Chest ACCP Member Benefits
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Guest Access | Sign In via User Name/Password
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via ISI Web of Science (4)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Shen, H.-N.
Right arrow Articles by Yang, P.-C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shen, H.-N.
Right arrow Articles by Yang, P.-C.
(Chest. 2003;123:1222-1228.)
© 2003 American College of Chest Physicians

Changes of Heart Rate Variability During Ventilator Weaning*

Hsiu-Nien Shen, MD; Lian-Yu Lin, MD; Kuan-Yu Chen, MD; Ping-Hung Kuo, MD; Chong-Jen Yu, MD, PhD; Huey-Dong Wu, MD and Pan-Chyr Yang, MD, PhD, FCCP

* From the Department of Internal Medicine (Dr. Shen), En-Chu-Kong Hospital; and Department of Internal Medicine (Drs. Lin, Chen, Kuo, Yu, Wu, and Yang), National Taiwan University Hospital, Taipei, Taiwan.

Correspondence to: Huey-Dong Wu, MD, Department of Internal Medicine, National Taiwan University Hospital, No. 7 Chung Shan South Rd, 100 Taipei, Taiwan; e-mail: hdwu{at}ha.mc.ntu.edu.tw


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study objectives: Despite the recognition that ventilator weaning is associated with a change in autonomic nervous system activity, there has not been any report concerning the change of heart rate variability (HRV), a reliable method to detect autonomic nervous system activity, in patients during weaning. The aim of this study was to investigate the change of autonomic nervous system activity during ventilator weaning by HRV analysis.

Design: Prospective study.

Setting: A 16-bed medical ICU of a tertiary university hospital.

Patients: Twenty-four patients receiving mechanical ventilation were included. Twelve patients with successful extubation after a spontaneous breathing trial (SBT) [T-piece trial] were classified as the success group; otherwise, the patients were placed in the failure group.

Interventions: None.

Measurements and results: Variables, including the total power (TP), and the high-frequency (HF) and low-frequency (LF) components of HRV, were measured in three phases: assist/control mandatory ventilation, pressure support ventilation (PSV), and SBT. While shifting from PSV to SBT, the HRV components decreased significantly in the failure group (TP, p = 0.025; LF, p = 0.007; HF, p = 0.031), but not in the success group.

Conclusions: By HRV analysis, reduced HRV and vagal withdrawal of the autonomic nervous system activity are the main changes in patients with weaning failure.

Key Words: heart rate variability • spectrum analysis • ventilator weaning


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Heart rate variability (HRV) is used as a noninvasive tool in the evaluation of altered autonomic nervous system function.1 2 Since 1981, when Akselrod et al2 introduced power spectral analysis of heart rate fluctuations, the frequency domain analyses of HRV have contributed to the understanding of autonomic cardiovascular control.3 From 5-min ECG recordings made under physiologically stable conditions, the power spectral analysis allows the determination of two major components: low frequency (LF) and high frequency (HF).2 Vagal activity has been consistently regarded as the major contributor to the HF component,2 3 which is known to decrease during exercise,2 3 4 5 6 and to change with different respiratory patterns.7 8 However, a discrepancy exists with respect to the LF component, which some consider to be a marker of sympathetic modulation,3 9 and others view it as a parameter that includes both sympathetic and vagal influences,2 3 while still others treat it as a poor indicator of sympathetic activity.4 5 6

Since ventilator weaning represents a period of transition from mechanical ventilation to spontaneous breathing and is associated with a change in autonomic activity,10 11 12 13 the change of HRV during weaning is to be expected. The influence of artificial ventilation on HRV has been described in preterm infants with respiratory distress syndrome, in decerebrated children, and in adults under anesthesia.1 14 15 16 The change of HRV during different ventilator settings has been investigated in an animal study by Frazier et al.17 They found that there were significant increases in very LF power (sympathetic tone) with a concomitant significant reduction in HF power (parasympathetic tone) with exposure to a combination of pressure support and continuous positive airway pressure.17 These changes in HRV were associated with significantly increased heart rate and reduced right ventricular end-diastolic volume.17 Despite the recognition, there has not been any report concerning the change of HRV during ventilator weaning in patients recovering from respiratory failure. The aim of this study was to investigate the change of autonomic nervous activity during ventilator weaning by HRV analysis.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
Patients
This prospective, observational study was carried out in a 16-bed medical ICU of a tertiary university hospital from November 2000 to February 2001. Patients enrolled in this study with respiratory failure were intubated and received mechanical ventilation for at least 24 h, met the general weaning criteria (see below), and were ready to undergo their first spontaneous breathing trial (SBT) as determined by a primary care physician. Patients were excluded if they were already, or ready to be, tracheostomized, or had frequent cardiac arrhythmias (defined as > 10% of nonsinus beats during Holter study).

