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Anesth Analg 2002;94:16-21
© 2002 International Anesthesia Research Society


CARDIOVASCULAR ANESTHESIA

Heart Rate Variability and Arterial Blood Pressure Variability Show Different Characteristic Changes During Hemorrhage in Isoflurane-Anesthetized, Mechanically Ventilated Dogs

Masaki Kawase, MD*, Toru Komatsu, MD{dagger}, Kimitoshi Nishiwaki, MD{ddagger}, Makoto Kobayashi, MD{ddagger}, Tomomasa Kimura, MD{ddagger}, and Yasuhiro Shimada, MD{ddagger}

Department of Anesthesiology and Intensive Care Unit, Tosei General Hospital, Seto, Aichi, Japan; {dagger}Department of Anesthesiology, Aichi Medical University School of Medicine, Yazako, Nagakute, Aichi, Japan; and {ddagger}Department of Anesthesiology, Nagoya University School of Medicine, Nagoya, Japan

Address correspondence and reprint requests to Masaki Kawase, MD, Department of Anesthesiology and Intensive Care Unit, Tosei General Hospital, 160 Nishioiwake-cho Seto, Aichi, 489-8642 Japan. Address e-mail to FZA00627{at}nifty.ne.jp


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
We assessed the changes in heart rate variability (HRV) and blood pressure variability (BPV) as indices of autonomic nervous system and volume status during hemorrhage in isoflurane-anesthetized, mechanically ventilated dogs. Nine dogs were used. They were sequentially subjected to withdrawal of 30% estimated blood volume and graded isoflurane inhalation of 1% and 2% followed by discontinuation of isoflurane and retransfusion. The power spectra of HRV and BPV were computed using the fast Fourier transformation, and were quantified by determining the areas of the spectrum in two component widths: low-frequency component (LF) (0.04–0.15 Hz) and high-frequency component (HF) (0.15–0.4 Hz). During hemorrhage and isoflurane anesthesia, both HRV-LF and HRV-HF were decreased and plateaued at the smaller concentration of isoflurane, whereas BPV-LF decreased concentration-dependently. BPV-HF showed a completely different response and increased significantly during 2% isoflurane. We speculate that HRV and BPV-LF would be affected by the autonomic nervous activity, whereas BPV-HF would depend on relative/absolute change in circulating blood volume.

IMPLICATIONS: Power spectra of heart rate variability (HRV) and blood pressure variability (BPV) were computed using the fast Fourier transformation. The HRV and BPV showed their differential characteristics during hemorrhage, isoflurane anesthesia, and retransfusion, and would help to assess changes in autonomic nervous system and preload under mechanical ventilation.


    Introduction
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Heart rate (HR) and blood pressure (BP) appear stable in the steady state but they have various fluctuations. Heart rate variability (HRV) and blood pressure variability (BPV) contain some frequency components, which are divided by a spectral analysis. The low-frequency (0.04–0.15 Hz) component (LF) of HRV is modulated by both the sympathetic nervous system and the parasympathetic nervous system and the high-frequency (0.15–0.4 Hz) component (HF) of HRV is mainly modulated by the parasympathetic nervous system (14), whereas LF of BPV is associated with the sympathetic nervous system (2,46) and HF of BPV is associated with the mechanical effect of respiration (1,2,4,7). The LF/HF ratio in HRV or BPV is used to assess a predominant shift in the sympatho-parasympathetic balance (3,4,7,8).

As hypovolemia increases in severity, we often observe a large respiratory arterial BP fluctuation, which is explained by the interaction between intrathoracic pressure and decreased venous return (9,10). Systolic pressure variation (SPV) is a sensitive indicator of hypovolemia in mechanically ventilated dogs (9,10). SPV is one of the analytical methods using a respiratory cycle. During mechanical ventilation, HF of BPV shows a peak power at ventilatory frequency. Therefore, we consider that HF of BPV would reflect hypovolemia similar to SPV. In conscious spontaneously breathing rats (11) and anesthetized mechanically ventilated dogs (12), HF of BPV increases during hemorrhage. This suggests that HF of BPV may be an alternative to preload indexes such as central venous pressure (CVP).

