(Hypertension. 1999;34:1060-1065.)
© 1999 American Heart Association, Inc.
Scientific Contributions |
Respiratory Systolic Pressure Variability During Atrial Fibrillation and Sinus Rhythm
From the Institute of Cardiology, University of Bari (M.V.P., C.F., C.B., A.F., P.R.), Bari, Italy; the Division of Cardiology, "Salvatore Maugeri" Foundation, IRCCS, Rehabilitation Institute of Cassano Murge (F. Massari, F. Mastropasqua), Bari, Italy; and Bioengineering Service, "Salvatore Maugeri" Foundation IRCCS, Veruno Medical Centre (R.C.), Veruno, Italy.
Correspondence to Maria Vittoria Pitzalis, MD, PhD, FESC, Institute of Cardiology, University of Bari, Piazza Giulio Cesare 11, 70124 Bari, Italy. E-mail pitzalis{at}tin.it
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Abstract |
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Abstract—Previous studies have found that respiratory variations of ventricular response in atrial fibrillation are infrequent and inconsistent. This asynchrony between heart rate and respiration may characterize the physiological mechanisms coupling heart rate and systolic blood pressure oscillations in the respiratory band. The aim of this study was to evaluate whether synchronous variations in systolic blood pressure and respiration depend on a simultaneous change in heart rate. Univariate and bivariate spectral analyses were made of the R-R interval, systolic blood pressure, and respiratory signals during controlled respiration (16 breaths/min) in 24 patients with atrial fibrillation before and after efficacious electrical cardioversion and in 24 age- and sex-matched control subjects. During atrial fibrillation, the spectral coherence between respiration and heart rate was low (0.18±0.03), but there was a high level of coherence between respiration and systolic blood pressure (0.67±0.05). After cardioversion, the coherence between respiration and heart rate increased to 0.86±0.04, whereas the geometric mean values of the concomitant respiratory systolic blood pressure oscillations decreased by 72% (from 21.1 to 5.9 mm Hg2, P<0.001), which was similar to that observed in the control group (5.7 mm Hg2). These results confirm the inconsistent effect of respiration on heart rate response during atrial fibrillation and demonstrate that respiratory sinus arrhythmia is not a prerequisite for systolic blood pressure oscillations but may play an antioscillatory role in respiratory systolic blood pressure variability, which is probably mediated by arterial baroreflex mechanisms.
Key Words: arrhythmia • blood pressure • heart rate
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Introduction |
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The clinical hallmark of atrial fibrillation (AF) is an irregular ventricular rhythm. Few studies have investigated the respiratory oscillations of ventricular rhythm during AF,1 2 3 and only 24 5 have made use of spectral analysis. These last 2 studies reported the presence of respiratory arrhythmia during AF in a small percentage of patients, but none measured respiration as a factor of analysis.
The mechanisms underlying the origin of respiratory sinus arrhythmia (RSA) are still debated, but 2 main and not mutually exclusive theories have been put forward: One considers it to be the effect of cycling respiratory stimulation on arterial baroreceptors (the "peripheral" theory), and the other emphasizes the direct role of central respiratory drive (the "central" theory). Bivariate spectral analyses may quantify the relations between the heart period (R-R interval) and systolic blood pressure (SBP) but do not build causality between 2 signals: The spontaneous relation between the R-R interval and SBP fluctuations is a closed loop, and cross-spectral analysis is unable to separate the mechanical R-R–SBP feedforward by baroreflex feedback from SBP to R-R.6 A number of methods7 8 9 10 11 and models12 13 14 15 for exploring the fundamental relations between R-R and SBP oscillations in the respiratory band have been suggested, but their results are conflicting.
Random ventricular rhythm during AF may represent a unique model for investigating the origin of RSA because the absence of respiratory-related oscillations in ventricular rhythm may make it possible to characterize respiratory-related SBP oscillations. Furthermore, comparison of respiratory-related oscillations in SBP before and after the restoration of sinus rhythm may make it possible to understand whether or not the variations in blood pressure synchronous with respiration depend on simultaneous changes in heart rate.
The aim of this study was to establish the relations between cardiorespiratory signals during AF and after the restoration of sinus rhythm. In particular, we considered 2 complementary questions (1) Does respiration have consistent effects on ventricular rhythm during AF; and (2) if not, does the magnitude of respiratory-related SBP oscillations during AF change after cardioversion to sinus rhythm?
