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1 Hypertension Clinic, Erasme Hospital, 1070 Brussels, Belgium; 2 Consiglio Nazionale delle Ricerca, Medicina Interna II, Dipartimento di Scienze Precliniche Laboratorio Interdisciplinare Technologie Avanzate di Vialba, Ospedale L. Sacco, Università degli Studi di Milano, 20157 Milan, Italy; and 3 Department of Internal Medicine, Mayo Clinic and Mayo Foundation, Rochester, Minnesota 55902
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ABSTRACT |
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 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
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Chemoreflex stimulation elicits both hyperventilation and sympathetic activation, each of which may have different influences on oscillatory characteristics of cardiovascular variability. We examined the influence of hyperventilation on the interactions between changes in R-R interval (RR) and muscle sympathetic nerve activity (MSNA) and changes in neurocirculatory variability, in 14 healthy subjects. We performed spectral analysis of RR and MSNA variability during each of the following interventions: 1) controlled breathing, 2) maximal end-expiratory apnea, 3) isocapnic voluntary hyperventilation, and 4) hypercapnia-induced hyperventilation. MSNA increased from 100% during controlled breathing to 170 ± 25% during apnea (P = 0.02). RR was unchanged, but normalized low-frequency (LF) variability of both RR and MSNA increased markedly (P < 0.001). During isocapnic hyperventilation, minute ventilation increased to 20.2 ± 1.4 l/min (P < 0.0001). During hypercapnic hyperventilation, minute ventilation also increased (to 19.7 ± 1.7 l/min) as did end-tidal CO2 (both P < 0.0001). MSNA remained unchanged during isocapnic hyperventilation (104 ± 7%) but increased to 241 ± 49% during hypercapnic hyperventilation (P < 0.01). RR decreased during both isocapnic and hypercapnic hyperventilation (P < 0.05). However, normalized LF variability of RR and of MSNA decreased (P < 0.05) during both isocapnic and hypercapnic hyperventilation, despite the tachycardia and heightened sympathetic nerve traffic. In conclusion, marked respiratory oscillations in autonomic drive induced by hyperventilation may induce dissociation between RR, MSNA, and neurocirculatory variability, perhaps by suppressing central genesis and/or inhibiting transmission of LF cardiovascular rhythms.
autonomic nervous system; spectral analysis; hyperventilation; apnea; chemoreflexes
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INTRODUCTION |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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SPECTRAL ANALYSIS OF CARDIOVASCULAR VARIABILITY may provide important insights into neural cardiovascular control (18). During sympathetic activation in normal humans there is an increase in the low-frequency (LF) normalized powers of R-R interval (RR) and muscle sympathetic nerve activity (MSNA) variability (22). This relationship may be lost in pathological conditions such as heart failure, where heightened sympathetic drive and tachycardia are associated with attenuated LF power (33). Furthermore, during conditions such as physical exercise where both ventilation and sympathetic outflow are augmented, increases of the LF component of RR are less evident, despite marked tachycardia (6, 17). Ventilation inhibits both cardiac vagal activity (2, 7, 8) and sympathetic nerve traffic (12, 14, 15, 29, 30). Thus changes in ventilation may significantly alter the oscillatory profiles of cardiovascular variability (5, 9, 20). Any interactions between absolute sympathetic drive and spectral parameters of cardiovascular variability are therefore disrupted not only by existing disease states (33) but also by changes in ventilation, as would occur during exercise, chemoreflex activation, and other similar conditions.
Hyperventilation would be expected to increase the high-frequency (HF) component of cardiovascular variability. Hypercapnia, acting primarily via the central chemoreceptors, increases both ventilation and sympathetic drive (30). Sympathetic activation with consequent increases in heart rate and sympathetic nerve traffic would be expected to cause a relative increase in the LF component of cardiovascular variability (22). Changes in neural and cardiovascular variability in response to simultaneous hyperventilation and sympathetic activation are poorly understood. The effects of apnea and consequent elimination of ventilation on MSNA variability are also unknown.
The goal of this study was to determine the influence of changes in ventilatory status on the interaction between changes in RR and MSNA and the spectral powers of neural and cardiovascular variability. By using spectral analysis of simultaneous measurements of RR, MSNA, and respiration, we studied the effects of the following: 1) chemoreflex activation (apnea), 2) hyperventilation, and 3) hyperventilation plus chemoreflex activation (hypercapnia), on the oscillatory characteristics of sympathetic and cardiovascular variability.