Hemorrhage changes autonomic nervous activity and decreases circulating blood volume, whereas isoflurane changes autonomic nervous activity and decreases vessels’ resistance. However, very little is known about the effects of hemorrhage and isoflurane on HRV and BPV (1215). The purpose of this study was to assess the relationships among HRV, BPV, and the physiologics of hemorrhage and isoflurane anesthesia in mechanically ventilated dogs.


    Methods
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
The study was approved by our local IRB. Nine dogs weighing 13~16kg were anesthetized with ketamine (10 mg/kg IM) and transferred to the animal operating room. The trachea was intubated with thiamylal (10 mg/kg IV) and succinylcholine (2 mg/kg IV). Anesthesia was maintained with {alpha}-chloralose (50 mg/kg bolus IV followed by 15 mg · kg-1 · h-1 IV) (16) and vecuronium (0.1 mg/kg bolus IV followed by 0.1 mg · kg-1 · h-1 IV). The lungs were mechanically ventilated with room air at 15 breaths/min. Catheters were placed in the abdominal aorta via the right femoral artery to measure arterial blood pressure (ABP) and in the left femoral artery to draw blood. A venous cannula inserted in the upper extremity was used to infuse drugs. After laparotomy, splenectomy was performed to avoid the blood reservoir effect (17). One hour before data acquisition, the dogs were infused with 40 mL/kg acetate Ringer’s solution. Throughout the experiment, body temperature was kept within the normal range (5).

After conditions stabilized (control phase), dogs were bled rapidly through the arterial catheter by 30% of estimated blood volume (EBV), which is calculated as 90 mL/kg (18). We kept the shed blood by adding heparin at room temperature. After stopping withdrawal of 30% of EBV blood, we waited until the ABP and HR stabilized on the monitor display. Then, 1% and 2% of isoflurane at expiratory concentration were administered by increasing the concentration of isoflurane. After isoflurane was discontinued, we transfused the shed blood. Six experimental phases were defined as follows: control phase, Hypo phase (the phase after 30% EBV bleeding), 1% Iso phase, 2% Iso phase, Dis-Iso phase (the phase after isoflurane discontinued), and the Re-BTF phase (the phase after 30% EBV was retransfused). Each phase was maintained for at least 10 min of stabilization of BP and HR.

The analyses of HRV and BPV were performed by using a microcomputer, as described previously (1214,18). The signals of the electrocardiogram (ECG) and ABP were A/D converted at a frequency of 1 kHz. The R wave of the signal of the ECG was detected by a peak detection method. Time series of 1/RR were then low pass filtered at 2 Hz and an instantaneous HR time series was sampled at 4 Hz. The data of the arterial blood waveform were low pass filtered at 2 Hz, and an ABP time series was sampled at 4 Hz.

These data were stored on a magnetic optical disk. Off-line spectral analysis was performed on 608-s segments of RR intervals and ABP time series of each phase. The power spectra of HR and BP were computed using the fast Fourier transformation. Then, the power spectra were normalized by squared mean HR and mean BP, respectively. Power spectra of HR and BP were quantified by determining the areas of the spectrum in two component widths, LF component (0.04–0.15 Hz) and HF component (0.15–0.4 Hz).

To accurately describe the frequency characteristics of HRV and BPV, the data must conform to the stationary assumption, i.e., mean and variance independent of time. However, during a 608-s period of each phase, it is not easy to meet the assumption. To solve this problem, we used the following two procedures (1214,18):

1) High-pass filter at 0.02 Hz; RR intervals and ABP time series were high-pass filtered at 0.02 Hz. The cut-off frequency is slower than the expected frequency of HRV and BPV relating with autonomic nervous activity and ventilation.
2) Sequential analysis of overlapping 128-s data segments; we derived 608-s segment LF and HF measurements using sequential analysis of overlapping 128-s data segments, with each sequential 128-s segment beginning 32 s after the beginning of the previous segment. Six-hundred-eight-second LF and HF were summed up into 16 sequential trended subsegments of power spectral arrays, which are shown as three-dimensional surfaces in Figures 1 and 2.