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Methods |
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Study Patients
The study population consisted of 24 patients (14 men and 10 women; mean age 54±8 years; range 36 to 68 years) hospitalized for elective electrical cardioversion of AF. The median time since the diagnosis of AF was 60±456 days (range 27 to 2190). Patients with intraventricular conduction disturbances, sick sinus syndrome, frequent premature ventricular contractions, or pacemaker-induced rhythms were excluded, as were those who showed any period of atrial flutter or premature ventricular contractions >1/min during signal acquisition. The clinical characteristics of the patients are summarized in Table 1. Care was taken to perform the precardioversion and postcardioversion evaluations while maintaining the same medications, if any. The study also included a control group of 24 normal subjects (14 men and 10 women, age 54±9 years: range 36 to 69) in whom the presence of any disease had been ruled out by means of history, physical examination, routine laboratory tests, ECG, echocardiography, and exercise test. None of them were receiving any medication. The study was approved by the local ethics committee, and all of the participants gave their informed consent.
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Electrical Cardioversion
External cardioversion was performed in all of the patients
according to the best-known established methods.16 Under
the supervision of an anesthesiologist, deep narcosis was induced by
means of the intravenous administration of fentanyl (0.2
mg), diazepam (5 mg), and propofol (20 to 100 mg). Up to 3
R-wave–triggered shocks of increasing energy were applied (the first
shock of 200 J, the second of 300 J, and, if necessary, a third of 360
J).
Protocol and Measurements
The experiments were carried out in the morning in a quiet,
light-attenuated room, whose ambient temperature was kept at 
24°C.
All of the subjects were asked to remain at rest in a supine position
for 10 minutes and then to perform metronome-paced, nonresistive
breathing at a rate of 16 breaths/min for 5 minutes. Tidal volume was
not controlled or measured because it has negligible effects on
respiratory-mediated autonomic oscillations.17
The test was performed during AF and 24 hours after successful
electrical cardioversion while continuously and
simultaneously acquiring ECG (R-R intervals), respiration
(RESP), and noninvasive SBP data, as previously
described.18 19 The respiratory signal was derived from
thorax ECG electrodes by means of an impedance pneumograph
(Hewlett-Packard model 78354C) and blood pressure from the finger with
the use of a Finapres unit (model 2300, Ohmeda) in accordance with
Imholz’s suggestions.20 Periods of 200 to 300 beats were
selected from the tachogram, systogram, and respirogram time series for
spectral analysis (Figure 1).
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Spectral Analysis
Power spectral analysis was performed on the R-R
intervals, SBP, and respiratory signals by means of an autoregressive
technique with the Levinson Durbin algorithm; Anderson’s test was used
to check the validity of the model,21 and the model order
was selected by use of the Akaike Information Criterion,22
starting from a minimum order of 7. A spectral decomposition
algorithm23 was used to measure the centered frequency and
the area below the spectral peaks in the respiratory band (near 0.27
Hz). The respiratory oscillations in the R-R interval (ie,
RSA) and SBP (ie, Ludwig waves, SBP-HF) spectra were identified by
means of cross-spectral analysis24 (expressed in
ms2 and mm Hg2,
respectively).
Cross-Spectral Analysis
To assess the relations between signals in the respiratory band,
we performed autoregressive bivariate spectral analyses between
the R-R intervals and RESP (R-R–RESP), SBP and RESP (SBP-RESP), and
R-R intervals and SBP (R-R–SBP) as in previous
studies24 25 by use of the squared coherence function
(K2) to evaluate the phase stability between the
oscillations of 2 signals (range: 0, no relation to 1,
close relation) at any frequency and phase function (
; range
-180° to +180°). When was negative, the first signal was
considered as following the second, and vice versa. was expressed
in both degree and seconds.26 Furthermore, we calculated
the spectral baroreflex gain in the high-frequency band (
HF) as the
square root of the ratio of the R-R and SBP variabilities
(ms/mm Hg).26
Statistical Analysis
The data are given as mean values±SEM or, when the distribution
was strongly skewed, as geometric means and ranges. A Student’s
t test for paired data was used to evaluate the differences
within the patient group, and an unpaired t test was used
for the differences between the patients in sinus rhythm and the
control group. A value of P<0.05 was considered
significant.