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ABSTRACT
INTRODUCTION
METHODS
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DISCUSSION
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Subjects. We studied 14 normal subjects (12 males, 2 females) aged 24 ± 5 yr. None was taking any medications. Informed written consent was obtained from all subjects. The Institutional Human Subjects Review Committee approved the study.
Measurements. Systolic, diastolic, and mean blood pressures were measured every minute with a Physiocontrol Lifestat 200 sphygmomanometer. Electrocardiogram (ECG), respiration (pneumograph), oxygen saturation (Nellcor N-100 C pulse oximeter), and end-tidal CO2 (Hewlett-Packard 47210A capnometer) were recorded on a Gould 2800 S recorder. Minute ventilation was determined by using a Kozak flow-volume turbine module (Vacumetrics). Breathing was via a mouthpiece with a nose clip to ensure exclusive mouth breathing. MSNA was recorded continuously by obtaining multiunit recordings of postganglionic sympathetic activity, measured from a nerve fascicle in the peroneal nerve posterior to the fibular head as described previously (9). Electrical activity in the nerve fascicle was measured by using tungsten microelectrodes (200-µm shaft diameter, tapering to a noninsulated tip of 1-5 µm). A subcutaneous reference electrode was inserted 2-3 cm away from the recording electrode, which was inserted into the nerve fascicle. The neural signals were amplified, filtered, rectified, and integrated to obtain a mean voltage display of sympathetic nerve activity.
Protocol and interventions. To minimize the effects of variations in respiratory rate and pattern on spectral measures during changes in inspired gases, we elected to use paced breathing throughout the experiment. Usually this breathing modality induces a relative increase of the respiratory component of RR variability (18). Respiration was paced at 0.20 Hz throughout the study by using a metronome. Measurements were taken during four interventions in random sequence. First, during a 10-min baseline period of stable ventilation, the subjects breathed room air (controlled breathing). Second, during chemoreceptor stimulation, in the absence of respiratory stimulation, subjects were asked to perform a maximal end-expiratory apnea after hyperventilating room air (without addition of CO2) for 10 min (end-expiratory apnea). This enabled the subjects to perform apneas long enough for autoregressive spectral analysis of cardiovascular variability. Third, the subjects hyperventilated for 10 min while breathing room air with CO2 titrated to maintain isocapnia (isocapnic hyperventilation). Fourth, chemoreflex activation was achieved by having the subjects breathe a hypercapnic hyperoxic gas mixture (7% CO2-93% O2) for 5 min (hypercapnic hyperventilation).
Comparison of spectral analysis of RR and MSNA variability during end-expiratory apneas and hypercapnic hyperventilation further clarified the contribution of ventilation to autonomic modulation during chemoreflex activation. The sequences were performed in random order and separated by a rest period of at least 15 min. The next sequence was started only after end-tidal CO2 and oxygen saturation had returned to initial baseline levels. Good studies examining the effects of chemoreflex activation and hyperventilation on MSNA were obtained in 9 of the 14 subjects. A loss of sympathetic nerve recording occurred during one of the sequences in five subjects. We obtained 11 complete recordings of MSNA during controlled breathing, isocapnic hyperventilation, and hypercapnic hyperventilation, and 9 complete recordings of MSNA were obtained during controlled breathing, hypercapnic hyperventilation, and the subsequent maximal end-expiratory apnea.Data analysis. Sympathetic bursts were identified by a careful inspection of the mean voltage neurogram, and sympathetic activity was calculated as bursts per min. The amplitude of each burst was determined, and sympathetic activity was calculated as bursts per min multiplied by mean burst amplitude. Changes in MSNA were calculated as percent change from the baseline during controlled breathing. P. van de Borne made measurements. The intra- and interobserver variability in our laboratory is 4.3 ± 0.3% and 5.4 ± 0.5%, respectively.