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   Figure 1. A typical example of changes in heart rate (upper panel) as well as 16 sequential power spectral arrays of heart rate variability-low frequency component (HRV-LF) and heart rate variability-high frequency component (HRV-HF) on a three-dimensional surface (lower panels) during hemorrhage in an isoflurane-anesthetized, mechanically ventilated dog. HR = heart rate; LF = low frequency component; HF = high-frequency component; CTL = experimental control phase; HYPO = experimental phase after 30% estimated blood volume (EBV) bleeding; 1% ISO = experimental phase of 1% isoflurane administration; 2% ISO = experimental phase of 2% isoflurane administration; Dis-ISO = experimental phase after isoflurane was discontinued; Re-BTF = experimental phase after 30% EBV was retransfused.
 


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   Figure 2. A typical example of changes in arterial blood pressure (ABP) (upper panel) as well as 16 sequential power spectral arrays of blood pressure variability-low frequency component (BPV-LF) and blood pressure variability-high frequency component (BPV-HF) on a three-dimensional surface (lower panels) during hemorrhage in an isoflurane-anesthetized, mechanically ventilated dog. LF = low frequency component; HF = high-frequency component; CTL = experimental control phase; HYPO = experimental phase after 30% estimated blood volume (EBV) bleeding; 1% ISO = experimental phase of 1% isoflurane administration; 2% ISO = experimental phase of 2% isoflurane administration; Dis-ISO = experimental phase after isoflurane was discontinued; Re-BTF = experimental phase after 30% EBV was retransfused.
 
We obtained ABP values by averaging the ABP time series data of 608-s, and we obtained LF and HF values by averaging the 16 sequential trended measurements. HRV- and BPV-LF/HF ratios were calculated (1719).

We investigated the effects of hemodynamics and metabolism on each phase. Hemodynamic variables included mean pulmonary arterial pressure (PAP), pulmonary capillary wedge pressure, CVP, mixed venous oxygen saturation (Svo2) and cardiac output (CO) by a flow-directed pulmonary artery catheter (CCO/SVO2:744H7.5F; Baxter, Irvine, CA). The metabolic variables included Hb, pH, HCO3-, base excess, and lactate measured by arterial blood analysis (ABL 300, Radiometer, Copenhagen, Denmark).

As statistical analysis, logLF and logHF were calculated by taking the common logarithm of the power spectra of each component (1214,20,21). A normal distribution of log power spectra at each phase was confirmed by the Kolmogorov-Smirnov test. Comparisons for the time course were analyzed by using one-way repeated-measures analysis of variance followed by multiple comparisons of Fisher’s protected least significant difference to assess HR, ABP, logLF, logHF, and the hemodynamic and metabolic numeral data except LF/HF ratio. The logLF and logHF data are expressed as mean (95% confidence intervals) and median, and other data are expressed as mean ± SD. Nonparametric Friedman test, followed by multiple comparisons of the Student-Newman-Keuls test, were used to assess comparisons of the LF/HF ratio for the time course. The LF/HF ratio data are expressed as median (range). P < 0.05 was considered statistically significant.


    Results
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
Figures 1 and 2 show a typical example of changes in HR and ABP as well as sequential LF and HF power spectral arrays of HRV and BPV on a three-dimensional surface.

Table 1 shows changes in HR and ABP during hemorrhage in isoflurane-anesthetized mechanically ventilated dogs. In the Hypo phase the HR did not change but in the 2% Iso phase the HR decreased significantly compared with the Hypo value. In the Re-BTF phase the HR decreased significantly compared with control, Hypo, 1% Iso, and Dis-Iso values.


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Table 1. Changes in Hemodynamic and Metabolic Variables During Hemorrhage in Isoflurane-Anesthetized Mechanically Ventilated Dogs
 
In the Hypo phase the ABP decreased significantly compared with the control value, and further decreased significantly dependent on isoflurane concentration. However, in the Dis-Iso phase the ABP returned to the Hypo value, and in the Re-BTF phase it returned to the control value.

Table 2 shows changes in HRV profile during hemorrhage in isoflurane-anesthetized mechanically ventilated dogs. In the Hypo phase the HRV-LF did not change, but in the 1% Iso and 2% Iso phases it decreased significantly compared with the control and Hypo values. However, there was no significant change between the 1% Iso and 2% Iso phases. In the Dis-Iso phase the HRV-LF significantly increased compared with the 2% Iso value, and in the Re-BTF phase the HRV-LF significantly increased compared with the 1% and 2% Iso values.