Weaning Process
The general criteria for initiating weaning trials were as follows: (1) resolution of the underlying cause of respiratory failure, (2) no need for vasopressors or sedatives, (3) PaO2 > 60 mm Hg on <= 40% inspired oxygen and a positive end-expiratory pressure (PEEP) <= 5 cm H2O, (4) adequate neurologic status and ability to follow simple vocal orders, and (5) intact airway reflexes with an adequate cough during suctioning.18 The ventilator weaning was generally carried out under the mode of synchronized intermittent mandatory ventilation with pressure support ventilation (PSV) or PSV only. Weaning was proceeded with a gradual reduction of the mandatory rates and PSV levels. Before the study, the respiratory therapists measured the traditional weaning parameters, including respiratory rate (f), tidal volume (VT), minute ventilation (E), and f/VT ratio, and physicians were informed to make decisions for the weaning process. The VT and E were measured using a handheld respirometer with the patient breathing spontaneously without ventilator use. The f/VT ratio was calculated according to the study of Yang and Tobin.19 The duration of SBT was variable but usually lasted 2 h. The decision for weaning or extubation was made by the primary care physicians who were not involved in this study.

The failure group was designated as those who failed SBT and needed reinstitution with mechanical ventilation, or those who were extubated but were reintubated within 48 h. The success group was designated as those who were extubated successfully after SBT. If patients were not extubated after SBT, the cause of weaning failure was determined by the same physician. The need for transient noninvasive bilevel pressure ventilation after extubation was not considered to be a weaning failure.

Study Protocol
Data Collection: The clinical features, including age, gender, medications, diagnosis on hospital admission, patient history, APACHE (acute physiology and chronic health evaluation) II score, reasons for initiation of ventilator support, duration of mechanical ventilation prior to SBT, arterial blood gas levels, and weaning parameters before SBT, were recorded. Patients were followed up until ICU discharge or death, and the other variables, such as time from SBT to extubation, causes of weaning failure, the need of tracheostomy, total ICU stays, and mortality, were recorded.

Procedures: The studies were performed during a period from 10 AM to 2 PM, with a total duration of 1.5 h in each patient. A consecutive sample of patients who met the inclusion criteria were studied. All patients were receiving mechanical ventilation (model NPB 7200; Nellcor Puritan Bennett; Carlsbad, CA). All regular medications scheduled prior to the study were not disturbed. Patients were kept in a semisitting position and left undisturbed during the study.

The HRV was measured in three phases: assist/control mandatory ventilation (ACMV), PSV, and SBT. Patients were suctioned and put on ACMV with a preset f of 16 breaths/min, VT of 8 to 10 mL/kg, and PEEP of 5 cm H2O, with the other settings unchanged. After 30 min on ACMV, the ventilator mode was switched to PSV in a range of 6 to 10 cm H2O, as was set prior to the study protocol, and with the same PEEP and fraction of inspired oxygen (FIO2) levels. Again, after 30 min of PSV, patients were put on SBT without external PEEP, with a FIO2 level 5% greater than the ventilator setting. Vital signs and ECG in each phase were recorded after 10 min of mode change.

Analysis of HRV: ECG was recorded on a three-channel ambulatory ECG recorder and scanned on a Holter analysis system (Del Mar 563; Del Mar Avionics; Irvine, CA). The QRS complexes were automatically classified and manually verified as normal sinus rhythm, atrial or ventricular premature beats, or noise by comparison to the adjacent QRS morphologic features. The normal-to-normal R-R intervals (N-N intervals) were deduced from the adjacent normal sinus beats. The N-N interval time series were then transferred to a personal computer and postprocessed by a program written in the Matlab language (version 5.2; Mathworks; Natick, MA).20 The missing intervals of the raw N-N data were interpolated by the cubic spline method and resampled at 4 Hz by the Ron-Berger method. After 10 min in each phase, a stable 5-min segment of N-N intervals was taken for HRV analysis. The power spectrum densities were estimated by the averaged periodogram method of Welch.21 The LF power (0.04 to 0.15 Hz) and HF power (0.15 to 0.4 Hz) were derived from the sum of area within specific frequency range under the power spectrum density curve of the same 5-min segment. The total power (TP) was calculated from the sum of LF and HF. The normalized unit (NU) of HF (HF NU) or LF (LF NU) was calculated as the ratio of the absolute powers of HF or LF to TP and multiplied by 100.2

