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Citation: Sánchez-Delgado, J.C.;
Jácome-Hortúa, A.M.; Yoshida de
Melo, K.; Aguilar, B.A.; Vieira
Philbois, S.; Dutra de Souza, H.C.
Physical Exercise Effects on
Cardiovascular Autonomic
Modulation in Postmenopausal
Women—A Systematic Review and
Meta-Analysis. Int. J. Environ. Res.
Public Health 2023,20, 2207. https://
doi.org/10.3390/ijerph20032207
Academic Editors: Ferran
Cuenca-Martínez, JoséCasaña
Granell and Luis Suso-Martí
Received: 17 December 2022
Revised: 17 January 2023
Accepted: 17 January 2023
Published: 26 January 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
International Journal of
Environmental Research
and Public Health
Review
Physical Exercise Effects on Cardiovascular Autonomic
Modulation in Postmenopausal Women—A Systematic Review
and Meta-Analysis
Juan Carlos Sánchez-Delgado 1, * , Adriana Marcela Jácome-Hortúa2, Kelly Yoshida de Melo 3,
Bruno Augusto Aguilar 3, Stella Vieira Philbois 3and Hugo Celso Dutra de Souza 3
1Grupo de Investigación Ser Cultura y Movimiento, Facultad de Salud, Universidad Santo
Tomás-Bucaramanga, Santander 680001, Colombia
2Universidad de Santander, Facultad de Ciencias Médicas y de la Salud, Bucaramanga 680003, Colombia
3Laboratory of Physiology and Cardiovascular Physioterapy, Ribeirão Preto Medical School,
University of São Paulo, Ribeirão Preto 14049-900, Brazil
*Correspondence: juansanchez@ustabuca.edu.co or juancarlossanchezd@gmail.com
Abstract:
Background: The cardioprotective effect of physical exercise has been demonstrated in
several studies. However, no systematic or updated analysis has described the effects of physical
exercise on cardiovascular autonomic modulation in postmenopausal women. Aim: to describe the
effects of physical exercise on cardiovascular autonomic modulation in postmenopausal women.
Methods: The Scopus, PubMed, and Embase databases were searched for randomized clinical trials
published between January 2011 and December 2021, and regarding the effects of physical exercise
on cardiovascular autonomic modulation in postmenopausal women. Two independent authors
processed the citations. The methodological quality was evaluated using the PEDRo scale. Results: Of
the 91 studies identified, only 8 met the inclusion criteria, of which 7 had fair or poor methodological
quality. The analyzed studies investigated the effects of functional training, whole-body vibration,
muscular resistance, stretching, and aerobic exercises performed at home or at the gym. The majority
of these exercise modalities showed improvements in heart-rate variability (HRV) indices and in the
low-frequency band of blood pressure variability. The meta-analysis shows that exercise increased
the standard deviation of instantaneous beat-to-beat variability (SD1) (mean difference (MD) = 3.99;
95% confidence interval (CI) = 1.22 to 6.77, n = 46; I
2
: 0%) and the standard deviation of long-term
variability (SD2) (MD = 11.37; 95% CI = 2.99 to 19.75; n = 46; I
2
: 0%). Conclusions: Aerobic exercise and
some nonconventional training modalities may have beneficial effects on cardiovascular autonomic
modulation in postmenopausal women. More high-quality studies are still needed to further confirm
their efficacy and safety.
Keywords: autonomic nervous system; menopause; physical activity; secondary prevention
1. Introduction
Menopause is characterized by ovarian hormone privation, which is often followed by
dysfunction in cardiovascular autonomic modulation. These alterations involve an increase
in sympathetic influence on the heart and vascular beds, and a decrease in vagal influence
on the heart. Both factors are associated with increased cardiovascular risk and mortality
in this population [
1
–
4
]. The reduction in heart-rate variability (HRV) and baroreflex
sensitivity (BRS) are physiological parameters that frequently reflect these dysfunctions
and the increase in blood-pressure variability (BPV). These indicators show a low capacity
of the heart to respond to multiple physiological and environmental stimuli, including
compensation for disorders induced by the same diseases [3–6].
Given that the autonomic nervous system (ANS) plays a relevant role in the patho-
genesis of cardiovascular diseases, the promotion of interventions that aim to improve
Int. J. Environ. Res. Public Health 2023,20, 2207. https://doi.org/10.3390/ijerph20032207 https://www.mdpi.com/journal/ijerph
Int. J. Environ. Res. Public Health 2023,20, 2207 2 of 13
autonomic modulation of the cardiovascular system should be considered [
6
,
7
]. Physical
exercise, owing to its beneficial effects on the cardiovascular system, is considered to be
the cornerstone for the nonpharmacological treatment and prevention of such diseases in
postmenopausal women [
7
–
11
]. Therefore, nonpharmacological treatment with different
exercise methodologies, mainly aerobic, promotes, among other benefits, changes in cardiac
autonomic balance, characterized by an increase in vagal autonomic drive and a decrease
in sympathetic drive, associated with an increase in SBR [7–15].