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Table 2. Changes in Heart Rate Variability (HRV) and Blood Pressure Variability (BPV) Profiles During Hemorrhage in Isoflurane-Anesthetized Mechanically Ventilated Dogs
 
In the Hypo phase the HRV-HF did not change but in the 1% Iso and 2% Iso phases it decreased significantly compared with the control and Hypo values. However, there was no significant change between the 1% Iso and 2% Iso phases. In the Dis-Iso phase the HRV-HF did not change significantly compared with both 1% Iso and 2% Iso values. In the Re-BTF phase the HRV-HF significantly increased compared with the 1% Iso, 2% Iso, and Dis-Iso values. The HRV-LF/HF had no significant change throughout the experiment, but in the Dis-Iso phase it was relatively high.

Table 2 also shows changes in BPV profile during hemorrhage in isoflurane-anesthetized mechanically ventilated dogs. In the Hypo phase the BPV-LF significantly increased compared with the control value, but it decreased stepwise dependent on isoflurane concentration, and significantly decreased in the 2% Iso phase compared with the Hypo value. In the Dis-Iso phase the BPV-LF increased significantly compared with the 2% Iso value. Even in the Re-BTF phase the BPV-LF was significantly high compared with the control value.

The BPV-HF in the Hypo phase increased significantly compared with the control value, and it increased stepwise dependent on isoflurane concentration. However, in the Dis-Iso phase the BPV-HF decreased significantly compared with the 2% Iso value. In the Re-BTF phase the BPV-HF showed the lowest value.

The BPV-LF/HF in the Hypo phase did not change, but it decreased dependent on isoflurane concentration, and significantly decreased in the 2% Iso phase compared with the Hypo value. In the Re-BTF phase the BPV-LF/HF significantly increased compared with the 2% Iso and the control values.

Table 1 shows hemodynamic and metabolic changes during hemorrhage in isoflurane-anesthetized mechanically ventilated dogs. In the Hypo phase pulmonary arterial pressure, CO and SvO2 values showed significant decreases compared with the respective control values. During isoflurane phase these values did not change, but in the Re-BTF phase they recovered to the control values. The arterial blood pH, HCO3-, base excess, and lactate were not affected by the 30% EBV blood loss and isoflurane.


    Discussion
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
The present HRV and BPV showed different characteristic changes during hemorrhage, isoflurane inhalation, and retransfusion. It is especially worth noting that during hemorrhage and isoflurane anesthesia the changes in HRV were plateaued at the smaller concentration of isoflurane but that the BPV changed dose dependently and that during isoflurane inhalation the response in BPV-HF was completely different from the responses of HRV-LF, HRV-HF, and BPV-LF. We speculate that BPV-LF would be affected by interaction between sympathetic nervous activity and circulating blood volume, although the mechanism was not clarified, and that BPV-HF would depend on at least relative and/or absolute change in circulating blood volume, although the role of the autonomic nervous system could not be denied. These indicate that by using both HRV and BPV values, we could assess changes in autonomic nervous system and preload under mechanical ventilation and inhaled anesthesia with isoflurane.

In the Hypo phase we noticed a characteristic difference between the HRV-LF and the BPV-LF. That is, BPV-LF could augment further in the presence of stable HRV. It is reported that LF (around 0.05 Hz) of both HRV and BPV increases in conscious spontaneously breathing dogs subjected to 30 mL/kg hemorrhage (16), although very few investigators (8,11,21) have mentioned the different responses of HRV-LF and BPV-LF. In conscious patients undergoing plasmapheresis, BPV-LF increases, although HRV-LF does not change (21). In patients undergoing gastrointestinal endoscopy, BPV-LF increases, although HRV values do not show any change (8). We also have previously demonstrated that BPV-LF is excellently correlated with the degree of hypovolemia until 40% EBV hemorrhage, nevertheless HRV-LF reaches its maximum value at 20% EBV hemorrhage and plateaus thereafter (11). Hence, we consider that the mechanism of generating BPV-LF may be related to other mechanisms besides sympathetic nervous activity, such as intrapleural pressure, hemodynamics, and circulating blood volume. However, the mechanism was not clarified in this study.

In the 2% Iso phase the HR and the ABP decreased. The changes suggest a further suppression of sympathetic nervous activity. The decreased BPV-LF clearly supported this autonomic tendency toward lesser sympatheticotonia. However, the HRV profiles did not detect the suppression of sympathetic nervous activity, and, in reality, the HRV-LF and the HRV-HF were plateaued at the 1% Iso phase.