Statistics
Patients were grouped and analyzed according to the outcome of SBT. All data were reported as mean ± SD, except when otherwise specified. Statistical analysis was performed with SPSS in the Windows 98 operating system (SPSS; Chicago, IL). Because of skewed distribution, the LF, HF, LF/HF ratio, and TP are transformed in the natural logarithm of the absolute units (square milliseconds). Categorical variables were analyzed by {chi}2 or Fisher exact tests. Means were compared between success and failure groups by independent Student t test. Measurements of heart rate (HR), BP, f, and HRV components over three phases (ACMV, PSV, and SBT) were compared with a repeated-measures analysis of variance, and then a post hoc paired t test for significant differences. A p value < 0.05 (two-tailed) was considered to be significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
Demographics
Twenty-four patients were enrolled, with 12 patients in the success group. The general clinical features, including gender, age, mean APACHE II score on hospital admission, duration of mechanical ventilation prior to SBT, reasons for respiratory failure, underlying diseases, and uses of various medications, were similar between both groups (Table 1 ). Pneumonia was the most common cause of respiratory failure. Both groups were similar in baseline blood gas data prior to study (Table 2 ).


View this table:
[in this window]
[in a new window]

  		Table 1.. Demographic Features of the Study Population at Baseline According to Weaning Outcomes*

 

View this table:
[in this window]
[in a new window]

  		Table 2.. Blood Gas and Respiratory Parameters Measured Before Weaning Trials*

 
Traditional Weaning Parameters
Respiratory parameters measured before SBT showed a significant lower VT and higher f/VT ratio in the failure group (p < 0.05; Table 2 ). The differences in f and E were insignificant.

Heart Rate, BP, and Spectral Components of HRV
The changes of f, HR, and spectral components of HRV during weaning trials are plotted in Figure 1 . When comparing the success and failure groups, we found no difference in the mean values of all variables in each phase, except for f during SBT in the failure group, which was significantly higher than that of the success group (29.6 ± 7.3 breaths/min vs 23.7 ± 4.7 breaths/min, p = 0.015). In both groups, the change of f from ACMV to PSV and that from PSV to SBT showed significant increases (Fig 1) .



View larger version (19K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1.. Change of mean f, HR, and spectral components of HRV during ventilator weaning. Top left, a: In both groups, mean f increased significantly from ACMV to PSV, and then to SBTs through a T-tube. During SBT, the mean f in the failure group was significantly higher than that in the success group. Top right, b: In the failure group, the mean HR increased significantly from PSV to SBT. Middle left, c; middle right, d; and bottom, e: In both groups, the difference of HRV in absolute units (with natural logarithm transformations) between ACMV and PSV was insignificant. In the failure group, the LF and HF components and TP of HRV decreased significantly from PSV to SBT; in addition, the difference of HRV between ACMV and SBT was also significant.

 
In the success group, the changes of HR, BP, and HRV components were insignificant among the three phases. In the failure group, HR increased from PSV to SBT (p < 0.05), and there were significant decreases in HF, LF, and TP of HRV when comparing SBT to PSV and ACMV (p < 0.05; Fig 1 ). In both groups, there was no significant change in the LF/HF ratio or the NUs of LF and HF powers (Table 3 ).


View this table:
[in this window]
[in a new window]

  		Table 3.. Change of HRV During Weaning Trial*

 
Follow-up
We followed up all patients until ICU discharge. The difference in total ICU stays between the two groups was statistically insignificant (10.5 ± 7.7 days vs 17.1 ± 12.8 days, p = 0.142). In the success group, all patients were alive and without late respiratory failure (namely, > 48 h); time from SBT to extubation was 2.3 ± 1.0 h. In the failure group, time from SBT to reinstitution of mechanical ventilation was 1.5 ± 0.77 h. The causes of weaning failure included four patients with tachypnea (> 35 breaths/min), one patient with hypertension (systolic BP elevation > 40 mm Hg), one patient with tachycardia (> 120 beats/min), two patients with decrease in consciousness level, two patients with respiratory distress/diaphoresis, and two patients with suspected airway edema because of negative cuff-leak test result performed before extubation. One patient died of ventilator-associated pneumonia before further weaning trial. Of the five weaned patients in the failure group, two patients were weaned after the second SBT, and three patients were weaned after the third attempt. Finally, the other six patients underwent tracheostomy; of these, four patients were weaned from the ventilator eventually, and two patients were still ventilator dependent after transfer to the ward.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
In this study, we found that there were no significant changes in spectral components of HRV when shifting from ACMV to PSV in all the patients. However, the HRV components (HF, LF, and TP) decreased significantly in the failure group while shifting from PSV to SBT, but not in the success group.