Despite this, to the best of our knowledge, no systematic or updated analysis has
described the effects of physical exercise on cardiovascular autonomic modulation in
postmenopausal women. Therefore, this review aimed to investigate the effects of physical
exercise on cardiovascular autonomic modulation in postmenopausal women.
2. Methods
A systematic review of the literature was performed by searching for randomized con-
trolled trials (control or comparison arms) published between January 2011 and December
2021 in English that described the effects of physical exercise on the autonomic modulation
of cardiovascular disease in postmenopausal women. Animal studies, cohorts that mixed
pre- and postmenopausal states, women on chemotherapy or radiation therapy, and those
that used combination treatment or showed acute effects were excluded from the analysis.
We searched for studies in the Scopus, Web of Science, PubMed, and Embase databases
using search equations that included keywords extracted from Medical Subject Headings
(MeSH) or EMTREE with Boolean descriptors “OR” within the word group and “AND” to
combine terms related to population, intervention, control group, and outcomes.
The keywords used for the population were: postmenopause, postmenopausal female,
postmenopausal period, and postmenopausal women; for the type of study: randomized
clinical trial, controlled clinical trial, and controlled clinical comparison; for the intervention:
exercise, exercise therapy, exercise training, and physical exercise; for the results: autonomic
nervous system, heart rate, blood pressure, blood tension, arterial baroreflex, tilt-table test,
heart-rate variability, and blood pressure variability.
In the study selection process, one author (J.C.S.-D.) eliminated duplicate records
obtained through the search strategy. Then, two investigators (A.M.J.-H., K.Y.d.M.) screened
the abstracts of potentially eligible studies and performed a full-text review to confirm that
the eligibility criteria were met. The analyzed studies were developed independently by
the evaluators and agreed upon by a third party (J.C.S.-D.) when there were discrepancies.
Subsequently, the methodological quality of each selected article was established
using the PEDro scale (www.pedro.org.au, accessed on 16 January 2023) [
16
–
18
]. This scale
comprises 11 items that assess eligibility, randomization, blinding, allocation masking,
group comparability at the baseline, masking, intent-to-treat analysis, and adequate follow-
up outcomes. The total score on the PEDro scale is the sum of each met criterion, ranging
from 0 to 10. The higher the score is, the better the methodological quality of the study is.
A summary score of 10–11 points was classified as excellent, 7–9 points as good, 5–6 points
as fair, and less than 5 points as poor methodological quality [
19
]. The evidence quality
or certainty was rated with the GRADEPro tool regarding the risk of bias, imprecision,
inconsistency, indirectness, and publication bias.
Information related to the sample size, age, type of intervention, and results found
to cardiovascular autonomic modulation (linear and nonlinear analyses of HRV and BPV)
was extracted and analyzed.
The linear analysis of HRV included time domain and frequency domain parameters.
RR interval (RRi), root mean square of the successive differences (RMSSD), standard devia-
tion of NN intervals (SDNN), coefficient of variation (CV), number of pairs of successive
NN (R–R), and intervals that differed by more than 50 ms (NN50) were the indices selected
under the time domain. Total spectral power (TP ms2), high-frequency power in absolute
(HF ms2) and normalized (HF nu) units, low-frequency power in absolute (LF ms2) and nor-
malized (LF nu) values, the LF/HF ratio with absolute and normalized values (LFn/HFn),
Int. J. Environ. Res. Public Health 2023,20, 2207 3 of 13
and geometric indices, such as the triangular index (RRtri), the triangular interpolation of
RR, and interval histogram (TINN) were selected from the frequency domain HRV indices.
The analyzed nonlinear HRV parameters included the standard deviation of instan-
taneous beat-to-beat variability (SD1), the standard deviation of the long-term variability
(SD2), the ratio of SD1/SD2, and detrended fluctuation analysis (DFA) (short-term fractal
exponent
α
1, long-term fractal exponent 2, and the ratio of exponents
α
1/
α
2). BPV was
obtained using the LF of the systolic blood pressure (SBP).
The synthesis and analysis of the information were narrative and qualitative. When
possible, meta-analyses were performed using RevMan 5.4 to compare differences in means
and 95% confidence intervals (95% CI) for continuous variables between the intervention
and control/comparison groups. Lastly, TSA 0.9.5.10 Beta software was used to perform
trial sequential analysis (TSA) on results associated with the meta-analyses. The param-
eters of this study were set as follows: Type I error probability
α
= 5%, and statistical
power 1
−β
= 90%. The sample size was used as the required information size (RIS) for a
two-sided test. The protocol for this systematic review was registered with PROSPERO
(CRD42022320414).
