Am J Physiol Heart Circ Physiol 287: H1821-H1827, 2004.
First published June 3, 2004; doi:10.1152/ajpheart.00252.2003
0363-6135/04 $5.00
Pulse-synchronous sympathetic burst power as a new index of sympathoexcitation in patients with heart failure
Yoshitaka Oda,
Hidetsugu Asanoi,
Hiroshi Ueno,
Kunihiro Yamada,
Shuji Joho,
Tomoki Kameyama,
Tadakazu Hirai,
Takashi Nozawa,
Shutaro Takashima, and
Hiroshi Inoue
Second Department of Internal Medicine, Toyama Medical and Pharmaceutical University, Toyama 930-0194, Japan
Submitted 3 April 2003
; accepted in final form 21 May 2004
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ABSTRACT
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The upper limit of incidence of muscle sympathetic neural bursts can lead to underestimation of sympathetic activity in patients with severe heart failure. This study aimed to evaluate the pulse-synchronous burst power of muscle sympathetic nerve activity (MSNA) as a more specific indicator that could discriminate sympathetic activity in patients with heart failure. In 54 patients with heart failure, the pulse-synchronous burst power at the mean heart rate was quantified by spectral analysis of MSNA. Thirteen patients received a central sympatholytic agent (guanfacine) for 5 days to validate the feasibility of this new index. Both burst incidence and plasma norepinephrine level showed no significant difference between patients in New York Heart Association functional class III (94 ± 6 per 100 heartbeats and 477 ± 219 pg/ml, respectively) and class II (79 ± 14 per 100 heartbeats and 424 ± 268 pg/ml, respectively). In contrast, the burst power was useful for discriminating patients in class III from those in class II (61 ± 8% vs. 39 ± 10%; P < 0.05). Inhibition of sympathetic nerve activity by guanfacine was more sensitively reflected by the change of burst power (–36 ± 25%) than by that of burst incidence (–12 ± 14%; P < 0.001). The sympathetic burst power reflects both burst frequency and amplitude independently of the absolute values and provides a sensitive new index for interindividual comparisons of sympathetic activity in patients with heart failure.
muscle sympathetic nerve activity; 
2-adrenoceptor agonist; spectral analysis
ALTHOUGH THE FUNDAMENTAL MECHANISMS involved remain unclear, sympathoexcitation is not merely a marker of a poor prognosis in patients with heart failure but plays a causative role in its development (2, 4, 7, 12). Muscle sympathetic nerve activity (MSNA), the most specific marker of sympathetic tone in humans, has provided direct evidence of increased central sympathetic outflow in patients with heart failure (4, 8, 9). However, one of the crucial problems with this parameter is quantification of MSNA for interindividual comparisons, because neural bursts are influenced not only by the number and firing rate of active sympathetic fibers but also by proximity to the recording electrodes (15). Therefore, interindividual comparisons have been traditionally based on the burst count per minute (burst frequency) or per 100 heartbeats (burst incidence). A major problem with applying the burst count to assessment of the severity of heart failure is that the maximum value could be limited by the heart rate. Consequently, the burst count is not useful for quantifying sympathetic tone in patients with moderately severe heart failure because most of these patients have a relatively high burst incidence that is close to the upper limit of 100 per 100 heartbeats. Recently, Sverrisdóttir et al. (16, 17) reported that the distribution of burst amplitude was a useful quantitative index for interindividual comparisons. This measure focused on the proportion of large bursts because the amplitude distribution tended to be more even in subjects with a high burst incidence (15).
In the present study, we quantified pulse-synchronous neural bursts by spectral analysis of MSNA in patients with chronic heart failure. The pulse-synchronous burst power was defined as the normalized spectral power of MSNA at the heart rate of each patient. This new index was used based on the hypothesis that when sympathetic activity is high, as in patients with severe heart failure, every heartbeat is accompanied by a neural burst with a similar amplitude. Consequently, power spectral analysis should reveal a single peak at the heart rate. In contrast, several spectral peaks would exist when sympathetic neural bursts are less frequent with variable amplitude, as in the case of normal young subjects. Since this method takes both the frequency and the amplitude of MSNA bursts into account, it does not require measurement of the amplitude of each burst for comparison.
