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Heart Rate Variability: Clinical Insights

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Heart Rate Variability: Clinical Insights

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ryan9985
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© All Rights Reserved
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REVIEW ARTICLE Rev Bras Cir Cardiovasc 2009; 24(2): 205-217

Basic notions of heart rate variability and its


clinical applicability
Noções básicas de variabilidade da frequência cardíaca e sua aplicabilidade clínica

Luiz Carlos Marques VANDERLEI1, Carlos Marcelo PASTRE1, Rosângela Akemi HOSHI2, Tatiana Dias de
CARVALHO2, Moacir Fernandes de GODOY3

RBCCV 44205-1078

Abstract in the HRV analyses, limitations in the use and clinical


Autonomic nervous system (ANS) plays an important applications of the HRV.
role in the regulation of the physiological processes of the
human organism during normal and pathological conditions. Descriptors: Autonomic nervous system. Heart rate.
Among the techniques used in its evaluation, the heart rate Parasympathetic nervous system. Sympathetic nervous
variability (HRV) has arising as a simple and non-invasive system.
measure of the autonomic impulses, representing one of
the most promising quantitative markers of the autonomic
balance. The HRV describes the oscillations in the interval Resumo
between consecutive heart beats (RR interval), as well as O sistema nervoso autônomo (SNA) desempenha um
the oscillations between consecutive instantaneous heart papel importante na regulação dos processos fisiológicos do
rates. It is a measure that can be used to assess the ANS organismo humano tanto em condições normais quanto
modulation under physiological conditions, such as patológicas. Dentre as técnicas utilizadas para sua avaliação,
wakefulness and sleep conditions, different body positions, a variabilidade da frequência cardíaca (VFC) tem emergido
physical training and also pathological conditions. Changes como uma medida simples e não-invasiva dos impulsos
in the HRV patterns provide a sensible and advanced autonômicos, representando um dos mais promissores
indicator of health involvements. Higher HRV is a signal of marcadores quantitativos do balanço autonômico. A VFC
good adaptation and characterizes a health person with descreve as oscilações no intervalo entre batimentos
efficient autonomic mechanisms, while lower HRV is cardíacos consecutivos (intervalos R-R), assim como
frequently an indicator of abnormal and insufficient oscilações entre frequências cardíacas instantâneas
adaptation of the ANS, provoking poor patient’s physiological consecutivas. Trata-se de uma medida que pode ser utilizada
function. Because of its importance as a marker that reflects para avaliar a modulação do SNA sob condições fisiológicas,
the autonomic nervous system activity on the sinus node tais como em situações de vigília e sono, diferentes posições
and as a clinical instrument to assess and identify health do corpo, treinamento físico, e também em condições
involvements, this study reviews conceptual aspects of the patológicas. Mudanças nos padrões da VFC fornecem um
HRV, measurement devices, filtering methods, indexes used indicador sensível e antecipado de comprometimentos na

1. PhD, Assistant Professor at the Faculty of Health and Technology This study was carried out at the Faculty of Health and Technology
– FCT/UNESP – Presidente Prudente – São Paulo, Physiotherapy – FCT/UNESP – Presidente Prudente – São Paulo, SP, Brazil and São
Department. José do Rio Preto Medical School – FAMERP – São José do Rio
2. Graduation in Physiotherapy; Master’s Degree Student of the Preto, SP, Brazil.
Stricto Sensu Postgraduation Course in Physiotherapy - Faculty
of Health and Technology – FCT/UNESP – Presidente Prudente Correspondence address:
– São Paulo, Physiotherapy Department. Luiz Carlos Marques Vanderlei. Rua Bela Vista, 822 - Cidade Jardim -
3. Full Professor of the São José do Rio Preto Medical School – Presidente Prudente, SP, Brazil. CEP 19023-440.
FAMERP – São José do Rio Preto – São Paulo, Cardiology and E-mail: vanderle@[Link]
Cardiovascular Surgery Department.
Article received on September 12th, 2008
Article accepted on May 12th, 2009

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VANDERLEI, LCM ET AL - Basic notions of heart rate variability Rev Bras Cir Cardiovasc 2009; 24(2): 205-217
and its clinical applicability

saúde. Uma alta variabilidade na frequência cardíaca é sinal artigo revisa aspectos conceituais da VFC, dispositivos de
de boa adaptação, caracterizando um indivíduo saudável, com mensuração, métodos de filtragem, índices utilizados para
mecanismos autonômicos eficientes, enquanto que, baixa análise da VFC, limitações de utilização e aplicações clínicas
variabilidade é frequentemente um indicador de adaptação da VFC.
anormal e insuficiente do SNA, implicando a presença de
mau funcionamento fisiológico no indivíduo. Diante da sua Descritores: Sistema nervoso autônomo. Frequência
importância como um marcador que reflete a atividade do cardíaca. Sistema nervoso parassimpático. Sistema nervoso
SNA sobre o nódulo sinusal e como uma ferramenta clínica simpático.
para avaliar e identificar comprometimentos na saúde, este

INTRODUCTION individuals, athletes and patients with diseases [1,9,10].


Figure 1 shows rate tachogram obtained from the RR
The control of the cardiovascular system is intervals of a normal young adult and a normal newborn. It
accomplished in part by the autonomic nervous system is observed that the HRV is much smaller in the newborn.
(ANS), which provides afferent and efferent nerves to the HRV has been studied for several years, with an
heart, in the form of sympathetic terminations throughout increasing interest in understanding its mechanisms and
the myocardium and parasympathetic to the sinus node, its clinical utility in diseases. Historically, its clinical interest
atrial myocardium and atrioventricular node [1]. emerged in 1965 when Hon and Lee showed a well-defined
The influence of the ANS on the heart is dependent on clinical application of HRV in the monitoring area of fetal
informations from baroreceptors, chemoreceptors, atrial distress. In 1977, Wolf et al. showed an association between
receptors, ventricular receptors, changes on the respiratory decreased HRV and increased risk of mortality after acute
system, vasomotor system, the renin-angiotensin- myocardial infarction, and Kleiger et al. in 1987, confirmed
aldosterone system and the thermoregulatory system, that HRV was a powerful and independent predictor of
among others [2,3]. mortality after acute myocardial infarction [11].
This neural control is closely linked to heart rate (HR)
and baroreceptor reflex activity [1]. From the afferent
informations, by means of a complex interaction between
stimulation and inhibition, the responses from sympathetic
and parasympathetic pathways are formulated and modify
the HR, by adapting to the needs of each moment.
The increase in HR is consequence of increased action
of the sympathetic pathway and reduced parasympathetic
activity, or that is, vagal inhibition, whereas its reduction
depends mainly on the predominance of vagal activity
[1,4,5].
Fig. 1 - Tachogram of a normal young adult (A) and a normal
The heart is not a metronome and its beats do not have newborn (B). The heart rate variability in panel B is much smaller
the regularity of a clock, so changes in HR, defined as heart than in panel A.
rate variability (HRV), are normal and expected and indicate
the heart’s ability to respond to multiple physiological and
environment stimuli, among them, breathing, physical
exercise, mental stress, hemodynamic and metabolic Changes in patterns of HRV provides a sensitive and
changes, sleep and orthostatism, as well as to compensate early indicator of health impairments. High HRV is a sign of
disorders induced by diseases [1,4,6-8]. good adaptation, by characterizing a healthy individual with
In general, HRV describes the oscillation of the intervals efficient autonomic mechanisms. Conversely, low HRV is
between consecutive heart beats (RR intervals), which are often an indicator of abnormal and inadequate adaptation
related to the influences of the ANS on the sinus node, of the ANS, which may indicate the presence of
being a noninvasive measurement that can be used to physiological malfunction in the patient, requiring further
identify phenomena related to the ANS in healthy investigations in order to find a specific diagnosis [10].