3. Results
The search criteria identified 91 studies, 8 of which met the eligibility criteria for
analysis (Figure 1). These included samples of 25 to 64 physically inactive postmenopausal
women, most apparently healthy [
20
–
23
], with obesity [
24
–
26
], hypertension [
26
], or coro-
nary artery disease [
27
], whose ages ranged between 50 and 66 years. According to the
PEDro scale, all studies specified eligibility criteria, used randomization, initial and inter-
group comparison, and variability measures, and assessed at least one key outcome in
more than 85% of the initially allocated subjects. None of the studies was blinded, nor
was there any blinding of the participants, interventionists, or intention-to-treat analyses.
The identified studies scored between 4 and 7 on the respective scales (Table 1). As to the
quality of the evidence at the meta-analysis outcome level, Table 2shows very low levels
of certainty.
Int. J. Environ. Res. Public Health 2023, 20, x 5 of 13
Figure 1. Methodological quality for the included trials.
The analyzed studies investigated the effects of different physical training modali-
ties on cardiovascular autonomic modulation assessed through HRV and BPV. The pro-
tocols included aerobic exercise in the home environment, functional training (FT), body
vibration, resistance, and muscle stretching.
3.1. Effects of Physical Exercise on Linear Parameters of HRV
The effects of physical exercise on linear HRV parameters were evaluated in six
studies, two of which showed significant changes in the time domain [20,21], while four
showed changes in the frequency domain [21–24] (Table 3).
Figure 1. Methodological quality for the included trials.
Int. J. Environ. Res. Public Health 2023,20, 2207 4 of 13
Table 1. Methodological quality for the included trials.
Methodological Quality (PEDro Scale)
First Author Eligibility
Criteria
Random
Assignment
Allocation
Concealment
Initial
Comparability
Participant
Blinding
Provider
Blinding
Blinding of
Outcome
Assessors
Retention
Analysis by
Intention
to Treat
Comparison
between
Groups
Variability
of Key
Outcome
Provided
Total
Score
Quality
of Study
Rezende et al. [
20
]
Y Y N Y N N N N N Y Y 4 Poor
Shen et al. [21] Y Y N Y N N N N N Y Y 4 Poor
Rezende et al. [
22
]
Y Y N Y N N N N N Y Y 4 Poor
Gerage et al. [23] Y Y N Y N N N Y N Y Y 5 Fair
Wong et al. [24] Y Y N Y N N N N N Y Y 4 Poor
Wong et al. [25] Y Y Y Y N N Y N N Y Y 7 Good
Wong et al. [26] Y Y N Y N N N Y N Y Y 6 Fair
Lai et al. [27] Y Y N Y N N N N N Y Y 4 Poor
Abbreviations: N, no; Y, yes.
Table 2. Summary of findings and certainty assessment–intervention (exercise vs. control).
Certainty Assessment Number of Patients Effect
Certainty Importance
№of Studies Study Design Risk of Bias Inconsistency Indirectness Imprecision Other Con-
siderations Exercise Control Relative
(95% CI)
Absolute
(95% CI)
Instantaneous beat-to-beat variability (follow-up: mean 14 weeks)
2
randomised trials
very serious anot serious not serious serious bnone 47 46 - 3.99
(1.22 to 6.77)
⊕### Very
low No importante
Standard deviation of the long-term variability (follow-up: mean 14 weeks)
2
randomised trials
very serious anot serious not serious serious bnone 47 46 - 11.37
(2.99 to 19.75)
⊕### Very
low No importante
CI: confidence interval; MD: mean difference. Explanations: aHigh risk of reporting bias in trials with >25% weight. bTotal population size or number of events is less than 400.
Int. J. Environ. Res. Public Health 2023,20, 2207 5 of 13
The analyzed studies investigated the effects of different physical training modalities
on cardiovascular autonomic modulation assessed through HRV and BPV. The protocols
included aerobic exercise in the home environment, functional training (FT), body vibration,
resistance, and muscle stretching.
3.1. Effects of Physical Exercise on Linear Parameters of HRV
The effects of physical exercise on linear HRV parameters were evaluated in six studies,
two of which showed significant changes in the time domain [
20
,
21
], while four showed
changes in the frequency domain [21–24] (Table 3).
3.1.1. Effects of Physical Exercise on HRV Time Domains
Two trials reported relevant results regarding the time domain. Rezende et al. [
20
]
showed that 12 weeks of FT at a frequency of three times a week and intensity of 13–14
(Borg scale) increased the RRi (Control Group (Con)
−
22.66
±
75.75 vs. Experimental
Group (Exp) 70.17
±
104.30, p< 0.05) and RMSSD (Con
−
0.18
±
5.66 vs. Exp 5.10
±
11.93,
p< 0.05). Shen et al. [
21
] showed that physical exercise based on an aerobic modality can
reduce the SDNN (Con
−
2.60
±
1.81 vs. Exp
−
7.33
±
2.15, p< 0,05), CV (Con
−
0.40
±
0.17
vs. Exp
−
0.81
±
0.23, p< 0.05) and the NN50 (Con 3.91
±
1.87 vs. Exp
−
5.81
±
2.27,
p< 0.05) (Table 3).