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METHODS
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Patients.
The present study included 54 patients with asymptomatic or symptomatic cardiac dysfunction (43 men and 11 women, aged 56 ± 13 yr). The underlying cardiac disease was dilated cardiomyopathy in 25 patients, ischemic heart disease in 19, valvular heart disease in 4, and other conditions in 6. The New York Heart Association (NYHA) functional class was I in 24 patients, II in 21, and III in 9. The specific activity scale (13) determined from an interview about daily physical activities was 6.1 ± 1.3 metabolic equivalents. Left ventricular ejection fraction (determined by radionuclide or contrast ventriculography) was 38 ± 17% (Table 1). Patients with atrial fibrillation or frequent premature beats were excluded because spectral analysis would yield a broad band in the presence of these conditions. Patients with lung disorders, anemia, severe hypoxemia (arterial oxygen partial pressure <80 mmHg), diabetes mellitus, or autonomic neuropathy due to other causes were also excluded from the present study. Angiotensin-converting enzyme inhibitors had been given in 33 patients, angiotensin-II receptor antagonists in 3 patients, 
-blockers in 9 patients, diuretics in 23 patients, and digitalis in 15 patients. Medications for heart failure were continued throughout the study. None of the subjects had a history of more than occasional alcohol consumption. Informed consent was obtained from each subject.
Measurements.
All measurements were performed with the subjects resting in the supine position, as reported previously (5, 6). Blood pressure was determined by noninvasive tonometry (Jentow 7700; Colin, Komaki, Japan). Respiratory flow was measured continuously on a breath-by-breath basis with a thermal dissipation technique (AE-300; Minato, Osaka, Japan). Multiunit recordings of efferent postganglionic sympathetic nerve activity to the skeletal muscle district were obtained with a microelectrode inserted directly into the left peroneal nerve posterior to the fibular head. The signal was amplified 100,000-fold, fed through a band-pass filter (500–5,000 Hz), and integrated with a custom nerve traffic analysis system (Neuropack
MEB-5504; Nihon Koden, Tokyo, Japan). Integrated neural activity, analog blood pressure tracing, ECG, and respiratory flow were digitized at 1,000 Hz per channel by an analog-digital converter (DT9804-USB; Data Translation, Marlboro, MA) and stored directly in a hard drive memory system (Latitude C600; Dell, Round Rock, TX). To evaluate baseline cardiac function, chest radiographs and two-dimensional echocardiograms were obtained in all patients. A blood sample for measurement of the plasma concentration of norepinephrine was drawn from the antecubital vein with the subject at rest. To examine the reproducibility of pulse-synchronous burst power, measurement of MSNA was repeated after 
1 h in 10 patients resting in the supine position.
In 13 patients, the 2-adrenoceptor agonist guanfacine (0.25 mg/day), which inhibits central sympathetic outflow, was administered orally for a mean of 5 days (4–6 days; Table 1). Measurement of sympathetic nerve activity and plasma norepinephrine level was then repeated.
Data analysis.
Baseline recordings of the ECG, blood pressure, and MSNA were performed for 10 min while patients were breathing room air in the supine position. Sympathetic neural bursts were identified in the integrated signals by their characteristic appearance and their relationship to the R wave of the ECG. The burst frequency was determined for each patient and expressed as bursts per 100 heartbeats. Slow baseline fluctuations of the integrated burst signals caused by transient electromyographic or motor and sensory nerve activity sometimes produced prominent low-frequency spectral artifacts. Therefore, the baseline drift caused by such noise was detected and subtracted from the original integrated nerve activity (Fig. 1). Fast Fourier transformation was then applied to the MSNA time series to distinguish the spectral components of burst signals. This transformation generated power spectra from 29,952-point epochs of data (29.952 s) with 50% overlap. A Hanning window in the time domain was used to attenuate the leakage effect. The mean burst frequency synchronized with the heartbeat was determined in each patient based on the mean frequency of the R-R interval (Fig. 1). In all patients, the R-R intervals were distributed within the frequency range of 0.183 Hz (average ± 2SD) around the mean R-R interval frequency. This frequency range was used for measurement of the spectral area of the pulse-synchronous burst power, and the burst power was then expressed as a percentage of the total power. We defined the total MSNA spectral power as the spectral area ranging from 0.04 to 2.5 Hz because most components of MSNA were within this frequency range. When there are no MSNA bursts, the pulse-synchronous burst power is theoretically 0%, whereas when the sympathetic system is maximally activated with all heartbeats accompanied by neural bursts with the same amplitude, the pulse-synchronous burst power is close to 100% with a single spectral peak at the heart rate. However, even when all heartbeats are accompanied by neural bursts, the variations in amplitude caused by respiratory modulation or blood pressure fluctuation generate several other peaks away from the heart rate frequency, resulting in a decrease of the pulse-synchronous burst power. Thus the pulse-synchronous burst power could potentially discriminate sympathetic tone between patients who have the same burst incidence but a different amplitude distribution. Because of normalization by the total power, measurement of the individual burst amplitudes was unnecessary. To determine the optimum period for acquisition of MSNA data for spectral analysis, the influence of a period of 1–5 min on the spectral power was examined in 11 patients before administration of guanfacine and in 6 patients after administration of guanfacine.