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Results |
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All of the subjects completed the paced breathing test, with none of them having any difficulty in controlling their respiration. Respiratory power was always centered at
0.27 Hz in all subjects and
under all conditions (Table 2).
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Sinus rhythm was restored by means of electrical shocks in all of the patients. The mean number of shocks was 1.3 and the mean delivered energy was 231 J.
Effects of Sinus Rhythm Restoration
As expected, the R-R intervals were shorter during AF than during
sinus rhythm. The difference in SBP before and after the restoration of
sinus rhythm was not statistically significant (Table 2),
whereas diastolic blood pressure was statistically lower
after cardioversion as a consequence of the longer run-off time. The PR
interval in the patient group was 184±6 ms (range 140 to 240 ms).
During AF, ventricular rhythm was decoupled from respiration because of the low degree of K2 between the two signals (0.18±0.03), but this value significantly increased with the reappearance of sinus rhythm (0.86±0.04) (Table 3).
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Similarly, the relation between the R-R interval and SBP variabilities was low during AF (0.27±0.04) and high after cardioversion (0.8±0.05) (Table 3).
The respiratory oscillations in SBP, whose
K2 during AF was 0.67±0.05, significantly
decreased by 72% during sinus rhythm (Table 2), with a concomitant increase in
K2 (0.93±0.03); sinus node restoration had no
effect on the between these 2 signals (Table 3). Examples of
spectral analysis are reported in Figure 2 and Figure 3.
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Differences Between Patients and Control Subjects During Sinus
Rhythm
The values of the R-R intervals and systolic and
diastolic blood pressures did not differ between the
2 groups (Table 2). The RSA and HF values were lower in the
patients than in the control subjects, but this difference was not
statistically significant. There was no difference between the 2
groups in terms of the magnitude of respiratory SBP variability (Table 2).
The phase lag between the considered signals and the K2 between respiration and SBP were similar in the two groups (Table 3), whereas the K2 between the R-R intervals and SBP, as well as that between respiration and the R-R intervals, was significantly higher in the control group (Table 3).
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Discussion |
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The main findings of the present study are that (1) respiration has inconsistent effects on ventricular rhythm during AF; and (2) respiratory modulation of heart rate, which is virtually absent during AF, plays an antioscillatory role in SBP variability, probably as a result of arterial baroreflexes.
Effects of Respiration on Ventricular Rhythm and SBP
During AF
Considerable interest has been shown in the possibility of
identifying any "regularity" in the irregular
ventricular rhythm characterizing AF27 and in
evaluating whether this "regularity" is related to the influence of
autonomic nervous system activity. This interest is due to the fact
that it has been suggested that reduced heart rate variability during
AF may be associated with an adverse prognosis in patients with
nonischemic mitral regurgitation28
or advanced heart failure.29 Cardiac vagal activity
fluctuates with respiration during sinus rhythm, thus leading to the
quantifiable phenomenon of RSA,30 which is associated with
parallel changes in atrioventricular
conduction.31 Previous studies have provided evidence
indicating the presence of vagal influences on ventricular
rhythm in patients with AF,32 and demonstration of the
effect of respiratory oscillations on
ventricular rhythm in such patients may provide a
noninvasive measure of cardiac vagal activity.
Few studies have so far investigated the possible respiratory effect on ventricular rhythm during AF. In 1920, Kilgore1 reported respiratory oscillations in 6 of 9 patients with AF and, in 1989, Rawles et al3 demonstrated the same phenomenon in 14% of patients by means of cosinor analysis. Chandler and Trewby4 and Nagayoshi et al5 found that only a small percentage of patients showed respiratory modulation of heart rate during AF (10.5% and 18%, respectively) but, although these are the only studies that used spectral techniques, they have the major limitation that respiration was not measured.33 The presence of a peak in the R-R interval spectrum at a similar respiratory rate does not necessarily imply a relation with breathing; furthermore, to verify the relation between 2 signals, it is necessary to perform cross-spectral analysis, as shown in Figure 4.
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We found a low degree of coherence between respiration and heart rate variability during AF (always <0.47), which makes it possible to conclude that the effects of respiration on heart rate variability are weak and inconsistent in this condition. If we had taken the widely accepted cutoff point of 0.5 to define the K2, a statistically reliable measure, none of our patients would have shown any respiratory modulation of R-R intervals during AF.