Analog-to-digital conversion was performed over 10 min at 300 sample/s for the ECG, MSNA, and respiratory signals. The data were then analyzed off-line with a personal computer (model 433DX/T, IBM). The principles of the software for data acquisition and autoregressive spectral analyses have been described elsewhere (18, 21, 22, 33). The signal of respiratory activity was sampled once every cardiac cycle, in correspondence with the R wave. The signal of MSNA was time-integrated over each RR. These procedures produced two time series (respirogram and neurogram), which were synchronized with the tachogram. Stationary segments devoid of arrhythmias and artifacts were analyzed with autoregressive algorithms. These algorithms automatically provide the number, center frequency, and power of the oscillatory components. Anderson's test (3, 19) verified that all information contained in the time series had been extracted in the computation, and Akaike's test allowed the determination of the optimal model order fitting the data. Previous studies (22, 26, 33) have shown that two major oscillatory components are usually detectable in short-term RR and MSNA variability. One of these oscillatory components is synchronous with respiration and is called HF oscillation. The other component is described as LF oscillation and has a center frequency of ~0.10 Hz, but can vary considerably from 0.04 to 0.15 Hz (22, 23). In this study, the LF and HF components were expressed in normalized units (NU). The normalized LF and HF units were obtained by calculating the absolute variability of each of LF and HF as a percentage of total power, after subtracting the power of the very LF component, i.e., frequencies <0.03 Hz (3, 21).Statistical analysis. Results are expressed as means ± SE. Statistical analysis of changes during quiet breathing, isocapnic hyperventilation, and hypercapnic hyperventilation consisted of a repeated-measures analysis of variance, followed by pairwise contrasts. The effects of maximal end-expiratory apneas compared with measurements during controlled breathing were determined using Student's paired (two-tailed) t-tests. When data were not normally distributed, Friedman's test corrected for ties was used. Significance was assumed at P < 0.05.
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RESULTS |
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ABSTRACT
INTRODUCTION
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DISCUSSION
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Effects of end-expiratory apneas.
Apneas of 87 ± 9 s (Fig. 1)
decreased oxygen saturation from 98 ± 1% during controlled
(paced) room air breathing (Table 1) to
69 ± 5% at the end of the apnea (P < 0.001).
MSNA increased from 100% (21 ± 4 bursts/min) during controlled
breathing to 170 ± 25% (39 ± 5 bursts/min) during apneas
(P = 0.02, Table 2). The
normalized LF variability of both RR and MSNA increased markedly during
end-expiratory apnea, compared with controlled breathing (P < 0.001, Fig. 2), as
well as the LF-to-HF ratio (P < 0.01, Table 2). The
frequency of the LF oscillations was similar to that measured during
quiet breathing (0.10 ± 0.01 and 0.09 ± 0.01 Hz for RR and
MSNA, respectively, during quiet breathing and 0.11 ± 0.01 Hz for
both RR and MSNA during the apneas). During apnea a small
high-frequency component (in NU) was present in both RR and MSNA
variability but at a frequency that was higher than the paced breathing
rate (Table 2).
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Effects of isocapnic hyperventilation and hypercapnic
hyperventilation.
Almost identical minute ventilations were achieved during isocapnic
hyperventilation and hypercapnic hyperventilation. Tidal volume
increased from 6 ± 0.4 l/min during controlled breathing to
20 ± 1 l/min during isocapnic hyperventilation and to 20 ± 2 l/min during hypercapnic hyperventilation (P < 0.0001, Table 1). End-tidal CO2 was 39 ± 1 mmHg
during controlled breathing, remained unchanged during isocapnic
hyperventilation (38 ± 1 mmHg), and increased to 53 ± 1 mmHg during hypercapnia (P < 0.0001). MSNA was similar
during controlled breathing (100%; 20 ± 3 bursts/min) and during
isocapnic hyperventilation (104 ± 7%) but increased to 241 ± 49% (30 ± 3 bursts/min) during hypercapnia (P = 0.02) (Fig. 3, Table
3).
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DISCUSSION |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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The novel finding of our study is that hyperventilation, despite
tachycardia and increased sympathetic nerve traffic, prevents increases
in LF oscillations during chemoreflex activation. Only during
end-expiratory apneas, in the absence of hyperventilation, is
sympathetic activation accompanied by increases in LF oscillatory power
in both MSNA and RR variability. Our study allowed us to achieve two
almost identical levels of hyperventilation: 1) in the
absence of changes in end-tidal CO2 or MSNA (isocapnic
hyperventilation) and 2) during hypercapnia and increased
MSNA (hypercapnic hyperventilation). In addition, spectral analysis of
RR and MSNA variability during maximal end-expiratory apneas
allowed us to determine the effects of chemoreflex-mediated sympathetic
activation in the absence of any mechanical influence of ventilation. A
qualitative summary of our results is provided in Table
4.