Change of the HF Component of HRV During Weaning
The HF component of HRV reflects the vagal outflow to the sinus node of the heart. It is increased in humans by cold stimulation of the face, rotational stimuli, and controlled respiration, which all increase vagal activity,1 3 9 and is reduced during mild-to-moderate intensity of exercise because of vagal withdrawal.5 6 Controlled respiration at frequencies within the resting physiologic range provides a convenient tool to enhance the vagal modulation of the heart rate, probably achieved through the synchronization of all respiratory components.9 A controlled f of 16 breaths/min (approximately 0.27 Hz) could result in a peak spectrum in the HF region (0.15 to 0.4 Hz). If the frequency of controlled breathing is decreased enough to approach LF rhythm, the two components merge into one more powerful oscillation.9

There are two reasons for the reduced HF component in the failure group. First, the intense sympathoadrenal stimulation during weaning from mechanical ventilation could result in the withdrawal of parasympathetic nervous system activity.5 6 12 13 Second, the HF component of HRV decreases with increased respiratory rate and decreased VT.7 8 During the shift from ACMV to SBT, the f in the failure group increased more than that in the success group (from 16.7 ± 1.6 to 29.6 ± 7.3 breaths/min vs from 16.5 ± 0.9 to 23.7 ± 4.7 breaths/min, p < 0.05), and spontaneous VT was significantly lower (281.6 ± 109.0 mL vs 411.3 ± 120.5 mL, p < 0.05). Consequently, the increased f coupled with a reduced VT, which is equivalent to a higher f/VT ratio,19 22 would result in a greater decrease in the HF power in the failure group.

Change of the LF Component of HRV During Weaning
In contrast to the HF component, there has been disagreement in the literature regarding the interpretation of the LF component.2 3 4 5 6 9 In resting dogs, Akselrod et al2 demonstrated that increasing the activity of either the sympathetic or parasympathetic nervous system augments the LF component. In healthy subjects, an increased LF component is observed during sympathetic activation in various conditions, such as standing, passive tilt, mental stress, and moderate exercise.3 9 However, in resting humans receiving cardiac sympathetic blockade by segmental epidural anesthesia (C6-T6), Hopf et al4 found that the LF component did not change significantly. Besides, in some conditions associated with sympathetic excitation such as heavy exercise, a decrease in the absolute power of the LF component is observed.3 4 5 6 It is not clear whether the results have been due to differences in design of the studies and methodologic factors or if HRV analysis is not applicable to this situation because of enhanced respiratory activity and increased movement during exercise.5 8 9

Because sympathoadrenal stimulation is intense during weaning from mechanical ventilation,12 13 one might expect an increase in the LF component if it is solely a marker of sympathetic modulation.3 In an animal study, Frazier et al17 noted a significant increase of very LF power (0.0033 to < 0.04 Hz) with exposure to PSV plus continuous positive airway pressure, but there was no change in the LF component. Though the authors considered the very LF power as an index of sympathetic activity, it is suggested to be a dubious measure and should be avoided when assessed from short-term recordings (<= 5 min).3 In our study, the LF power in the failure group decreased from ACMV to SBT. Our result is similar to the human study by Polanczyk et al,5 who observed a marked reduction in all components of HRV during exercise with the peak heart rate of 86% of maximum, and there was also no significant change in the LF/HF ratio. Therefore, the concept of the LF component as a marker of cardiac sympathetic modulation is debatable.4 5 6 Whether the decrease in the LF component during weaning is due to respiratory-autonomic interactions, the pathologic processes of sympathetic modulation of heart beat fluctuations in patients recovering from respiratory failure, or the influence of underlying diseases and medications is indeterminate.