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Fig. 1. Spectral analysis of muscle sympathetic nerve activity (MSNA). The baseline of integrated MSNA bursts was automatically detected in the original integrated neural activity recording (middle left). Baseline fluctuations of the neural activity caused an increase of low-frequency components (middle right). After subtraction of these fluctuations (bottom left), the spectral density showed several discrete peaks (bottom right). Arrow indicates the range of the pulse-synchronous neural frequencies. ECG recording (left) and R-R interval histogram (right) are shown at top.
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Statistical analysis.
Data are expressed as means ± SD. Simple exponential fitting was applied to the relationship between MSNA burst power and burst incidence. Interindividual comparisons of sympathetic parameters were performed with one-way ANOVA followed by Bonferroni's test for multiple comparisons. The effect of guanfacine was tested by paired t-test. Analyses were performed with SigmaStat software (version 2.03; SPSS, Chicago, IL), and the level of significance was set at P < 0.05.
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RESULTS
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Sympathetic burst power.
The reproducibility of pulse-synchronous burst power data was examined in 10 patients with widely differing burst powers ranging from 24 to 73% (43 ± 17%). For patients lying quietly in the same position, the difference in burst power between two measurements obtained >1 h apart was quite small (3 ± 3%, Fig. 2). The pulse-synchronous burst power derived from different measurement periods (1–5 min) also showed no significant difference. The burst power measured before administration of guanfacine was 41 ± 10%, 41 ± 10%, 40 ± 9%, 40 ± 9%, and 39 ± 9% with 1, 2, 3, 4, and 5 min of data, respectively. After suppression of sympathetic activity with guanfacine, there was no significant difference (2 ± 3%) in the spectral power derived from 1 and 5 min of data. Thus the burst power determined from 1 min of data was used for all analyses in the present study.
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Fig. 2. Reproducibility of the burst power of MSNA. Baseline measurement of MSNA burst, power burst spectra, and R-R interval histogram are shown on left. Measurement of MSNA burst power was repeated after >1 h while the patient lay quietly in the same position (right). A similar spectral pattern was obtained by the 2 measurements. There is no variation of the R-R interval in this patient because of cardiac pacing.
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Figure 3 shows the MSNA time series, burst spectra, and frequency histograms of the R-R interval for representative patients with different severity of heart failure. The MSNA power spectra displayed several peaks within the frequency range of 0.04–2.5 Hz. The major spectral band was located at the same frequency as that of the mean heart rate. In patient A with mild heart failure, within-breath variation of bursts created a spectral peak at 0.25 Hz that was separated from the pulse-synchronous burst spectra. In patients B and C with moderately severe heart failure, all heartbeats were accompanied by neural bursts, i.e., the burst incidence was 100 per 100 heartbeats. However, the burst amplitude was more uniform in patient C than in patient B. The differences in variations of burst amplitude resulted in different burst spectra; the power spectra of patient B were distributed widely with several peaks, whereas patient C showed a prominent single peak with the same frequency as the heart rate. Consequently, the pulse-synchronous burst power was significantly greater in patient C than in patient B despite the same burst incidence. There was a significant correlation between burst incidence and pulse-synchronous burst power, as shown in Fig. 4. In the patients with a higher burst incidence (>85 per 100 heartbeats), the incidence reached a plateau of 100 per 100 heartbeats (Figs. 4 and 5), but the burst power still differed substantially among these patients.