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End-expiratory apnea. Subjects were able to perform very long apneas as a result of hyperoxia and hypocapnia achieved after sustained hyperventilation. Loss of the inhibitory influence of pulmonary afferents, progressive oxygen desaturation, and CO2 retention have been shown to increase muscle sympathetic discharge during apnea (29, 30). In our study the increased MSNA observed during apnea was not associated with an increased heart rate, likely because of activation of the diving reflex (7). Thus the simultaneous vagal activation may help explain the absence of tachycardia during apnea. Regarding the oscillatory components, small HF oscillations in RR and MSNA were still evident after cessation of breathing. The frequency of these oscillations differed, however, from the 0.20-Hz paced rhythm (0.27 ± 0.02 for RR and 0.24 ± 0.01 Hz for MSNA; P < 0.05). Horner et al. (15) reported a similar persistence of HF oscillations in RR during central apneas in hypocapnic and hyperoxic hyperventilated conscious animals. However, the frequency of the respiratory oscillations in RR at the end of apnea was slower than the frequency of the hyperventilatory cycles (15), in contrast to our study. Species, study protocol, and voluntary inhibition of respiratory activity may account for this difference in our findings. Nevertheless, the reduction in HF oscillatory power of MSNA and RR during apnea speaks to the importance of ventilation as a contributor to the HF power of cardiovascular variability. Reflex effects of stretch of pulmonary afferents and consequent cardiac vagolytic effects (2, 7) and inhibition of MSNA are hence important mechanisms in generating the HF variability components of both RR and MSNA.
A key finding of our study is the demonstration of marked LF oscillations in both RR and MSNA during end-expiratory apneas. This is consistent with data demonstrating an increase in LF power of RR in neonatal pigs exposed to hypoxia (13). The frequency of these oscillations was similar to that measured during quiet breathing (0.10 ± 0.01 and 0.09 ± 0.01 Hz for RR and MSNA, respectively, during quiet breathing, and 11 ± 0.01 Hz for both RR and MSNA during the apneas). Our data are also consistent with a report of power spectral analysis of RR and blood pressure in humans, where the LF power of their variability is augmented during apnea (23). However, in that study, during apnea, the authors observed LF oscillations in RR of similar amplitude, but of a lower frequency than during quiet breathing. Differences in methodology (absolute vs. normalized units) and in apnea duration (<40 vs. 87 ± 9 s in our study), and hence in the intensity of chemoreflex activation, may be implicated. There are no previous studies examining the effects of apnea on MSNA variability. The increased LF of cardiovascular variability may be linked to the increased sympathetic drive. Sympathetic-mediated LF oscillations may be potentiated further by the elimination of ventilation-related HF oscillatory influences on LF oscillatory mechanisms. Reduced HF oscillations during apnea further allow most oscillatory power to be concentrated at the LF and increase the LF-to-HF ratio.Isocapnic and hypercapnic hyperventilation. This study addressed the effects of hyperventilation, alone and combined with central chemoreceptor activation, on cardiovascular and sympathetic neural oscillations. Importantly, our subjects achieved almost identical levels of ventilation both in the absence of changes in end-tidal CO2 and during marked hypercapnia. Vagolytic effects of isocapnic hyperventilation (2, 7) reduced RR, whereas the power of both RR and MSNA variability was shifted toward the HF component, despite tachycardia and in the absence of changes in average MSNA. Isocapnic hyperventilation reduced RR and shifted the power of both RR and MSNA variability toward the HF component, without reducing average sympathetic activity. This finding supports the view that average and oscillatory properties of autonomic outflows might respond to different control mechanisms and carry complementary information. Surprisingly, addition of hyperoxic hypercapnia, activating chemoreceptors by increasing PaCO2, increased average sympathetic activity but did not increase LF oscillatory power. Thus, hyperventilation alone, or combined with chemoreceptor activation, reduces the relative LF oscillatory power in autonomic drive. Only when ventilation is eliminated by apnea, does chemoreflex-mediated sympathetic activation elicit increases in relative LF power of cardiovascular variability.
Hypercapnia, acting primarily via the central chemoreceptors, increases MSNA, blood pressure, and ventilation. Sympathetic firing is known to be inhibited during inspiration (9, 13, 26). Several authors (22, 26, 32, 33) have reported the presence of prominent HF oscillations of muscle sympathetic activity in normal subjects. Deep breathing potentiates this inhibitory influence of inspiration (27). However, as in a previous study (27), which used a different methodology, sustained isocapnic hyperventilation did not decrease total MSNA, as decreased activity during the inspiratory phase is compensated for during expiration. Consequently, we observed marked increases in the HF variability of both RR and MSNA during hyperventilation in our study. Hyperventilation has also been reported (1) to increase HF power of RR, whereas Trzebski et al. (32) described similar marked HF cardiovascular variability during hypercapnia. It has also been suggested that in humans, the HF variability of RR and MSNA interval may in part represent baroreceptor-mediated responses to respiratory blood pressure fluctuations (24, 28). Sinus node stretch from respiration-related changes in venous return may in addition contribute to HF RR oscillations (4) but should not directly influence MSNA HF oscillations. Sympathetic activation in the absence of ventilatory changes results in increases in the LF oscillatory power of RR and MSNA (21, 22). Our present study shows that deep breathing overwhelms this modulatory effect of sympathetic activation. Hyperventilation is associated with a redistribution of oscillatory powers of RR and MSNA so that there is a predominant HF component. This is true even when hyperventilation is accompanied by an increased sympathetic drive, as evidenced by tachycardia and heightened MSNA. Thus the oscillatory characteristics of RR and MSNA are almost indistinguishable during isocapnic hyperventilation and hypercapnic hyperventilation, although sympathetic nerve traffic is almost twofold higher during hypercapnia than during isocapnic hyperventilation. Signals originating from the brain stem, from the baroreceptors, or from pulmonary and thoracic stretch receptors may be involved in the inhibitory action of inspiration on sympathetic nerve activity, increased HF power, and a relative reduction in LF oscillatory power. The symmetric respiratory waveform occurring with metronome breathing may also cause a shift in spectral power toward the HF region, and a reduced responsiveness to excitatory stimuli (18, 21). All of these inputs could influence the oscillatory properties of brain stem neurons involved in cardiovascular regulation (19). Thus it is conceivable that marked HF oscillations in autonomic drive could override and suppress central genesis and/or inhibit transmission of LF oscillations in sympathetic and parasympathetic neural oscillatory structures. This mechanism could also explain the attenuated LF variability in RR, during physical exercise, where both ventilation and sympathetic outflow are augmented (6, 17). Changes in ventilation may result in dissociation between RR and MSNA and also disrupt the interactions between LF power and sympathetic drive. Thus, changes in LF power, in particular when expressed in absolute units (11, 16, 25), may not be a reliable correlate of changes in sympathetic activity outside the controlled laboratory environment.Limitations of the study. An important limitation is the incorporation of a controlled, or paced, breathing frequency. Paced breathing may itself influence spectral measures of cardiovascular variability (18, 21). First, in mitigation, the paced breathing protocol eliminated any possible effects of changes in respiratory pattern on spectral measures (5, 20). Second, the same paced breathing protocol was used for all ventilatory interventions, minimizing the likelihood that paced breathing may have selectively influenced our data.
In summary, during apnea, MSNA increases but heart rate remains unchanged. During isocapnic hyperventilation, heart rate increases, but MSNA is unchanged. During hypercapnic hyperventilation, both heart rate and MSNA increase. These ventilatory states are also accompanied by dissociation in the relationships of spectral powers of heart rate and MSNA. Chemoreceptor activation during end-expiratory apnea induces increases in both MSNA and normalized LF components of RR and MSNA. Conversely hyperventilation, alone or combined with chemoreceptor activation, reduces LF oscillations and increases HF oscillations in both heart rate and MSNA. This relative increase in HF powers, also during hypercapnic hyperventilation occurs despite tachycardia and increased MSNA, which in normal conditions would be associated with a relative enhancement of LF powers of RR and MSNA. Thus, during altered patterns of breathing, tachycardia, an important and widely recognized index of sympathetic drive, does not always accompany increases in MSNA. Marked changes in respiration may also elicit a dissociation between changes in cardiovascular sympathetic drive and changes in spectral oscillatory power of neurocirculatory variability.| |
ACKNOWLEDGEMENTS |
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The authors are indebted to Françoise Pignez, Isabella Ghirardelli, and Linda Bang for typing this manuscript.
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FOOTNOTES |
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This study was supported by the National Fund for Research and a 3M Pharma Grant. P. van de Borne was supported by a Bekales Research Award, Belgium. V. K. Somers is an Established Investigator of the American Heart Association and was supported by National Heart, Lung, and Blood Institute Grants HL-60618 and HL-61560, and General Cardiovascular Research Center Grant M01-RR00585. N. Montano was supported by Ministero dell' Università e della Ricerca Scientifica e Tecnologica.
Address for reprint requests and other correspondence: N. Montano, Dipartimento di Scienze Precliniche, LITA di Vialba, Ospedale L. Sacco, Via G. B. Grassi 74, 20157 Milano, Italy (E-mail: Nicola.Montano{at}unimi.it).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 31 August 1999; accepted in final form 14 August 2000.
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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