Influences of Medications and Underlying Diseases on HRV
Many medications act directly or indirectly on the autonomic nervous system, but the data about pharmacologic effects of HRV are limited to a few patient populations.1 3 20 23 24 25 The acute effects of an inhaled selective ß-adrenoreceptor agonist on HRV are decreases in total variability, LF and HF components, and an increase in LF/HF ratio.25 Since the prescriptions of the nebulized ß-agonists were common in patients receiving mechanical ventilation, approximately 60% of this study, the decrease of HRV might also be influenced. In both groups, we found that there was no difference in uses of various medications known to be able to affect HRV. Therefore, the significant decrease of HRV in the failure group, but not in the success group, cannot be explained by the effects of medications.

In addition, age, gender,26 and some diseases, such as diabetes mellitus,1 3 congestive heart failure,1 3 20 and various neurologic diseases,3 have been shown to have influences on HRV. Since all the measures in this study were performed within hours of the patients meeting the general weaning criteria, the influences of these factors between the two groups could be removed when comparing the spectral changes of HRV by paired t test among the three phases.

Limitations, Clinical Applications, and Future Research
There are some limitations in this study. First, the sample size is small. Second, we did not collect the other data of the autonomic nervous system, such as plasma catecholamine levels, muscle sympathetic nerve traffic, and baroreflex sensitivity. Third, although pneumonia (21 of 24 patients, 87.5%) was the most common cause of respiratory failure in this study, a mixed patient population with various underlying diseases was included and the weaning process before SBT was not standardized, both of which might have had considerable effects on the weaning outcome. Fourth, despite statistical significance, the change of HRV during weaning (approximately 2.5 to 2.7% in logarithm unit, ie, 14% in absolute unit, between ACMV and SBT in the failure group) is relatively small from an operational point of view. Finally, because of the inherited limitation of HRV analysis,1 3 the application as a weaning parameter is limited to those without significant arrhythmias.

Nonetheless, an automatically derived weaning predictor in a busy intensive care setting would be an attractive one, and commercial equipment designed to measure HRV is available.3 To predict weaning outcome by the changes of HRV indexes as a stress response test among different levels of ventilator support, further study in a larger population to define the most useful method of HRV analysis during ventilator weaning is needed.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
The spectral components, including HF, LF, and TP of HRV, decreased significantly in the failure group during the shift from ACMV, PSV, to SBT. The reduced HF component is consistent with a higher f/VT ratio, and vagal withdrawal of the autonomic nervous system in patients with weaning failure. The finding of a reduced LF component during weaning does not support the concept of the LF component of HRV as a marker of cardiac sympathetic modulation. The changes of the HRV components may be a potential tool of automatically gathered parameter during ventilator weaning.


   Acknowledgements
 
The authors thank respiratory therapists Chao-Ling Wu, Chin-Yu Chiu, Jai-Jane Jerng, Shu-Ying Liu, Been-Ying Liu, Chun-Meei Lin, and Yu-Chan Lee, and the nurses in the ICU for their assistance.


   Footnotes
 
Abbreviations: ACMV = assist/control mandatory ventilation; APACHE = acute physiology and chronic health evaluation; f = respiratory rate; FIO2 = fraction of inspired oxygen; HF = high frequency; HR = heart rate; HRV = heart rate variability; LF = low frequency; NU = normalized unit; PEEP = positive end-expiratory pressure; PSV = pressure support ventilation; SBT = spontaneous breathing trial; TP = total power; E = minute ventilation; VT = tidal volume

Received for publication February 27, 2002. Accepted for publication July 26, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