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VANDERLEI, LCM ET AL - Basic notions of heart rate variability Rev Bras Cir Cardiovasc 2009; 24(2): 205-217
and its clinical applicability

The wide possibility of use and ease of data FILTERING METHODS


acquisition characterize this resource. One should also
highlight that the disclosure of current information The presence of premature ectopic beats or artifacts
regarding the HRV, such as concepts, analysis models, interfere with the analysis of HRV, compromising the
forms of interpreting results and clinical applicability, is reliability of the indexes obtained, if they were not removed
an aid to both researchers and clinicians who work in [21-23]. Filtering methods are able to detect abnormal RR
various areas of health. Thus, in order to insert elements intervals and correct them [24].
in the literature relating to an easy-to-use, comprehensive Most of the texts selected for the preparation of this
and non-invasive technique, it was considered appropriate manuscript does not approach detaily the procedures
to undertake research on the subject. adopted for filtering. However, despite the lack of
information, some authors describe the methodology
MEASUREMENT DEVICES used.
In the study of Thuraisingham [22], the method adopted
The cardiac excitation begins with an impulse generated to remove the artifacts was a impulse rejection filter that
in the sinus node, which is distributed through the atria, was effective for this purpose. Godoy et al. [23] used the
resulting in atrial depolarization, which is represented on Polar S810 for the collection of RR intervals and performed
the electrocardiogram (ECG) by the P wave. This impulse is filtering in two stages, one digital by means of the
conducted to the ventricles through the atrioventricular equipment’s software and other manual, characterized by
node and distributed by the Purkinje fibers, resulting in visual inspection of the RR intervals and excluding abnormal
depolarization of the ventricles, which is represented on intervals. In this study, only series with more than 95% of
the ECG by the Q, R and S waves, forming the QRS complex. sinus beats were included.
Ventricular repolarization is represented by the T wave [12].
The HRV indexes are obtained by analyzing the intervals INDEXES OF HEART RATE VARIABILITY
between R waves, which can be captured by instruments
such as electrocardiographer, digital-to-analog converter For the HRV analysis, indexes obtained by linear
and the cardio-frequency meter, from external sensors methods, time and frequency domain, and nonlinear
placed at specific points of the body [1,4]. methods can be used [1].
One of the digital-to-analog converter available is the
Powerlab, an instrument used for biosignal multimodal Linear Methods
monitoring, considered the gold standard for high-fidelity The linear methods are divided into two types: time
ECG measuring, whose signals captured are transferred to domain analysis, performed by statistical and geometric
a computer, saved and analyzed after filtering [13]. indexes, and frequency domain analysis.
The ECG and analog-to-digital converter used for HRV For the HRV time domain analysis, thus named for
analysis, make difficult the applicability in situations outside expressing the results in unit time (milliseconds), every
the laboratory environment, such as on physical training normal RR intervals (sinus beats) is measured during a
conditions, in addition to present a high cost [14-16]. determined time interval and, thereafter, based on statistical
The cardio-frequency meters have solved these or geometric methods (mean, standard deviation and
problems, since such devices are more accessible both in histogram-derived indexes or the Cartesian coordinates map
respect to cost and practicality [17]. A model with such of the RR intervals), it is calculated the translator indexes
characteristics is the frequency meter Polar S810 that, of fluctuations during the cardiac cycles [9.25].
according Kingsley et al. [15], showed good accuracy in The statistical indexes in the time domain, obtained by
the records in low-intensity exercise, when compared to the determination of the RR intervals corresponding to any
the outpatient electrocardiogram, which was also observed point in time, are [1,10,26-29]:
by Gamelin et al. [14] in a study comparing the data obtained a) SDNN - Standard deviation of all normal RR intervals
by ECG and the Polar S810, both in situations of exercise recorded in a time interval, expressed in ms;
and rest. b) SDANN – Represents the standard deviation of the
In this device, a belt with electrodes positioned in the normal RR intervals means, every 5 minutes in a time
chest of the patient, captures the heart’s electrical impulses interval, expressed in ms;
and transmits them through an electromagnetic field to the c) SDNNi – It is the mean of the standard deviation of
monitor. The signal captured is sent by an interface to the normal RR intervals every 5 minutes, expressed in ms;
Polar Precision Performance software. In this equipment, d) rMSSD - is the root-mean square of differences
the units of time are fixed at 1ms and the samples of RR between adjacent normal RR intervals in a time interval,
intervals are collected at a frequency of 1000 Hz [1,18-21]. expressed in ms;

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and its clinical applicability

e) pNN50 - Represents the percentage of adjacent RR


intervals with a difference of duration greater than 50ms.
The SDNN, SDANN and SDNNi are obtained from long-
term records and represent the sympathetic and
parasympathetic activity, but they do not allow to
distinguish when changes in HRV are due to increased
sympathetic tone or the withdrawal of vagal tone [28.29 ].
The rMSSD and pNN50 indexes represent the
parasympathetic activity [1,10,26,27] as they are found from
the analysis of adjacent RR intervals [25].
Another possibility to process RR intervals in time
domain is from geometrical methods, whereas the triangular
index and Lorenz plot (or Poincaré Plot) are the most known.
The geometric methods present RR intervals in geometric
patterns and several approaches are used to derive
measures of HRV from them [1,4].
The triangular index is calculated based on the
construction of a density histogram of normal RR intervals,
which shows on the horizontal axis (x axis), the length of
RR intervals and the vertical axis (y axis), the frequency on
which each interval occurred. The junction of the points of
the histogram columns forms a triangle-shaped figure and
the width of the base of the triangle expresses the variability
of RR intervals. The triangular index (corresponding to the
base of the triangle) can be calculated by dividing the area
(corresponding to the total number of RR intervals used to
construct the figure) and height (corresponding to the
number of RR intervals with modal frequency) of the triangle
[4, 25,30].
This index has a close correlation with the standard
deviation of all RR intervals and does not suffer the
influence of ectopic beats and artifacts, as these are located
outside the triangle [4].
The Poincaré plot is a geometric method for dynamic
analysis of HRV, which represents a temporal series within
a Cartesian plane in which each RR interval is correlated
with the preceding interval and define a point in the plot
[17,31-34]. Figure 2 shows the Poincaré plot of a normal
young adult and a normal newborn. Fig. 2 – Poincaré chart of a normal young adult (A) and a normal
The analysis of Poincaré plot can be performed in a newborn (B). The dispersion of both short- (SD1) and long-term
qualitative manner (visual), by assessing the figure formed in panel B (SD2) is smaller than in panel A
by its attractor, which is useful for showing the degree of
complexity of RR intervals [35], or quantitative, by
adjusting the ellipse of the figure formed by the attractor,
from which three indexes can be obtained: SD1, SD2 and
SD1/SD2 ratio [17].
SD1 represents the dispersion of points perpendicular The qualitative analysis (visual) of the Poincaré plot is
to the line of identity and it seems to be an index of performed through the analysis of the figures formed by
instantaneous recording of beat-to-beat variability; the SD2 the plot attractor, which were described by Tulppo et al.
represents the dispersion of points along the line of identity [36] who classified them as follows:
and represents the HRV in long-term records; the 1) Comet-shaped figure, on which an increase in the
relationship of both (SD1/SD2) shows the ratio between dispersion of beat-to-beat RR intervals is observed with
the short- and long-term variations of the RR intervals [4.14]. increase in RR intervals, characteristic of a normal plot;

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and its clinical applicability

2) Torpedo-shaped figure, with a small global beat-to- Frequency - ULF) - Indexes less used whose physiological
beat dispersion (SD1) and without increasing the long-term explanation is not well established and seems to be related
dispersion of RR intervals; to the renin-angiotensin-aldosterone system,
3) Complex or parabolic figure, on which two or more thermoregulation and the peripheral vasomotor tone [23.29].
distinct ends are separated from the main body of the plot, The LF/HF ratio reflects the absolute and relative
with at least three points included in each end. changes between the sympathetic and parasympathetic
components of the ANS, by characterizing the sympathetic-
vagal balance on heart [29].
To obtain the spectral indexes, the frequency tachogram
undergoes mathematical processing, generating a
tachogram, graph that expresses the variation of RR
intervals as a function of time. The tachogram contains a
signal apparently periodic that varies in time and is
processed by mathematical algorithms, such as Fast Fourier
Transform (FFT) or autoregressive models (AR) [1].
The FFT method is used to obtain an estimate of power
spectral HRV during stationary studies. It also allows that
the tachogram signal be recovered even after processing
by the FFT, which demonstrates the objectivity of the
technique, since informations are not lost during the
process. The ease of application of this method and good
layout are the main reasons for its widespread use [1].
In the AR model, the parameters estimation can be
performed easily by solving linear equations. Thus, the
spectral components can be distinguished regardless of
preset frequency bands and power contained in the peaks
can be calculated without the need of predefined spectral
Fig. 3 - Spectral analysis of frequencies (Fast Fourier Transform)
bands [1.43].
of a normal young adult (A) and a normal newborn (B). The high
frequency (HF) component is proportionally smaller in the newborn Normalizing data of the spectral analysis can be used to
(arrows) as well as the total power minimize the effects of changes in the VLF band. This is
determined by dividing the power of a given component
(LF or HF) by the total power spectrum, minus the VLF
component and multiplied by 100 [9,44,45].
For analysis of the HRV indexes using linear and multiple
methods, softwares can be used, among them the HRV
analysis software [28], which can be downloaded free over
Another linear method is the frequency domain, whereas the Internet.
the spectral power density is the most widely used, when it
deals with studies with individuals at rest [17]. Examples of Nonlinear methods
the frequency domain analysis can be seen in Figure 3. The nonlinear behavior is predominant in human
This analysis decomposes the HRV in fundamental systems, because of its dynamic nature complex, which
oscillatory components, whereas the main ones are can not be described properly by linear methods. Chaos
[4,7,23,29,37-42]: theory describes elements manifesting behaviors that are
a) High-frequency component (High Frequency - HF), extremely sensitive to initial conditions, and they are difficult
ranging from 0.15 to 0.4 Hz, which corresponds to the to repeat, but nonetheless are deterministic elements [23].
respiratory modulation and is an indicator of the The theories of nonlinear systems have been
performance of the vagus nerve on the heart; progressively applied to interpret, explain and predict the
b) Low frequency component (Low Frequency - LF), behavior of biological phenomena. These parameters have
ranging between 0.04 and 0.15 Hz, which is due to the joint proved to be good predictors of morbidity and mortality in
action of the vagal and sympathetic components on the the clinical sphere, despite the need for scientific deepening,
heart, with a predominance of the sympathetic ones; with expressive samples and prolonged follow-up. Such
c) Components of very low frequency (Very Low studies may be useful in research and treatment of heart
Frequency - VLF) and ultra-low frequency (Ultra Low disease [23].

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VANDERLEI, LCM ET AL - Basic notions of heart rate variability Rev Bras Cir Cardiovasc 2009; 24(2): 205-217
and its clinical applicability

Among the nonlinear methods used for HRV analysis, obstructive sleep apnea [74], epilepsy [75], headache [76],
we can mention: detrended fluctuation analysis, correlation among others.
function, Hurst exponent, fractal dimension and Lyapunov A reduced HRV has been identified as a strong indicator
exponent [4,23,29]. of risk related to adverse events in healthy individuals and
The records for analysis of HRV indexes by linear patients with a large number of diseases, reflecting the vital
methods can be obtained in short periods (2, 5, 15 minutes) role that ANS plays in maintaining health [10].
or long periods (24 hours), which is more common in clinical In diseases such as hypertension [29,59-61], acute
practice [25], whereas a minimum of 256 RR intervals is myocardial infarction, coronary artery disease [29] and
recommended for this analysis [7,9]. Seiler et al. [18], Brown atherosclerosis [56], HRV indexes are reduced. Menezes Jr
& Brown [46] and Parekh & Lee [47] in their experiments for et al. [60] found reduced HRV in hypertensive compared to
analysis of linear indexes, dismissed the initial periods of normotensive patients, when analyzing the SDNN, RMSSD,
capture, on which many oscillations occur and the system pNN50, HF, LF, LF/HF, probably due to a sympathetic
is not in a stability state. hyperactivity. Decreased post-AMI HRV was also reported
For analysis of the indexes in the chaos domain, a larger by several studies, as presented by Pecyna [63] in a review
number of RR intervals is recommended. Godoy et al. [23] article.
used a quantity of 1000 consecutive RR intervals for In hypertrophic cardiomyopathy, it is assumed that
analysis. the neuronal uptake of norepinephrine is impaired due to
a decrease in the density of beta receptors [26]. Studies
LIMITATIONS ON USE using HRV indexes in cardiovascular diseases can be seen
in Table 1.
In addition to factors such as ectopic beats and The assessment of HRV has also been widely used in
artifacts [22], other conditions such as heart transplants, order to diagnose both physiological and psychological
presence of arrhythmias and pacemakers produce disorders [77]. In sports medicine, for example, is generally
inappropriate RR intervals to assess HRV, by limiting the used to assess adaptations related to resistance training
use of this tool under these conditions. In transplant [78] and exercise [17-19,29,38].
patients, control of the denervated heart is performed The difference in HRV between trained and untrained
based on the venous return, atrial receptor stimulation, individuals has been widely investigated. Both variables
atrial stretch and hormones and other substances in the in the time domain and frequency domain are higher in
circulatory system [48-51], suggesting that HRV analysis trained individuals compared to sedentary ones, indicating
does not represent the modulation of the heart by the that HRV is higher in these individuals [16].
ANS. The regular practice of physical activity has been
Artificial cardiac pacemakers are electronic devices of reported as a factor in increased vagal tone due to
multiprogrammable stimulation that can replace electrical physiological adaptations that have occurred by the
impulses and/or ectopic rhythms, to obtain the cardiac increase in cardiac work, since there is a decreased
electrical activity as physiological as possible [52]. Since sensitivity of beta receptors [29]. Thus, the increase in
patients with pacemakers may have their heart rate parasympathetic modulation induces an electrical stability
modulated by such equipments, the analysis of HRV will of the heart, while the high sympathetic activity increases
not also reflect the autonomic modulation of the heart, the vulnerability of the heart and the risk of cardiovascular
limiting its use under this condition. events [17].
Condition also restricted the analysis of HRV is the Novais et al. [29] assessing the RMSSD, VLF, LF, HF,
presence of atrioventricular block because the impulse is found no significant differences at rest between healthy
not conducted properly to the ventricle, avoiding an sedentary men and active patients with AH and AMI,
analysis of RR intervals [53]. suggesting the effect of physical activity on autonomic
modulation of these patients. This effect has also been
CLINICAL APPLICATIONS proposed by Takahashi et al. [55], when analyzing the
RMSSD index at rest in active coronary artery disease
Currently, the HRV indexes have been used to patients and healthy individuals, in which significant
understand various conditions, such as coronary artery differences were also not found.
disease [54-57], cardiomyopathy [26.58], arterial Moreover, these indexes also allow verification of the
hypertension [29,59-61], myocardial infarction [62-64 ], influence of factors such as age [4,7,37,79,80], gender [81-
sudden death [65], chronic obstructive pulmonary disease 83] and exercise [17-19,29,38] on the autonomic control.
[2,66,67], renal failure [68], heart failure [69], diabetes [70], Table 2 shows studies using HRV in various physiological
stroke [71], Alzheimer’s disease [72] leukemia [73], and pathological conditions.

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and its clinical applicability

Table 1. Studies using comparatively the HRV in heart diseases.

Authors Year Disease Assessed Conclusions


indexes
Reis et al. [64] 1998 AMI Review Aticle The positive predictive power of
noninvasive methods is usually low, supporting
the use of other resources
in the stratification of post-AMI

Carnethon et al. [56] 2002 CAD SDNN, HF HRV can be used to identify
differences in cardiac autonomic
balance in healthy adults

Novais et al. [29] 2004 AH RMSSD, VLF, LF, HF No differences at rest between healthy and
active individuals with AMI and AH

Menezes et al. [60] 2004 AH SDNN, RMSSD, pNN50, HRV is decreased in hypertensive patients
HF, LF, LF/HF when compared to normotensive ones

Terathongkum et al. [61] 2004 AH Review Article Decreased HRV is an independent predictor of
arterial hypertension in the patients

Takahashi et al. [55] 2005 CAD RMSSD There were no significant differences in HRV
indexes in healthy sedentary and active
coronary artery disease men

Bittencourt et al. [26] 2005 HC RMSSD, pNN50, HF There was a significant increase in parasympathetic
modulation during controlled breathing associated
with the tilt test in the patients

Pecyna [63] 2006 AMI Indexes in time and HRV is decreased


frequency domain in post-AMI patients

Carney et al. [54] 2007 CAD HF, LF, VLF Moderate correlation was found between
inflammatory factors and HRV in depressed
coronary artery disease patients

Limongelli et al. [58] 2007 HC SDNN, pNN50, RMSSD, The main clinical implication is the predictive
LF, HF, LF/HF value of HRV in risk stratification of children
and young patients with HC

Karas et al. [59] 2008 AH LF,HF,LF/HF There was a reduction of hemodynamic


responses (SAP and DAP) and sympathetic
(LF) of elderly hypertensive

Larosa et al. [62] 2008 AMI SDNN, frequency domain HRV is decreased in patients with AMI

AMI: Acute myocardial infarction; CAD: Coronary artery disease; AH: Arterial hypertension; HC: Hypertrophic cardiomyopathy; HRV:
Heart rate variability; SAP: Systolic arterial pressure; DAP: Diastolic arterial pressure

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and its clinical applicability

Table 2. Studies using comparatively the HRV in various conditions.

Authors Year Condition Assessed Conclusions


indexes
Paschoal et al. [2] 2002 COPD SDNN With the evolution, the patients tend to have
reduced HRV

Javorka et al. [38] 2002 Recovery after SDNN, RMSSD, The cardiodeceleration after exercise is related to
exercise pNN50, LF, HF the immediate recovery, confirming
parasympathetic contribution at this stage

Catai et al.[7] 2002 Aerobic training in LF, HF, LF/HF The vagal predominance during sleep is reduced
young and middle with increasing age. The resting bradycardia induced
age men by active postural maneuver suggests that
adaptation is more related to intrinsic changes in
sinus node than to vagal modulation

Weerapong et al. [41] 2005 Effects of the Review Evidences of an increased parasympathetic activity
sportive massage and HRV. There is an increase of relaxing substances
such as endorphins

Mello et al. [37] 2005 Age and physical RMSSD, LF, HF, Aging reduces HRV. However, regular
activity LF/HF physical activity is likely to affect the vagal
activity in the heart and consequently attenuates
the effects of aging

Paschoal et al. [72] 2006 Different RMSSD, The HRV analysis is an important tool for
age-groups pNN50, LF, HF, investigating the cardiac autonomic function related
LF/HF to increasing age

Sin DD et al. [66] 2007 COPD SDNN, SDANN, Nocturnal application of noninvasive mechanical
RMSSD, TINN ventilation for three months may improve HRV in
patients with stable COPD

Kudaiberdieva et al. [65] 2007 Sudden death Review article The positive predictive value for
sudden cardiac death remains low, requiring a
combination of other markers

Lopes et al. [71] 2007 Age and resistance SDNN, pNN50, Aging causes changes in autonomic
training RMSSD modulation on the sinus node, reducing HRV in
middle-age individuals. The physical training
studied did not change HRV

Neves et al. [73] 2007 Women SDNN, RMSSD, Estrogen therapy seems to attenuate
post-menopause LF, HF, LF/HF the process of HRV reduction with increasing age,
under estrogen promoting a reduction in sympathetic
therapy activity on the heart

Furuland et al. [68] 2008 Renal failure SDNN,LF Chronic renal failure patients not undergoing
dialysis presented reduced HRV

COPD: Chronic obstructive pulmonary disease; HRV: Heart rate variability

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and its clinical applicability

Lopes et al. [79] and Paschoal et al. [80] observed that CONCLUSION
the aging process causes a depletion of vagal tone and
consequent increase in sympathetic activity, therefore older HRV has gained importance today as a technique to
individuals have a lower HRV. In 2006, Rajendra Acharya et explore the ANS, which has an important role in maintaining
al. [4] observed that HRV is lower with age and the variation homeostasis. Its use is diverse and it stands as mentioned
is greater in women. Melo et al. [37] in a study linking the above, as a predictor of the internal functions of the body,
effects of age and exercise showed that exercise training both in normal and pathological conditions. The widest
can mitigate these effects. possible use, the cost-effectiveness in the application of
Ribeiro et al. [82] and Mercuro et al. [83] proposed that the technique and ease of data acquisition makes the HRV
depression of hormone levels of estrogen that occurs during an interesting option for interpretation of the functioning
menopause, may be responsible for the reduction of HRV of the ANS and a promising clinical tool to assess and
in elderly women. However, in a study by Neves et al. [81] identify impairments on health.
greater vagal modulation and lower sympathetic in women
were found when compared to men of similar age, suggesting
that differences related to gender are not just hormone levels
of estrogen.
Despite the widespread use of HRV analysis in
understanding the phenomena involved with the SNA in
normal and pathological conditions, studies related to its
use in clinical practice are still scarce. However, some
studies have shown the great potential that HRV analysis
can have in clinical practice.
Godoy et al. [23], using indexes of HRV in the chaos
domain, showed that these indexes can be used to predict
morbidity and mortality in patients undergoing coronary
artery bypass graft surgery. Patients with HRV indexes
that showed a reduction in chaotic behavior showed
increased rates of morbidity and mortality. The authors REFERENCES
report that analysis of HRV indexes may be a new approach
in clinical practice as prognostic tool in the preoperative 1. Aubert AE, Seps B, Beckers F. Heart rate variability in athletes.
Sports Med. 2003;33(12):889-919.
evaluation of patients undergoing coronary artery bypass
surgery. 2. Paschoal MA, Petrelluzzi KFS, Gonçalves NVO. Estudo
Meyerfeldt et al. [84] assessed whether changes in da variabilidade da frequência cardíaca em pacientes com
HRV could serve as early warning signs of ventricular doença pulmonar obstrutiva crônica. Rev Ciênc Med.
tachycardia and predict ventricular tachycardia of low 2002;11(1):27-37.
or high frequency in patients with implantable
cardioverter-defibrillators. The authors analyzed the time 3. Cooke WH, Cox JF, Diedrich AM, Taylor JA, Beightol LA,
series of RR intervals stored on the device that had Ames JE 4th, et al. Controlled breathing protocols probe human
happened immediately before the onset of fibrillation, autonomic cardiovascular rhythms. Am J Physiol. 1998;274(2
Pt 2):H709-18.
and compared it to a control period without
tachyarrhythmia in 63 patients with chronic congestive 4. Rajendra Acharya U, Paul Joseph K, Kannathal N, Lim CM,
heart failure. The comparison of these series showed Suri JS. Heart rate variability: a review. Med Bio Eng Comput.
that patients presented low HRV before the onset of 2006;44(12):1031-51.
episodes of ventricular tachycardia, which may allow
the construction of devices with algorithms for early 5. Paschoal MA, Petrelluzzi KFS, Gonçalves NVO. Controle
detection of arrhythmias. autonômico cardíaco durante a execução de atividade física
Indexes of HRV have also been used as a tool for dinâmica de baixa intensidade Rev Soc Cardiol. 2003;13(5 supl
prediction of mortality among patients with acute A):1-11.
myocardial infarction and depressed left ventricular
6. Santos MDB, Moraes FR, Marães VRFS, Sakabe DI,
systolic function [85,86] and in the characterization of a Takahashi ACM, Oliveira L, et al. Estudo da arritmia sinusal
large number of morbid conditions, suggesting that the respiratória e da variabilidade da frequência cardíaca de homens
Heart Rate Variability can be a possible marker of jovens e de meia-idade. Rev Soc Cardiol. 2003;13(3 supl
homeostasis loss. A):15-24.

213
VANDERLEI, LCM ET AL - Basic notions of heart rate variability Rev Bras Cir Cardiovasc 2009; 24(2): 205-217
and its clinical applicability

7. Catai AM, Chacon-Mikahil MP, Martinelli FS, Forti VA, Silva from a Wingate test in adolescent males. Med Sci Sports Exerc.
E, Golfetti R, et al. Effects of aerobic exercise training on heart 2006;38(5):875-81.
rate variability during wakefulness and sleep an
cardiorespiratory responses of young an middle-aged healthy 21. Jurca R, Church TS, Morss GM, Jordan AN, Earnest CP.
men. Braz J Med Biol Res. 2002;35(6):741-52. Eight weeks of moderate-intensity exercise training increases
heart rate variability in sedentary postmenopausal women.
8. Caruana-Montaldo B, Gleeson K, Zwillich CW. The control Am Heart J. 2004;147(5):e21.
of breathing in clinical practice. Chest. 2000;117(1):205-25.
22. Thuraisingham RA. Preprocessing RR interval time series for
9. Task Force of the European Society of Cardiology and the North heart rate variability analysis and estimates of standard deviation
American Society of Pacing and Electrophysiology. Heart rate of RR intervals. Comput Methods Programs Biomed.
variability: standards of measurement, physiological interpretation 2006;83(1):78-82.
and clinical use. Circulation. 1996;93(5):1043-65.
23. Godoy MF, Takakura IT, Correa PR. Relevância da análise do
10. Pumprla J, Howorka K, Groves D, Chester M, Nolan J. comportamento dinâmico não-linear (Teoria do Caos) como
Functional assessment of heart rate variability: physiological elemento prognóstico de morbidade e mortalidade em pacientes
basis and practical applications. Int J Cardiol. 2002;84(1):1-14. submetidos à cirurgia de revascularização miocárdica. Arq Ciênc
Saúde. 2005;12(4):167-71.
11. Barros VCV, Brito MR. Estudo da variabilidade da frequência
cardíaca no paciente após infarto agudo do miocárdio. Rev 24. Logier R, De Jonckheere J, Dassonneville A. An efficient
Soc Mineira de Cardiol. [Citado 2005 fev 02]; 5(1). algorithm for R-R intervals series filtering. Conf Proc IEEE
Disponível em: [Link] Eng Med Biol Soc. 2004;6:3937-40.
[Link]?LibDocID=13320&ReturnCatID=14138&action=full
25. Rassi Jr. A. Compreendendo melhor as medidas de análise da
12. James AF, Choisy SC, Hancox JC. Recent advances in variabilidade da frequência cardíaca. J Diag Cardiol. 8 ed., 2000.
understanding sex differences in cardiac repolarization. Prog [Citado 2005 fev 25]. Disponível em: [Link]/
Biophys Mol Biol. 2007;94(3):265-319. jornal-01/tese%[Link]

13. Radespiel-Tröger M, Rauh R, Mahlke C, Gottschalk T, Muck- 26. Bittencourt MI, Barbosa PRB, Drumond Neto C, Bedirian
Weymann M. Agreement of two different methods for R, Barbosa EC, Brasil F, et al. Avaliação da função autonômica
measurement of heart rate variability. Clin Auton Res. na cardiomiopatia hipertrófica. Arq Bras Cardiol.
2003;13(2):99-102. 2005;85(6):388-96.

14. Gamelin FX, Berthoin S, Bosquet L. Validity of the polar 27. Ribeiro JP, Moraes Filho RS. Variabilidade da frequência
S810 heart rate monitor to measure R-R intervals at rest. Med cardíaca como instrumento de investigação do sistema nervoso
Sci Sports Exerc. 2006;38(5):887-93. autônomo. Rev Bras Hipertens. 2005;12(1):14-20.

15. Kingsley M, Lewis MJ, Marson RE. Comparison of polar 28. Niskanen JP, Tarvainen MP, Ranta-Aho PO, Karjalainen PA.
810s and an ambulatory ECG system for RR interval Software for advanced HRV analysis. Comput Methods
measurement during progressive exercise. Int J Sports Med. Programs Biomed. 2004;76(1):73-81.
2005;26(1):39-44.
29. Novais LD, Sakabe DI, Takahashi ACM, Gongora H, Taciro
16. Achten J, Jeukendrup AE. Heart rate monitoring: applications C, Martins LEB, et al. Avaliação da variabilidade da frequência
and limitations. Sports Med. 2003;33(7):518-38. cardíaca em repouso de homens saudáveis sedentários e de
hipertensos e coronariopatas em treinamento físico. Rev Bras
17. Brunetto AF, Roseguini BT, Silva BM, Hirai DM, Guedes DP. Fisioter. 2004;8(3):207-13.
Limiar ventilatório e variabilidade de frequência cardíaca em
adolescentes. Rev Bras Med Esporte. 2005;11(1):22-7. 30. Rocha RM, Albuquerque DC, Albanesi Filho FM. Variabilidade
da frequência cardíaca e ritmo circadiano em pacientes com
18. Seiler S, Haugen O, Kuffel E. Autonomic recovery after exercise angina estável. Rev Socerj. 2005;18(4):429-42.
in trained athletes: intensity and duration effects. Med Sci
Sports Exerc. 2007;39(8):1366-73. 31. Smith AL, Reynolds KJ, Owen H. Correlated Poincaré indices
for measuring heart rate variability. Australas Phys Eng Sci
19. Bosquet L, Gamelin FX, Berthoin S. Is aerobic endurance a Med. 2007;30(4):336-41.
determinant of cardiac autonomic regulation? Eur J Appl
Physiol. 2007;100(3):363-9. 32. Lerma C, Infante O, Pérez-Grovas H, José MV. Poincaré plot
indexes of heart rate variability capture dynamic adaptations
20. Goulopoulou S, Heffernan KS, Fernhall B, Yates G, Baxter- after haemodialysis in chronic renal failure patients. Clin Physiol
Jones AD, Unnithan VB. Heart rate variability during recovery Funct Imaging. 2003;23(2):72-80.

214
VANDERLEI, LCM ET AL - Basic notions of heart rate variability Rev Bras Cir Cardiovasc 2009; 24(2): 205-217
and its clinical applicability

33. Mäkikallio TH, Tapanainen JM, Tulppo MP, Huikuri HV. 46. Brown SJ, Brown JA. Resting and postexercise cardiac
Clinical applicability of heart rate variability analysis by autonomic control in trained masters athletes. J Physiol Sci.
methods based on nonlinear dynamics. Card Electrophysiol 2007;57(1):23-9.
Rev. 2002;6(3):250-5.
47. Parekh A, Lee CM. Heart rate variability after isocaloric exercise
34. Penttilä J, Helminen A, Jartti T, Kuusela T, Huikuri HV, Tulppo bouts of different intensities. Med Sci Sports Exerc.
MP, et al. Time domain, geometrical and frequency domain 2005;37(4):599-605.
analysis of cardiac vagal outfow: effects of various respiratory
patterns. Clin Physiol. 2001;21(3):365-76. 48. Guimarães GV, D’Avila VM, Chizzola PR, Bacal F, Stolf N,
Bocchi EA. Reabilitação física no transplante de coração. Rev
35. De Vito G, Galloway SD, Nimmo MA, Maas P, McMurray Bras Med Esporte. 2004;10(5):408-11.
JJ. Effects of central sympathetic inhibition on heart rate
variability during steady-state exercise in healthy humans. Clin 49. Beckers F, Ramaekers D, Van Cleemput J, Droogné W,
Physiol Funct Imaging. 2002;22(1):32-8. Vanhaecke J, Van de Werf F, et al. Association between
restoration of autonomic modulation in the native sinus node
36. Tulppo MP, Mäkikallio TH, Seppänen T, Laukkanen RT, and hemodynamic improvement after cardiac transplantation.
Huikuri HV. Vagal modulation of heart rate during exercise: Transplantation. 2002;73(10):1614-20.
effects of age and physical fitness. Am J Physiol. 1998;274(2
Pt 2):H424-9. 50. Salles AF, Oliveira Fº JA. Adaptações ao exercício pós-
transplante cardíaco Arq Bras Cardiol. 2000;75(1):79-84.
37. Melo RC, Santos MD, Silva E, Quitério RJ, Moreno MA,
Reis MS, et al. Effects of age an physical activity on the 51. Bacal F, Bocchi EA, Vieira MLC, Lopes N, Moreira LF, Fiorelli
autonomic control of heart rate in healthy men. Braz J Med A ,et al. Uso de marcapasso provisório e definitivo em pacientes
Biol Res. 2005;38(9):1331-8. submetidos a transplante cardíaco ortotópico. Arq Bras Cardiol.
2000;74(1):5-8.
38. Javorka M, Zila I, Balhárek T, Javorka K. Heart rate recovery
after exercise: relations to heart rate variability and complexity. 52. Ramos G, Ramos Filho J, Rassi Júnior A, Pereira E, Gabriel
Braz J Med Biol Res. 2002;35(8):991-1000. Neto S, Chaves E. Marcapasso cardíaco artificial:
considerações pré e per-operatórias. Rev Bras Anestesiol.
39. Chua KC, Chandran V, Acharya UR, Lim CM. Cardiac state 2003;53(6):854-62.
diagnosis using higher order spectra of heart rate variability. J
Med Eng Technol. 2008;32(2):145-55. 53. Hsiao HC, Chiu HW, Lee SC, Kao T, Chang HY, Kong CW.
Esophageal PP intervals for analysis of short-term heart rate
40. Martinelli FS, Chacon-Mikahil MP, Martins LE, Lima-Filho variability in patients with atrioventricular block before and
EC, Golfetti R, Paschoal MA, et al. Heart rate variability in after insertion of a temporary ventricular inhibited pacemaker.
athletes and nonathletes at rest and during head-up tilt. Braz J Int J Cardiol. 1998; 64(3):271-6.
Med Biol Res. 2005;38(4):639-47.
54. Carney RM, Freedland KE, Stein PK, Miller GE,
41. Middleton N, De Vito G. Cardiovascular autonomic control in Steinmeyer B, Rich MW, et al. Heart rate variability and
endurance-trained and sedentary young women. Clin Physiol markers of inflammation and coagulation in depressed
Funct Imaging. 2005;25(2):83-9. patients with coronary heart disease. J Psychosom Res.
2007;62(4):463-7.
42. Hedelin R, Bjerle P, Henriksson-Larsén K. Heart rate variability
in athletes: relationship with central and peripheral 55. Takahashi ACM, Novais LD, Silva E, Sakabe DI, Oliveira L,
performance. Med Sci Sports Exerc. 2001;33(8):1394-8. Milan LA, et al. Avaliação do controle autonômico da
frequência cardíaca e determinação do limiar de anaerobiose em
43. Martinmäki K, Rusko H. Time-frequency analysis of heart homens saudáveis e coronariopatas. Rev Bras Fisioter.
rate variability during immediate recovery from low and high 2005;9(2):157-64.
intensity exercise. Eur J Appl Physiol. 2008;102(3):353-60.
56. Carnethon MR, Liao D, Evans GW, Cascio WE, Chambless
44. Malliani A, Pagani M, Lombardi F, Cerutti S. Cardiovascular LE, Heiss G. Correlates of the shift in heart rate variability
neural regulation explored in the frequency domain. Circulation. with an active postural change in a health population sample:
1991;84(2):482-92. The Atherosclerosis Risk In Communities study. Am Heart J.
2002;143(5):808-13.
45. Pagani M, Lombardi F, Guzzetti S, Rimoldi O, Furlan R,
Pizzinelli P, et al. Power spectral analysis of heart rate and 57. Carnethon MR, Liao D, Evans GW, Cascio WE, Chambless
arterial pressure variabilities as a marker of sympatho-vagal LE, Rosamond WD, et al. Does the cardiac autonomic response
interaction in man and conscious dog. Circulation. to postural change predict incident coronary heart disease and
1986;59(2):178-93. mortality? Am J Epidemiol. 2002;155(1):48-56.

215
VANDERLEI, LCM ET AL - Basic notions of heart rate variability Rev Bras Cir Cardiovasc 2009; 24(2): 205-217
and its clinical applicability

58. Limongelli G, Miele T, Pacileo G, Di Salvo G, Calabro P, Ancona reduced in patients with type 1 diabetes mellitus. Clin
R, et al. Heart rate variability is a weak predictor of sudden Neurophysiol. 2008;119(5):1071-81.
death in children and young patients with hypertrophic
cardiomyopathy. Heart. 2007;93(1):117-8. 71. Lakusic N, Mahovic D, Babic T. Gradual recovery of impaired
cardiac autonomic balance within first six months after ischemic
59. Karas M, Larochelle P, LeBlanc RA, Dubé B, Nadeau R, cerebral stroke. Acta Neurol Belg. 2005;105(1):39-42.
Champlain J. Attenuation of autonomic nervous system
functions in hypertensive patients at rest and during orthostatic 72. Zulli R, Nicosia F, Borroni B, Agosti C, Prometti P, Donati P,
stimulation. J Clin Hypertens (Greenwich). 2008;10(2):97-104. et al. QT dispersion and heart rate variability abnormalities in
Alzheimer’s disease and in mild cognitive impairment. J Am
60. Menezes Jr AS, Moreira HG, Daher MT. Análise da Geriatr Soc. 2005;53(12):2135-9.
variabilidade da frequência cardíaca em pacientes hipertensos,
antes e depois do tratamento com inibidores da enzima 73. Nevruz O, Yokusoglu M, Uzun M, Demirkol S, Avcu F, Baysan
conversora da angiotensina II. Arq Bras Cardiol. O, et al. Cardiac autonomic functions are altered in patients
2004;83(2):165-8. with acute leukemia, assessed by heart rate variability. Tohoku
J Exp Med. 2007;211(2):121-6.
61. Terathongkum S, Pickler RH. Relationships among heart rate
variability, hypertension, and relaxation techniques. J Vasc 74. Park DH, Shin CJ, Hong SC, Yu J, Ryu SH, Kim EJ, et al.
Nurs. 2004;22(3):78-82. Correlation between the severity of obstructive sleep apnea
and heart rate variability indices. J Korean Med Sci.
62. Larosa C, Sgueglia GA, Sestito A, Infusino F, Niccoli G, 2008;23(2):226-31.
Lamendola P, et al. Predictors of impaired heart rate variability
and clinical outcome in patients with acute myocardial 75. El-Sayed HL, Kotby AA, Tomoum HY, El-Hadidi ES, El
infarction treated by primary angioplasty. J Cardiovasc Med Behery SE, El-Ganzory AM. Non-invasive assessment of
(Hagerstown). 2008;9(1):76-80. cardioregulatory autonomic functions in children with epilepsy.
Acta Neurol Scand. 2007;115(6):377-84.
63. Pecyna MB. The level of intelligence and heart rate variability
in men after myocardial infarction. J Physiol Pharmacol. 76. Mosek A, Novak V, Opfer-Gehrking TL, Swanson JW, Low
2006;57(suppl 4):283-7. PA. Autonomic dysfunction in migraineurs.
Headache.1999;39(2):108-17.
64. Reis AF, Bastos BG, Mesquita ET, Romeu Filho LJM, Nóbrega
ACL. Disfunção parassimpática, variabilidade de frequência 77. Dishman RK, Nakamura Y, Garcia ME, Thompson RW, Dunn
cardíaca e estimulação colinérgica após infarto agudo do AL, Blair SN. Heart rate variability, train anxiety, and perceived
miocárdio. Arq Bras Cardiol. 1998;70(3):193-7. stress among physically fit men and woman. Int J
Psychophysiol. 2000;37(2):121-33.
65. Kudaiberdieva G, Görenek B, Timuralp B. Heart rate variability
as a predictor of sudden cardiac death. Anadolu Kardiyol Derg. 78. Tulppo MP, Hautala AJ, Mäkikallio TH, Laukkanen RT, Nissilä
2007;7(suppl 1):68-70. S, Hughson RL, et al. Effects of aerobic training on heart rate
dynamics in sedentary subjects. J Appl Physiol.
66. Pantoni CBF, Reis MS, Martins LEB, Catai AM, Costa D, 2003;95(1):364-72.
Borgui-Silva A. Estudo da modulação autonômica da frequência
cardíaca em repouso de pacientes idosos com doença pulmonar 79. Lopes FL, Pereira FM, Reboredo M, Castro TM, Vianna JM,
obstrutiva crônica. Rev Bras Fisioter 2007;11(1):35-41. Novo Júnior JM, et al. Redução da variabilidade da frequência
cardíaca em indivíduos de meia-idade e o efeito do treinamento
67. Sin DD, Wong E, Mayers I, Lien DC, Feeny D, Cheung H, et de força. Rev Bras Fisioter. 2007;11(2):113-9.
al. Effects of nocturnal noninvasive mechanical ventilation on
heart rate variability patients with advanced COPD. Chest. 80. Paschoal MA, Volanti VM, Pires CS, Fernandes FC.
2007;131(1):156-63. Variabilidade de frequência cardíaca em diferentes faixas etárias.
Rev Bras Fisioter. 2006;10(4):413-9.
68. Furuland H, Linde T, Englund A, Wikström B. Heart rate
variability is decreased in chronic kidney disease but may improve 81. Neves VF, Silva de Sá MF, Gallo L Jr, Catai AM, Martins
with hemoglobin normalization. J Nephrol. 2008;21(1):45-52. LE, Crescêncio JC, et al. Autonomic modulation of heart rate
of young and postmenopausal women undergoing estrogen
69. Silva VJD, Januário EM. Variabilidade da frequência cardíaca e therapy. Braz J Med Biol Res. 2007;40(4):491-9.
da pressão arterial na insuficiência cardíaca congestiva. Rev
Bras Hipertens. 2005;12(1):21-6. 82. Ribeiro TF, Azevedo GD, Crescêncio JC, Marães VR, Papa V,
Catai AM, et al. Heart rate variability under resting conditions
70. Javorka M, Trunkvalterova Z, Tonhajzerova I, Javorkova J, in postmenopausal and young women. Braz J Med Biol Res.
Javorka K, Baumert M. Short-term heart rate complexity is 2001;34(7):871-7.

216
VANDERLEI, LCM ET AL - Basic notions of heart rate variability Rev Bras Cir Cardiovasc 2009; 24(2): 205-217
and its clinical applicability

83. Mercuro G, Podda A, Pitzalis L, Zoncu S, Mascia M, Melis U, Moller M. Fractal correlation properties of R-R interval
GB, et al. Evidence of a role of endogenous estrogen in the dynamics and mortality in patients with depressed left
modulation of autonomic nervous system. Am J Cardiol. ventricular function after an acute myocardial infarction.
2000;85(6):787-9. Circulation. 2000;101(1):47-53.

84. Meyerfeldt U, Wessel N, Schutt H, Selbig D, Schumann A, 86. Mäkikallio TH, Hoiber S, Kober L, Torp-Pedersen C, Peng
Voss A, et al. Heart rate variability before the onset of ventricular CK, Goldberger AL, et al. Fractal analysis of heart rate
tachycardia: differences between slow and fast arrhythmias. dynamics as a predictor of mortality in patients with depressed
Int J Cardiol. 2002;84(2-3):141-51. left ventricular function after acute myocardial infarction.
TRACE Investigators. TRAndolapril Cardiac Evaluation. Am
85. Huikuri HV, Mäkikallio TH, Peng CK, Goldberger AL, Hintze J Cardiol. 1999;83(6):836-9.

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