. Instead, we focused specifically on the role of respiration and the cardiovagal baroreflex on beat-to-beat cardiovascular dynamics. Additional studies are needed to examine potential relationships between beat-to-beat changes in stroke volume or systemic vascular resistance and arterial BP in both health and disease. The number of syncopal subjects with complete data during upright tilt was relatively small, because syncope occurred before data collection could be completed. This attrition of subjects decreased the power of the study to detect differences in respiration and may have biased the study by removing those with the most maladaptive response to tilt. Nevertheless, the symptomatic subjects who remained in the sample still demonstrated exaggerated Mayer wave oscillations during tilt, without a corresponding increase in the number or amplitude of low-frequency respiratory cycles. Therefore, we believe our findings are valid. Finally, it is unlikely that high-amplitude Mayer wave oscillations are a fixed characteristic of syncope-prone subjects and thus could be used for diagnostic purposes. Both the occurrence of these oscillations and the syncopal response to tilt are highly variable within individuals. However, their coincident relationship suggests that the emergence of highly periodic BP rhythms may be indicative of an unstable physiological control network that predisposes individuals to circulatory collapse. Similar cyclic variations in vasomotor activity are seen in other conditions leading to cardiovascular decompensation such as hemorrhage (15), sinoaortic denervation (3), and myocardial ischemia (14).ACKNOWLEDGEMENTS
The authors are grateful to Roberta Rosenberg for assistance with subject recruitment, Dr. J. Andrew Taylor for his insightful suggestions, and Dr. Adrienne Cupples for help with the statistical analysis.
FOOTNOTES
Address for reprint requests: L. A. Lipsitz, Hebrew Rehabilitation Center for Aged, 1200 Centre St., Boston, MA 02131 (E-mail: Lipsitz{at}Mail.HRCA.Harvard.edu).
Received 16 December 1996; accepted in final form 31 March 1997.
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L. A. Lipsitz, J. Hayano, S. Sakata, A. Okada, and R. J. Morin Complex Demodulation of Cardiorespiratory Dynamics Preceding Vasovagal Syncope Circulation, September 8, 1998; 98(10): 977 - 983. [Abstract] [Full Text] [PDF]
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 R. Zhang, J. H. Zuckerman, and B. D. Levine Deterioration of cerebral autoregulation during orthostatic stress: insights from the frequency domain J Appl Physiol, September 1, 1998; 85(3): 1113 - 1122. [Abstract] [Full Text] [PDF]
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