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Fig. 3. Comparison between the burst incidence and pulse-synchronous burst power of MSNA in 3 patients with different severity of heart failure. Patient A (mild heart failure; left) has a lower burst incidence and power than the others. Patients B and C (moderately severe heart failure; center and right) have the same burst incidence of 100 per 100 heartbeats despite a different burst amplitude distribution. The uniform amplitude of neural bursts in patient C is reflected by a single spectral peak at the heart rate, resulting in a larger pulse-synchronous burst power. In contrast, patient B shows greater variation of burst amplitude, which has several spectral peaks with different frequencies, leading to a relative reduction of the pulse-synchronous burst power. BP, blood pressure.
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Fig. 4. Relationship between the pulse-synchronous burst power and burst incidence of MSNA. There was a significant correlation between the burst incidence and pulse-synchronous burst power. In patients with a higher burst incidence (>85 per 100 heartbeats), the incidence was close to the maximum level of 100 per 100 heartbeats but the burst power varied substantially.
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Fig. 5. Comparison of three parameters of sympathetic activity for different severity of heart failure. Although each parameter increases with the deterioration of functional capacity, the burst incidence of MSNA (middle) and the plasma norepinephrine level (bottom) do not show a significant difference between New York Heart Association (NYHA) classes II and III. In contrast, the pulse-synchronous burst power (top) was more discriminatory, with patients in NYHA class III having a significantly higher burst power than those in class II. *P < 0.05.
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Interindividual and longitudinal comparisons.
Figure 5 illustrates the pulse-synchronous burst power, burst incidence, and plasma norepinephrine levels in the subgroups of patients from NYHA functional classes I, II, and III. Although all of the sympathetic parameters increased along with the deterioration of functional capacity, the differences in the burst incidence and plasma norepinephrine level did not reach statistical significance for comparison between NYHA classes II and III. In contrast, burst power was more discriminatory, because patients in NYHA class III had a significantly higher burst power than those in class II.
Figure 6 shows the changes of MSNA and pulse-synchronous burst power after administration of a central sympatholytic agent (guanfacine) in a representative patient. Before administration of guanfacine, the burst incidence was >90 per 100 heartbeats and a single power spectral peak was seen at the frequency of the mean heart rate. Guanfacine decreased the number of bursts and increased the within-breath variation of MSNA. Consequently, several other spectral components appeared in addition to the pulse-synchronous component, where a prominent low-frequency component was seen at the respiratory frequency. After administration of guanfacine, the plasma norepinephrine level tended to decline, but this change did not reach statistical significance. Although the burst incidence decreased by –12 ± 14% (P < 0.05) after guanfacine, the inhibition of sympathetic activity was more sensitively reflected by the change of burst power (–36 ± 25%; P < 0.001, Fig. 7).
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Fig. 6. Influence of a central sympatholytic agent (guanfacine) on MSNA burst incidence and pulse-synchronous burst power. Left: baseline burst incidence was >90 per 100 heartbeats, with a prominent pulse-synchronous peak at the heart rate. Cont, control. Right: guanfacine (Gunf) decreased the number of bursts and produced within-breath variation of MSNA bursts. Consequently, several other components and a prominent low-frequency peak around the respiratory frequency appeared in addition to the pulse-synchronous component. There were no variations of the R-R interval in this patient because of cardiac pacing.
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Fig. 7. Inhibitory effects of guanfacine on sympathetic activity. Guanfacine reduced the burst power (left) and burst incidence (middle) of MSNA, with a greater reduction for burst power. The plasma norepinephrine level (right) also tended to decline, but the change did not reach the statistical significance. C, control; G, guanfacine.
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DISCUSSION
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The major findings of this study are as follows. First, the pulse-synchronous burst power of MSNA could discriminate sympathetic tone between patients with heart failure who had similar burst frequencies. Second, assessment of the burst power detected central sympathetic inhibition more sensitively than measurement of the burst incidence or the plasma norepinephrine concentration. Another advantage of the pulse-synchronous burst power is that this parameter is independent of the absolute value of each burst amplitude. Therefore, the MSNA burst power may serve as a sensitive new index for interindividual or longitudinal comparisons of sympathetic activity, especially in patients with moderately severe or severe heart failure.