3.1.2. Effects of Physical Exercise on HRV Frequency Domains
Of the six trials in which linear analysis was performed in the frequency domain, four
indicated the presence of significant changes in HRV. Lai et al. [
27
] reported that eight
weeks of home aerobic exercise at a frequency of three times a week and intensity 13–15
(Borg scale), increased the TP (Con
−
107.24
±
270.3 vs. Exp 165.25
±
215,0; p< 0.05),
HF ms
2
(Con 3.07
±
37.81 vs. Exp 91.0
±
106.7; p< 0.05), and LF ms
2
(Con
−
17.67
±
55.83
vs. Exp 48.12
±
73.32; p< 0.05). Wong et al. [
24
] showed that eight weeks of training with
vibrating platforms, three times a week and with progressively increased intensity between
25–40 Hz, promoted a reduction in LnLF/LnHF ratio (Con
−
0,01
±
0.02 vs. Exp
−
0.09
±
0.0;
p< 0.05), nLF/nHF (Con 0
±
0.2 vs. Exp
−
0.3
±
0.3; p< 0.05), and an increase in nHF
(Con 2.1
±
2.54 vs. Exp 8.2
±
4.03; p< 0,05). Similarly, Wong et al. [
25
] observed that, after
eight weeks of stretching exercises performed three times a week, there was a significant
increase in the nHF (Con 1.1
±
2.75 vs. Exp 13.9
±
1.87 p< 0.05) and reduction in nLF
(Con
−
2.8
±
2.69 vs. Exp
−
14
±
1.9; p< 0.05) and LnLF/LnHF (Con
−
0.01
±
0.0 vs. Exp
−
0.08
±
0.02; p< 0.05). Finally, Shen et al. [
21
] found that ten weeks of aerobic exercise
performed using a step, three times a week, and with intensity between 75% and 85% of
the reserve heart rate (RHR), promoted a reduction of 55.8% in LF, 39.9% in HF, 11.2% in
normalized LF, and 34.5% in LF/HF ratio. In addition, an increase of 40% was observed in
normalized HF (Table 3).
3.2. Effects of Physical Exercise on Nonlinear HRV Parameters
According to Rezende et al. [
22
], individuals who underwent FT for 18 weeks, three
times a week, showed an increase in the SD1 component (Con
−
0.13
±
4.0 vs. Exp 3.6
±
8.43,
p< 0.05) and in the fractal property of
α
1 (Con
−
0.04
±
0.13 vs. Exp 0.07
±
0.21) (Table 3).
The meta-analysis revealed an increase in SD1 and SD2 in the trained group compared to
the control (SD1: MD = 3.99; 95% [CI] = 1.22 to 6.77, n = 46; I
2
: 0%), (SD2: MD = 11.37;
95% CI = 2.99 to 19.75; n = 46; I
2
: 0%). (Figure 2A,B). Additionally, the TSA results show
that the cumulative Z value crossed the traditional boundary value; however, the RIS curve
was not crossed, indicating that the study sample size did not reach the expected value, as
shown in Figure 3A,B.
Int. J. Environ. Res. Public Health 2023,20, 2207 6 of 13
Table 3. Effect of physical exercise and HRT on cardiovascular and metabolic system in postmenopausal women.
Study Participants
nat Baseline Age Groups Evaluated Outcomes Significant Differences
between Groups
Lai et al. [27] (2011)
CON n= 19 66.69 ±5.26 Control group did not participate in any
supervised exercise. Linear HRV indexes.
Time domain: SDRR.
Frequency domain: TP (ms2),
LF (ms2), HF (ms2), LF (nu),
HF (nu), LF/HF.
A home-based exercise program
appears able to improve HRV:
(TP, HF, LF).
EX n= 21 64.19 ±5.86
Type: Aerobic—at home
Each session consisted of a 5 min warm-up of
slow walking, a brisk-walking exercise segment
of 30 min, and a 5 min cooldown of slow walking.
D: 8; Ds: 40; F: 3; I: 13 and 15 on the Borg scale
during the fast walk.
Wong et al. [23] (2016)
CON n= 12 59 ±1Control group did not participate in any
supervised exercise. Linear HRV indexes.
Time domain: LnRMSSD.
Frequency domain: LnTP ms,
nLF, nHF, nLF/nHF,
LnLF ms2, LnHF ms2,
LnLF/LnHF ms2.
LnLF/LnHF and nLF/nHF
decreased, and nHF increased
after WBV (p≤0.01). The
control group showed
no changes.