The absence of respiratory arrhythmia during AF in our patient population was not related to reduced vagal activity; respiratory arrhythmia was found after the restoration of sinus rhythm, and this was not the effect of drugs because medication was the same at both evaluations. On the other hand, SBP oscillated widely during AF, and there was a good level of K2 with respiration, which, in the absence of a synchronous oscillation in heart rate, clearly demonstrates a direct effect of respiration on blood pressure. As expected, no relation was found between R-R intervals and SBP variabilities. These findings suggest that respiratory fluctuations in SBP do not depend on changes in R-R intervals. Similar results have been reported in studies of respiratory-related blood pressure variability in normal subjects after pharmacological autonomic blockade34 and in heart transplantation patients.13 14 15 When RSA is eliminated, the respiratory modulation of SBP persists.
Effects of Sinus Rhythm Restoration
During sinus rhythm, the high coherence values between the
considered signals made it possible to evaluate vagal activity on the
sinoatrial node by calculating RSA and the HF. After cardioversion,
the magnitude of Ludwig waves decreased by 72%, and there was a
synchronous reappearance of RSA. The only explanation for this
phenomenon is represented by the mechanical influence of
respiration on cardiac output; in particular, respiration modulates
venous return, whose modification is transmitted to the left ventricle
and causes a variation in arterial pressure. These changes
are rapidly buffered by the vagal arm of the arterial
baroreflex. Therefore the reduction in respiratory SBP variability
found in the present study appears to be due to the buffering
action of the baroreflex on these oscillations: An increase
in blood pressure is associated with an increase in R-R intervals. This
model is also supported by the value of the phase relation between the
R-R interval and SBP (-8°) after cardioversion and in the control
group: The fluctuations in the R-R interval appeared to follow SBP
fluctuations, and an increase in SBP was associated with a concomitant
lengthening in R-R intervals. On the other hand, Taylor and
Eckberg8 found a positive HF (9±7°) in humans during
sinus rhythm and that the elimination of RSA by means of electrical
esophageal pacing significantly reduced SBP variability in the
respiratory band. In accordance with the results of Akselrod et
al,35 the authors concluded that the baroreflex was not
involved in the genesis of RSA in a supine position. The difference
between Taylor’s and our own results may be explained by the
discomfort related to electrical pacing, which, as suggested by Piepoli
et al,36 could have given rise to an alteration in
baroreflex activity. Moreover, the same authors36 have
also suggested the important role of arterial baroreceptors
in generating RSA in humans on the basis of their results after the
selective stimulation of carotid baroreceptors by means of neck
suctions.
The role of baroreceptors in influencing SBP is still unclear despite the fact that various studies have attempted to analyze this relation with different models and methods: Some have eliminated RSA by means of pharmacological autonomic blockade10 11 34 or fixed cardiac pacing7 8 9 ; others have studied cardiac denervation in heart transplantation patients13 14 15 or in those with autonomic failure.12 However, the results obtained in these studies are discordant for a number of different reasons, including the presence or absence of cardiac disease, the use of drugs, and the fact that the analyses were performed during controlled breathing.
The importance of the present study is that it is the first to explore the relation between RSA and Ludwig waves with the use of a model in which the R-R intervals are virtually random in the respiratory band.
Limitations of the Study
We cannot exclude that lower baroreflex sensitivity in patients as
compared with control subjects could be due to 1 or more of the
following: drug treatment; systemic hypertension; or an altered
activation of atrial cardiopulmonary receptors secondary to a
"mechanical stunning" of atrial systolic function, which
could interact with arterial baroreflex
responsiveness. Moreover, we cannot exclude that the lower
stroke volume during atrial fibrillation may cause greater
respiratory-related blood pressure oscillations.
Conclusions
Analysis of cardiorespiratory interactions in patients
during AF and after the restoration of sinus rhythm shows that (1)
respiratory modulation of heart rate during AF is inconsistent
and should therefore be considered virtually absent; and (2) AF
represents a unique human model in which respiratory
oscillations in heart rate are eliminated, thus making it
possible to study the synchrony of SBP oscillations and
respiration. The restoration of sinus rhythm is associated with the
reappearance of RSA and a marked reduction in SBP
oscillations. These findings suggest that in a supine
resting position, respiratory sinus arrhythmia may
represent the baroreflex buffering of arterial
SBP.
Received April 12, 1999; first decision May 12, 1999; accepted June 28, 1999.
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