Because of the dependence on proximity to the recording electrode, the burst amplitude cannot be used for interindividual comparisons of MSNA. To normalize differences in the electrode position, several neural indexes have been introduced in the clinical setting (11, 16–18). Burst rate and burst incidence, the traditional indexes used for interindividual comparisons, focus only on the frequency by ignoring differences in amplitude. Consequently, interindividual differences in sympathetic tone could be underestimated as the burst incidence reaches its plateau of 100 per 100 heartbeats. Recently, Sverrisdóttir et al. (17) proposed the usefulness of amplitude distribution of neural bursts. This was based on the observation that the proportion of high-amplitude bursts tends to increase along with an increase in burst incidence, resulting in a more even amplitude distribution (15). As a specific indicator of sympathetic nerve activity, these investigators derived the median from a histogram of the normalized amplitudes of all neural bursts. Therefore, the determination of the highest burst amplitude is crucial to normalize each burst amplitude and a large number of bursts, such as 1,000–2,000 cardiac cycles in animals (10) or 5-min data in humans (17), are required to determine the 0% and 100% levels of the burst amplitude.
In contrast, the burst power used in the present study does not require measurement of the amplitude of each burst and can be determined from only 1 min of MSNA data. The similarity of the pulse-synchronous burst power obtained from 1-min and 5-min data could be related to the fact that the burst incidence was relatively high in our patients with heart failure and sufficient to assess sympathetic nerve activity. Even when sympathetic activity was suppressed with guanfacine, the burst power showed no significant difference between 1 min and 5 min of data. However, a short data acquisition period might not be feasible in normal subjects with a lower burst incidence. Generally, most of the spectral components of MSNA are found within the frequency range from 0.03 Hz up to that of the heart rate in normal subjects. One of the typical factors causing variation of the burst amplitude is respiratory modulation of sympathetic activity (1, 3, 5, 6, 10, 14). Sympathetic neural silence during the inspiratory phase produces a large spectral peak at the respiratory frequency around 0.25 Hz (Fig. 1; Ref. 5). A well-defined peak related to low-frequency blood pressure variation is also found near 0.1 Hz (6). As sympathetic tone increases with the development of heart failure, the pulse-synchronous peak of the neural bursts becomes predominant over the other spectral components. Consequently, beat-by-beat activation of neural bursts with a similar amplitude results in a single spectral peak at the same frequency as the heart rate. When sympathetic neural bursts have variations in frequency and amplitude, a variety of spectral peaks other than the pulse-synchronous peak can be produced. Thus the pulse synchronicity and shape uniformity of the neural bursts are faithfully reflected by the burst power.
In the present study, the difference in the discriminatory ability between burst incidence and burst power did not seem so striking (Fig. 5) because few of our patients had severe heart failure. When sympathetic activity is low and is largely reflected by the number of neural bursts, both burst frequency and burst power can be useful and will show parallel changes. However, when sympathetic activity is high, it is largely reflected by the distribution of the amplitude of neural bursts. Spectral analysis is more effective in such situations because it can sensitively assess the uniformity of the burst amplitude.
In conclusion, assessment of the pulse-synchronous burst power of MSNA does not require measurement of amplitude of each burst and can be obtained from a relatively short data recording. This parameter is a more sensitive discriminator of sympathetic nerve activity than the traditional burst count or the plasma norepinephrine level and could be useful for interindividual comparisons of sympathetic tone in patients with heart failure.
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ACKNOWLEDGMENTS
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This work was supported by Grant-in-Aid for General Scientific Research No. 13670697 from the Ministry of Education, Science and Culture of Japan.
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FOOTNOTES
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Address for reprint requests and other correspondence: H. Asanoi, Second Dept. of Internal Medicine, Toyama Medical and Pharmaceutical Univ., 2630 Sugitani, Toyama 930-0194, Japan (E-mail: hidetugu{at}ms.toyama-mpu.ac.jp)
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.
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Copyright © 2004 by the American Physiological Society.
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