EX n= 13 58 ±1
Type: Whole-Body Vibration:
Subjects performed four static and four dynamic
leg exercises on a vibration platform.
Training intensity progressed increasing the
vibration (25–40 Hz) and the frequency from low
to high amplitude (4, 5 and 21.3 gr).
D: 8; Ds: 30–60; F: 3 separated by at least 48 h.
Wong et al. [24] (2017)
CON n= 12 58 ±1
Control group did not participate in any
supervised exercise. Participants were instructed
not to change their regular habits during
the study. Linear HRV indexes.
Time domain: LnRMSSD, ms
Frequency domain: LnTP ms,
nLF, nHF, nLF/nHF,
LnLF ms2, LnHF ms2,
LnLF/LnHF ms2
For the Stretching training (ST)
group between baseline and
post intervention, there were
significant increases in
parasympathetic modulation as
measured by (nHF), p< 0.01,
and decreases in sympathetic
modulation as measured by nLF
and LnLF/LnHF (<0.05).
EX n= 13 57 ±1
Type: Stretch training
Supervised sessions with one set of 18 active and
20 passive stretches (20 exercises in a standing
position, 8 in a sitting position, and 10 in lying
position). A stretched muscle was held for 30 s at
the point of maximal exertion or range of motion.
Each stretch was followed by a 15 s
relaxation period.
D: 8; Ds: 60; F: 3
Int. J. Environ. Res. Public Health 2023,20, 2207 7 of 13
Table 3. Cont.
Study Participants
nat Baseline Age Groups Evaluated Outcomes Significant Differences
between Groups
Shen et al. [21] (2013)
CON n= 30 59.1 ±0.83
Control group did not participate in any
supervised exercise and were asked not to
change their physical activity habits during
the study.
Linear HRV indices.
Time domain: RR mean,
SDNN (ms), CV, NN50,
pNN50, NN20, pNN20,
RMSSD SDSD
Frequency domain: TP (ms2),
VLF (ms2), nHF, nLF, LF/HF.
The SAE had significant mean
decreases in SDNN, CV, NN50,
LF (ms2), HF (ms2), nLF, and
LF/HF, and showed a
significant increase in nHF.
EX n= 32 57.86 ±0.64
Type: Step-aerobic exercise SAE.
Each session: (1) warm-up: 10–15 min stretching,
(2) SAE: 35–40 min, (3) balance and cool down:
10–15 min, and (4) stretching and relaxation:
10–15 min. The step aerobic exercise program
was performed in the low-impact version in
which one foot remains in contact with the
ground or bench at all times, preventing any
hopping or jumping movements. The music
cadence of all sessions was set between 120 and
126 foot strikes per minute.
D: 10; Ds: 90; F: 3; I: 75–85% HRR.
Rezende et al. [20] (2019)
CON n= 32 58.45 ±4.8 Control group did not participate in any
supervised exercise. Linear HRV indexes.
Time domain: RR interval,
SDNN, RMSSD ms
Frequency domain: nLF, nHF,
LF ms2, HF ms2
The results obtained from the
training showed improvement
of the following cardiac
parameters in the FTG: heart
rate, RR intervals and RMSSD.
EX n= 32 60 ±4.5
Type: Functional Training.
Eleven stations, passing three times in each
station with a rest time of thirty seconds. When
finished, the participant spends
18 to 30 min walking.
D: 18; F: 3; I: 13–14 Borg scale.
Rezende et al. [22] (2017)
CON n= 32 58.45 ±4.8 Control group did not participate in any
supervised exercise. Linear HRV indexes.
RRTri, TINN.
Nonlinear HRV indexes.
SD1, SD2, SD1/SD2, DFA (α1,
α2, α1/α2).
The trained subjects had
increased SD1, beat-to-beat
global dispersion much greater,
increased in the dispersion of
long-term RR intervals and
increased short-term fractal
properties (α1).
EX n= 32 50 ±4.5
Type: Functional Training.
Eleven stations, passing three times in each
station with a rest time of thirty seconds. When
finished, the participant spends
14 to 30 min walking.
D: 18; F: 3
Int. J. Environ. Res. Public Health 2023,20, 2207 8 of 13
Table 3. Cont.
Study Participants
nat Baseline Age Groups Evaluated Outcomes Significant Differences
between Groups
Wong et al. [26] (2014)
CON n= 14 57 ±1
Control group did not participate in any
supervised exercise. Participants were instructed
not to make changes in their regular habits
during the study.
Blood pressure variability:
LFSBP
ST reduces vascular sympathetic
activity in obese
postmenopausal women
with prehypertension
and hypertension.
EX n= 14 56 ±1
Type: Stretch training.
Supervised sessions, with one set of 18 active
and 20 passive stretches (20 exercises in a
standing position, 8 in a sitting position, and 10
in the lying position). A stretched muscle was
held for 30 s at the point of maximal exertion, or
range of motion. Each stretch was followed by a
15 s relaxation period.
D: 8; Ds: 60; F: 3
Gerage et al. [23] (2013)
CON n= 14 66.2 ±4.1 Control group did not participate in any
supervised exercise.
Linear HRV indexes.
Time domain: RR interval, HR
(bpm), SDNN, RMSSD.
Frequency domain: HF (ms2),
LF (ms2), lnLF(ms2),
lnHF(ms2), LF/HF.
Geometric index:
RRTRI, TINN.
Nonlinear HRV indexes.
SD1, SD2, SD1/SD2
The results of our study suggest
that a 12-week supervised RT
program does not affect HRV
in postmenopausal,
nonhypertensive, untrained
elderly women.
EX n= 15 65.5 ±5
Type: Resistance training.
The RT program was a total body program with
8 exercises (machine bench press, leg extension,
wide-grip front lat pulldown, leg curl, preacher
curl seated calf raise, triceps pushdown, and
abdominal crunches); 2 sets, 10–15 repetitions.
D: 12; F: 3; I: 13–14 Borg scale.
Subjects performed 2 consecutive sets of 10–15
repetitions until moderate fatigue in each
exercise or stopped when it began to be difficult.
The only exception was the abdominal crunch
exercise which was performed on the floor using
the subject’s body weight (20 to 30 repetitions
without any additional overload)
n, sample size at baseline;; CON, control; EX, exercise; D, duration of the intervention (weeks); Ds, duration of the exercise session (minutes); F, exercise frequency (times/week); WBV,
whole-body vibration; Ln, natural logarithm; TP, total power; LF, low frequency; HF, high frequency; LF/HF, LF to HF ratio; n, normalized unit; CV, coefficient of variation; CAV, ; SDRR,
SD of the RR; RMSSD, root mean square of successive differences of R–R interval; RRTri, triangular index; TINN, triangular interpolation of RR intervals SD1, standard deviation of
instantaneous beat-to-beat variability; SD2, standard deviation of the long-term variability; SD1/SD2, ratio between SD1/SD2; DFA, detrended fluctuations analysis;
α
1, short-term
fractal exponent;
α
2, long-term fractal exponent;
α
1/
α
2, ratio between the exponents; LFSBP, low-frequency component of systolic blood pressure; RT. resistance training; HRR, heart
rate reserve.
Int. J. Environ. Res. Public Health 2023,20, 2207 9 of 13
Int. J. Environ. Res. Public Health 2023, 20, x 8 of 13
3.1.1. Effects of Physical Exercise on HRV Time Domains
Two trials reported relevant results regarding the time domain. Rezende et al. [20]
showed that 12 weeks of FT at a frequency of three times a week and intensity of 13–14
(Borg scale) increased the RRi (Control Group (Con) −22.66 ± 75.75 vs. Experimental
Group (Exp) 70.17 ± 104.30, p < 0.05) and RMSSD (Con −0.18 ± 5.66 vs. Exp 5.10 ± 11.93, p <
0.05). Shen et al. [21] showed that physical exercise based on an aerobic modality can
reduce the SDNN (Con −2.60 ± 1.81 vs. Exp −7.33 ± 2.15, p < 0,05), CV (Con −0.40 ± 0.17 vs.
Exp −0.81 ± 0.23, p < 0.05) and the NN50 (Con 3.91 ± 1.87 vs. Exp −5.81 ± 2.27, p < 0.05)
(Table 3).
3.1.2. Effects of Physical Exercise on HRV Frequency Domains
Of the six trials in which linear analysis was performed in the frequency domain,
four indicated the presence of significant changes in HRV. Lai et al. [27] reported that
eight weeks of home aerobic exercise at a frequency of three times a week and intensity
13–15 (Borg scale), increased the TP (Con −107.24 ± 270.3 vs. Exp 165.25 ± 215,0; p < 0.05),
HF ms2 (Con 3.07 ± 37.81 vs. Exp 91.0 ± 106.7; p < 0.05), and LF ms2 (Con −17.67 ± 55.83 vs.
Exp 48.12 ± 73.32; p < 0.05). Wong et al. [24] showed that eight weeks of training with vi-
brating platforms, three times a week and with progressively increased intensity between
25–40 Hz, promoted a reduction in LnLF/LnHF ratio (Con −0,01 ± 0.02 vs. Exp −0.09 ± 0.0;
p < 0.05), nLF/nHF (Con 0 ± 0.2 vs. Exp −0.3 ± 0.3; p < 0.05), and an increase in nHF (Con 2.1
± 2.54 vs. Exp 8.2 ± 4.03; p < 0,05). Similarly, Wong et al. [25] observed that, after eight
weeks of stretching exercises performed three times a week, there was a significant in-
crease in the nHF (Con 1.1 ± 2.75 vs. Exp 13.9 ± 1.87 p < 0.05) and reduction in nLF (Con
−2.8 ± 2.69 vs. Exp −14 ± 1.9; p < 0.05) and LnLF/LnHF (Con −0.01 ± 0.0 vs. Exp −0.08 ± 0.02;
p < 0.05). Finally, Shen et al. [21] found that ten weeks of aerobic exercise performed using
a step, three times a week, and with intensity between 75% and 85% of the reserve heart
rate (RHR), promoted a reduction of 55.8% in LF, 39.9% in HF, 11.2% in normalized LF,
and 34.5% in LF/HF ratio. In addition, an increase of 40% was observed in normalized HF
(Table 3).
3.2. Effects of Physical Exercise on Nonlinear HRV Parameters
According to Rezende et al. [22], individuals who underwent FT for 18 weeks, three
times a week, showed an increase in the SD1 component (Con −0.13 ± 4.0 vs. Exp 3.6 ±
8.43, p < 0.05) and in the fractal property of α1 (Con −0.04 ± 0.13 vs. Exp 0.07 ± 0.21) (Table
3). The meta-analysis revealed an increase in SD1 and SD2 in the trained group compared
to the control (SD1: MD = 3.99; 95% [CI] = 1.22 to 6.77, n = 46; I2: 0%), (SD2: MD = 11.37;
95% CI = 2.99 to 19.75; n = 46; I2: 0%). (Figure 2A,B). Additionally, the TSA results show
that the cumulative Z value crossed the traditional boundary value; however, the RIS
curve was not crossed, indicating that the study sample size did not reach the expected
value, as shown in Figure 3A,B.
(A)
Int. J. Environ. Res. Public Health 2023, 20, x 9 of 13
(B)
Figure 2. Forest plot of meta-analysis results presented as pooled standard mean differences with
95% CIs for changes in (A) SD1 and (B) SD2 for exercise and control groups. The exercise effects are
plotted with black diamonds. IV, inverse variance; SD1, standard deviation of instantaneous
beat-to-beat variability; SD2, standard deviation of the long-term variability [22,23].
Figure 2.
Forest plot of meta-analysis results presented as pooled standard mean differences with
95% CIs for changes in (
A
) SD1 and (
B
) SD2 for exercise and control groups. The exercise effects
are plotted with black diamonds. IV, inverse variance; SD1, standard deviation of instantaneous
beat-to-beat variability; SD2, standard deviation of the long-term variability [22,23].
Int. J. Environ. Res. Public Health 2023, 20, x 9 of 13
(B)
Figure 2. Forest plot of meta-analysis results presented as pooled standard mean differences with
95% CIs for changes in (A) SD1 and (B) SD2 for exercise and control groups. The exercise effects are
plotted with black diamonds. IV, inverse variance; SD1, standard deviation of instantaneous
beat-to-beat variability; SD2, standard deviation of the long-term variability [22,23].
A
Figure 3. Trial sequential analysis—effect on (A) SD1 and (B) SD2.
Int. J. Environ. Res. Public Health 2023,20, 2207 10 of 13
3.3. Effects of Physical Exercise on BPV
The effects of physical training on BPV were investigated in only one of the evaluated
studies [
26
]. The study showed that eight weeks of stretching exercises at a frequency of
three times a week and with 50 min per session promoted a significant reduction in LFSBP
in obese postmenopausal women (Con −0.05 ±4.0 vs. Exp 1.62 ±0.05, p< 0.001).
4. Discussion
The results of the review indicate that physical exercise may have beneficial effects
on cardiovascular autonomic modulation in postmenopausal women, as reflected by an
increase in the linear and nonlinear indices of HRV and BPV. However, the methodological
quality of most of the studies was fair or poor, suggesting that the analyzed results may
have been overestimated.
On the basis of studies that performed linear analysis of HRV, we observed that FT
and aerobic training using a step caused an increase in RRi and RMSSD, and a reduction
in SDNN, CV, and NN50. The mechanisms responsible for changes generated by FT are
still unknown; however, the literature assumes that they may be partly related to the
improvement of vascular endothelial function, resulting in an increased production of
nitric oxide (NO), which is associated with stimulation and a lower concentration of renin
after a physical training session, thereby inducing a lower amount of angiotensin II, which
has an inhibitory effect on the cardiac vagal component [
28
]. However, the decrease in
HRV parameters in the time domain caused by aerobic exercise using a step [
21
] had a
discrepancy when compared to other studies carried out in postmenopausal women [
29
,
30
].
This finding can be explained by the monitoring period used, noting that the total variance
of HRV increased with the duration of the recording [31].
Regarding the frequency domain, there was an increase in the vagal modulation
measured by the HF component in normalized units, and a decrease in the sympathetic
modulation measured by the LF component in absolute units and LF/HF ratio after dif-
ferent training modalities, such as aerobics at home, stretching exercises, aerobics using a
step, and a vibrating platform [
21
,
24
,
25
,
27
]. In addition to the increase in NO synthesis, the
decreases in circulating angiotensin II and arterial stiffness are possible responsible factors
for the vagal predominance after treatment with these four modalities [
28
,
32
–
34
]. There
is another hypothesis that could specifically explain the effect of stretching on autonomic
modulation, which can generate a state of mental–physical hypometabolic relaxation that
promotes a hypothalamic response characterized by a decrease in cardiac sympathetic
autonomic influence [35].
Our study suggests that both aerobic and strength training can increase the SD1,
SD2, and short-term fractal (
α
1;
α
1/
α
2) indices. These findings are important considering
that nonlinear methods have shown a new view of HRV behavior in different conditions,
providing additional prognostic information on cardiovascular morbidity/mortality when
compared to linear methods [
3
,
4
,
36
–
38
]. On the basis of the TSA, more studies are necessary
to confirm the effectiveness of this type of training on the behavior of these HRV parameters
in postmenopausal women.
In turn, BPV was analyzed only in a single study, and was significantly reduced in
postmenopausal women undergoing eight weeks of stretching exercises [
25
]. Resulting
from the sum of the mechanisms that respond to disturbances external to the organism,
this variable can be classified according to the time interval in which it is evaluated.
When analyzed in short beat-to-beat intervals, the method used in this work, the ob-
served variation was mainly associated with the sympathetic modulation of the vascular
tone [
39
,
40
]. Although population studies are still needed to enhance the clinical validity of
this method, some studies have suggested that high values are associated with a higher risk
of cardiovascular outcomes and mortality. Furthermore, changes in the respective parame-
ters may be indicative of changes in vascular sympathetic activity. Although few studies
have evaluated the effects of stretching exercises on vascular sympathetic modulation, the
literature suggests that, when performed chronically, this modality can improve endothelial
Int. J. Environ. Res. Public Health 2023,20, 2207 11 of 13
function by reducing vessel stiffness and blood pressure. The explanation for such effects
also involves the increase in NO bioavailability promoted by this type of activity [
41
].
In postmenopausal women, musculoskeletal discomfort and physical limitations may be
frequent, which are related to low motivation to adhere to conventional exercise programs,
especially high-intensity ones [
42
,
43
]. This is the reason why nontraditional modalities
such as those developed at home, and vibration and stretching training could be considered
to be good alternatives to improve cardiovascular autonomic balance, especially in the
early stages of treatment. Other possible advantages are the relatively low cost and easy
applicability, which would allow for training to be carried out even at home.
There are some limitations to our findings that should be considered when interpreting
the results: the small number of randomized clinical trials, with few participants, the lack
of control for confounding factors (dietary habits, the use of drugs or hormone therapy,
and morbidity status) [
22
,
27
], and the poor methodological quality determined by the very
nature of the studies that does not allow for the use of placebo or of analysis selection
by intervention protocol and not by intention to treat, which can generate a bias in the
results [
44
]. Lastly, it is suggested to include the processes of assessment of BRS, and
levels of catecholamines and angiotensin II, which could contribute to a more comprehen-
sive understanding of the effects of exercise on cardiovascular autonomic modulation in
postmenopausal women.
5. Conclusions
According to the analyzed studies, aerobic physical exercise and some unconventional
training modalities could have beneficial effects on cardiovascular autonomic modulation
in postmenopausal women. However, considering the limitations of this study, these
results should be interpreted with caution. New clinical trials with larger samples and
greater methodological rigor that compare alternative and conventional treatments in
longer intervention periods would also be useful.
Author Contributions:
Study conception and design: J.C.S.-D. and A.M.J.-H.; data acquisition: J.C.S.-D.
and K.Y.d.M.; data analysis and/or interpretation: J.C.S.-D., A.M.J.-H., H.C.D.d.S., K.Y.d.M., B.A.A. and
S.V.P. Manuscript drafting: J.C.S.-D., A.M.J.-H., H.C.D.d.S., K.Y.d.M. and B.A.A.; critical manuscript revision
for important intellectual content: J.C.S.-D., A.M.J.-H., H.C.D.d.S., K.Y.d.M., B.A.A. and S.V.P. All authors
have read and agreed to the published version of the manuscript.
Funding: this research received no external funding.
Institutional Review Board Statement:
The protocol was approved by the Bioethics Committee
of the University of Santander (protocol code 031-CBU). Informed consent was obtained from the
patients following the ethical standards of the committee and the World Medical Association and
the Declaration of Helsinki. The protocol for this systematic review was registered with PROSPERO
(CRD42022320414).
Informed Consent Statement: Not applicable.
Data Availability Statement:
The extracted data used to support the findings of this study are
available from the corresponding author upon request.
Conflicts of Interest: The authors have no conflict of interest to disclose.
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