Interestingly, as far as the HRV-LF is concerned, as shown at the 2% Iso phase in Figure 1, the HRV-LF is suppressed in the earlier power spectral arrays, but is rather activated in the later arrays. Reportedly, the component of 0.04–0.09 Hz band of HRV decreases at 1.0 MAC isoflurane (1.15%) but reincreases at 1.5 MAC isoflurane (1.7%), whereas the component of 0.09–0.15 Hz band of HRV decreases dependent on isoflurane-MAC (13). Thus, these two divided bands have different responses to isoflurane concentration. This might be the reason why the present summed-up value of 0.04–0.15 Hz band, that is, the HRV-LF value did not change from the 1% Iso phase to the 2% Iso phase.

BPV-HF would be generated from interaction between mechanical ventilation and the mechanisms other than autonomic nervous system. During isoflurane inhalation, only the increased response of BPV-HF was completely different from the decreased response of HRV-LF, HRV-HF, and BPV-LF. Isoflurane suppresses autonomic nervous activity (13,15), so we have difficulty explaining the isoflurane-induced increase in BPV-HF by the autonomic responsiveness in sympathoparasympathetic balance.

There could be some correlation between BPV-HF and absolute/relative hypovolemia. In conscious hemorrhagic rats, respiratory systolic BP variation increases (7). In dogs subjected to mechanical ventilation, BPV-HF increases after 30% EBV hemorrhage (12), whereas in rats the HF component of systolic BP increases by administration of prazocine ({alpha}-adrenergic blocker) (4) and the HF of systolic and diastolic BP increase by administration of nitroglycerin (1). However, isoflurane inhalation also decreases peripheral vessel resistance and exaggerates relative hypovolemia, which, we think, induced the stepwise increase in the BPV-HF during isoflurane anesthesia. Thus, BPV-HF, appearing exactly at the frequency of respiration, could be renamed as respiratory-frequentic BP fluctuation associated with decreased venous return and mechanical respiration, which is already demonstrated by SPV (9,10). Furthermore, BPV-HF and BPV-LF/HF would be inappropriate variables in assessing autonomic nervous balance, at least when circulating blood volume changes absolutely or relatively.

All these present changes in the HRV and BPV profiles would have resulted from the autonomic and hemodynamic effects of circulating blood volume and isoflurane anesthesia, not from metabolism, because the metabolic variables did not change throughout the experiment. First, at the control period the HR, the ABP, and the LF/HF ratio of HRV show high values (14,22). The sympathetic predominant balance might have affected some changes in the hemodynamics and the HRV and BPV profiles throughout this experiment. For example, during the isoflurane anesthesia the HRV-HF plateaued and the HR decreased, although it is reported that the HF of HRV decreases dependent on isoflurane-MAC (13,15) and that the HR increases during the isoflurane anesthesia (13,23,24).

Alternatively, HR decreased throughout the experiments. One might expect similar values before and after the hypovolemic situation. {alpha}-Chloralose was used to maintain the anesthetic state during the study period. Although {alpha}-chloralose reportedly has little effect on the autonomic nervous system, the cumulation of the drug could have altered the results obtained. One could speculate the continuous decrease in HR as a time effect or as an effect of isoflurane and/or {alpha}-chloralose anesthesia. We consider that the current results could mostly reflect other larger perturbations of the study. Perhaps the autonomic nervous system and other physiologic subsystems associated with HRV and BPV are underestimated or unrecognized when there are large perturbations going on, such as hemorrhage, anesthesia, and mechanical ventilation. Therefore, it might be suggested that the present results merely affirm a complex relationship among the autonomic nervous system, preload, isoflurane anesthesia, and mechanical ventilation.

In conclusion, this study indicates the new findings in the HRV and BPV as follows: the changes of HRV-LF, HRV-HF, and BPV-LF are in accordance with the previously described reports; and BPV-HF reflects the changes in circulating blood volume. Thus, BPV and HRV in combination could be useful indices in assessing autonomic nervous activity and preload under mechanical ventilation.


    References
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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Accepted for publication August 21, 2001.




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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins with the assistance of Stanford University Libraries' HighWire Press®. Copyright 2006 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press