  1. van Ravenswaaij-Arts, C, Kollee, L, Hopman, J, et al (1993) Heart rate variability. Ann Intern Med 118,436-447[Abstract/Free Full Text]
  2. Akselrod, S, Gordon, D, Ubel, FA, et al Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science 1981;213,220-222[Abstract/Free Full Text]
  3. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Circulation 1996;93,1043-1065[Free Full Text]
  4. Hopf, H-B, Skyschally, A, Heusch, G, et al Low-frequency spectral power of heart rate variability is not a specific marker of cardiac sympathetic modulation. Anesthesiology 1995;82,609-619[CrossRef][ISI][Medline]
  5. Polanczyk, CA, Rohde, LEP, Moraes, RS, et al Sympathetic nervous system representation in time and frequency domain indices of heart rate variability. Eur J Appl Physiol 1998;79,69-73[CrossRef]
  6. Houle, MS, Billman, GE Low-frequency component of the heart rate variability spectrum: a poor marker of sympathetic activity. Am J Physiol 1999;276,H215-H223
  7. Hayano, J, Mukai, S, Sakakibara, M, et al Effects of respiratory interval on vagal modulation of heart rate. Am J Physiol 1994;267,H33-H40
  8. De Meersman, RE, Reisman, SS, Daum, M, et al Influence of respiration on metabolic, hemodynamic, psychometric, and R-R interval power spectral parameters. Am J Physiol 1995;269,H1437-H1440
  9. Malliani, A, Pagani, M, Lombardi, F, et al Cardiovascular neural regulation explored in the frequency domain. Circulation 1991;84,1482-1492
  10. Pinsky, MR Breathing as exercise: the cardiovascular response to weaning from mechanical ventilation. Intensive Care Med 2000;26,1164-1166[CrossRef][ISI][Medline]
  11. De Backer, D, El Haddad, P, Preiser, JC, et al Hemodynamic responses to successful weaning from mechanical ventilation after cardiovascular surgery. Intensive Care Med 2000;26,1201-1206[CrossRef][ISI][Medline]
  12. Kennedy, SK, Weintraub, RM, Skillman, JJ Cardiorespiratory and sympathoadrenal responses during weaning from controlled ventilation. Surgery 1977;82,233-240[ISI][Medline]
  13. Oh, TE, Bhatt, S, Lin, ES, et al Plasma catecholamines and oxygen consumption during weaning from mechanical ventilation. Intensive Care Med 1991;17,199-203[CrossRef][ISI][Medline]
  14. Äärimaa, T, Oja, R, Antila, K, et al Interaction of heart rate and respiration in newborn babies. Pediatr Res 1998;24,745-750
  15. Kero, P, Antila, K, Ylitalo, V, et al Decreased heart rate variation in decerebration syndrome: quantitative clinical criterion of brain death? Pediatrics 1978;62,307-311[Abstract/Free Full Text]
  16. Koh, J, Brown, TE, Beightol, LA, et al Contribution of tidal lung inflation to R-R interval and arterial pressure fluctuations. J Auton Nerv Syst 1998;68,89-95[CrossRef][ISI][Medline]
  17. Frazier, SK, Moser, DK, Stone, KS Heart rate variability and hemodynamic alterations in canines with normal cardiac function during exposure to pressure support, continuous positive airway pressure, and a combination of pressure support and continuous positive airway pressure. Biol Res Nurs 2001;2,167-174[Abstract/Free Full Text]
  18. Epstein, SK Weaning parameters. Respir Care Clin N Am 2000;6,253-301[CrossRef][Medline]
  19. Yang, KL, Tobin, MJ A prospective study of indexes predicting the outcome of trials of weaning from mechanical ventilation. N Engl J Med 1991;324,1445-1450[Abstract]
  20. Lin, LY, Lin, JL, Du, CC, et al Reversal of deteriorated fractal behavior of heart rate variability by ß-blocker therapy in patients with advanced congestive heart failure. J Cardiovasc Electrophysiol 2001;12,26-32[CrossRef][ISI][Medline]
  21. Welch, PD The use of fast Fourier transform for the estimation of power spectra: a method based on time averaging over short, modified periodograms. IEEE Trans Audio Electroacoust 1967;AU-15,70-73[CrossRef]
  22. Tobin, MJ, Perez, W, Guenther, SM, et al The pattern of breathing during successful and unsuccessful trials of weaning from mechanical ventilation. Am Rev Respir Dis 1986;134,1111-1118[ISI][Medline]
  23. Cook, JR, Bigger, JT, Jr, Kleiger, RE, et al Effect of atenolol and diltiazem on heart period variability in normal persons. J Am Coll Cardiol 1991;17,480-484[Abstract]
  24. Bekheit, S, Tangella, M, el-Sakr, A, et al Use of heart rate spectral analysis to study the effects of calcium channel blockers on sympathetic activity after myocardial infarction. Am Heart J 1990;119,79-85[CrossRef][ISI][Medline]
  25. Jartti, T, Kaila, T, Tahvanainen, K, et al The acute effects of inhaled salbutamol on the beat-to-beat variability of heart rate and blood pressure assessed by spectral analysis. Br J Clin Pharmcol 1997;43,421-428[CrossRef][ISI][Medline]
  26. Ryan, SM, Goldberger, AL, Pincus, SM, et al Gender-, and age-related differences in heart rate dynamics: are women more complex than men? J Am Coll Cardiol 1994;24,1700-1707[Abstract]




This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via ISI Web of Science (4)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Shen, H.-N.
Right arrow Articles by Yang, P.-C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shen, H.-N.
Right arrow Articles by Yang, P.-C.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS