Early Human Development 86 (2010) 213217

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Early Human Development

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / e a r l h u m d ev

Aerobic exercise during pregnancy inuences fetal cardiac autonomic control of

heart rate and heart rate variability
Linda E. May a,, Alan Glaros b, Hung-Wen Yeh c, James F. Clapp III d, Kathleen M. Gustafson e
a

Department of Anatomy, Kansas City University of Medicine and Biosciences (KCUMB) Kansas City, MO, USA
Department of Basic Medical Sciences, KCUMB, Kansas City, MO, USA
Department of Biostatistics, University of Kansas Medical Center (KUMC) Kansas City, KS, 66160, USA
d
Department of Reproductive Biology, Case Western Reserve University, Cleveland, OH, USA
e
Hoglund Brain Imaging Center, Department of Neurology, KUMC, Kansas City, KS, USA
b
c

a r t i c l e

i n f o

Article history:
Received 7 December 2009
Received in revised form 5 March 2010
Accepted 8 March 2010
Keywords:
Autonomic nervous system
Fetal heart rate
Heart rate variability
Maternal exercise
Magnetocardiology

a b s t r a c t
Background: Previous studies using ultrasound technology showed that fetal heart rate (HR) may be
responsive to maternal aerobic exercise. Although it is recognized that cardiac autonomic control may be
inuenced by the intrauterine environment, little is known about how maternal exercise affects fetal heart
development.
Aims: This study tested the hypothesis that regular maternal exercise throughout gestation inuences fetal
cardiac autonomic control of HR and heart rate variability (HRV) when compared to fetuses of nonexercising women.
Study design: Magnetocardiograms (MCGs) were recorded using a dedicated fetal biomagnetometer at 28, 32
and 36 weeks gestational age (GA) from 26 regularly exercising (N 30 min of aerobic exercise, 3 per week)
and 35 healthy, non-exercising pregnant women. Fetal MCG was isolated and normal R-peaks were marked
to derive fetal HR and HRV in the time and frequency domains. We applied a mixed-effects model to
investigate the effects of exercise, GA and fetal activity state.
Results: At 36 weeks GA, during the active fetal state, fetal HR was signicantly lower in the exercise group
(p = b0.0006). Post-hoc comparisons showed signicantly increased HRV in the exercise group during the
active fetal state at 36 weeks GA for both time and frequency domain measures.
Conclusion: These results indicate that regular maternal exercise throughout gestation results in signicantly
lower fetal HR and increased HRV.
2010 Elsevier Ireland Ltd. All rights reserved.

1. Introduction
It is generally accepted that the intrauterine environment inuences fetal development and may have implications for the longterm health of the child. Factors that inuence fetal development can
include maternal nutrition, gestational diabetes, obesity or psychosocial factors [13].These conditions can alter fetal growth and
subsequently increase risk in the offspring for obesity [4], type 2
diabetes, cardiovascular disease and disorders of the immune system
in later life [5,6]. While the importance of adequate nutrition during
pregnancy is understood, less is known about the potential benets of
maternal exercise on fetal outcomes.
In the non-pregnant state, women who exercise regularly have
lower cardiovascular risk and experience a reduction in the incidence
of obesity, diabetes, and hypertension as evidenced by a decrease in
blood pressure, improved glucose tolerance, lower fat mass, and
Corresponding author. 1750 Independence Ave, SEP 463, Kansas City, MO 64106.
Tel.: + 1 816 283 2228 (ofce); fax: + 1 816 283 2373.
E-mail address: lmay@kcumb.edu (L.E. May).
0378-3782/$ see front matter 2010 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.earlhumdev.2010.03.002

enhanced autonomic tone [7,8]. In the pregnant state, regular exercise

has multiple, positive maternal effects such as decreased pains/discomforts and depression, shorter labor and delivery, fewer pregnancy
complications, and faster recovery after delivery [914]. Earlier
studies showed that moderate exercise during pregnancy does not
increase risk to the fetus [1518]. Consequently, the American
Congress of Obstetricians and Gynecologists recommended moderate
exercise before, during and after pregnancy. However, the question of
whether maternal exercise during pregnancy imparts similar benets
to the fetus is largely unanswered.
Previous studies using ultrasound technology to detect differences
in baseline fetal heart rate during maternal exercise showed that fetal
heart rate (HR) may increase during or immediately after maternal
aerobic exercise. This suggests the fetal cardiovascular system is
responsive to maternal exercise [1923]. However, little is known
about how maternal exercise affects fetal HR even though it is
recognized that cardiac autonomic control may be inuenced by the
intrauterine environment [24]. If the fetus responds to the change in
hormonal and metabolic milieu resulting from maternal exercise,
continuous exposure throughout pregnancy could have a measurable

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L.E. May et al. / Early Human Development 86 (2010) 213217

effect on fetal cardiac autonomic control during development. We

hypothesized that maternal exercise during pregnancy would result
in lower fetal HR and increased HRV. For precise and non-invasive
measures of fetal R-R intervals, we used a dedicated fetal biomagnetometer to record magnetocardiograms (MCG) at 28, 32 and 36 weeks
gestational age. Fetal MCG has certain advantages compared to other
technologies since the fetal cardiac signal can be detected and separated easily from the maternal MCG. This non-invasive technology is
able to measure the fetal QRS complex without distortion or loss of
signal, making it a safe, reliable and sensitive tool for monitoring fetal
cardiac events and movements [2527]. Our aim was to determine if
maternal exercise throughout pregnancy would inuence fetal
cardiac autonomic control as indexed by fetal HR and HRV.
2. Materials and methods
2.1. Study population
This prospective, longitudinal non-blinded study was designed to
determine the inuence of self-reported maternal exercise on fetal
cardiac autonomic nervous system development. The study was
approved by the Kansas City University of Medicine and Biosciences
and University of Kansas Medical Center Institutional Review Boards,
following the tenets of the Declaration of Helsinki. Recruitment was
limited to low-risk, 2035 year-old women carrying singleton
pregnancies that were up to 28 weeks GA. Informed consent was
obtained prior to participation. Women were assigned to the exercise
group if they continued moderate to vigorous aerobic exercise
throughout their pregnancy for a minimum of 30 min, three times
per week. This criterion is based on the American College of
Obstetricians and Gynecologists (ACOG) minimum recommendation
for women previously sedentary prior to pregnancy. Women in the
non-exercising control group reported not participating in consistent
moderate to vigorous aerobic exercise activity throughout their
pregnancy. In total, 61 pregnant women enrolled (26 exercise, 35
control) and were asked to have an MCG at 28, 32 and 36 weeks GA.
Not all women participated in all 3 MCG visits due to non-compliance
or delivery prior to 36 weeks GA.
2.2. Data acquisition
Physical activity levels were assessed with the Modiable Physical
Activity Questionnaire (MPAQ) at the 28 and 36 week MCG session.
The MPAQ is a reliable and valid instrument for assessing the intensity
and duration of physical activities performed during the preceding
12 months in various populations including pregnant women [2835].
Kilocalories (kcal) expended per minute in light, moderate, and
vigorous physical activities were calculated by multiplying the
activities metabolic equivalent (MET) value by the subjects' body
weight in kilograms and then dividing by 60 min. Next, kcal/min was
multiplied by the time spent (number of sessions session length in
minutes) in each activity to provide kcal expenditures for time periods
of interest (e.g., kcal expended in light, moderate, and vigorous
activities for each term of pregnancy).
During the MCG recording, women were seated comfortably in a
slightly reclined position with their abdomen in slight contact with
the biomagnetometer surface. The device is an investigational 83channel fetal biomagnetometer (CTF Systems Inc., subsidiary of
VSM MedTech Ltd., Vancouver, Canada), housed in a magnetically
shielded room to eliminate the inuence of electromagnetic artifacts. The sensors covered the maternal abdominal surface from the
perineum to the top of the uterus. A continuous 18 min MCG
recording was obtained using a 300 Hz sampling rate. Digital ltering between 1 and 40 Hz (bidirectional fourth-order Butterworth
lters) was applied ofine.

2.3. Data pre-processing

Multivariate data were subjected to an Infomax independent
component analysis algorithm implemented in EEGLAB [36]. This
method segregates raw biomagnetic signals into maternal cardiac,
fetal cardiac, fetal movement and other artifacts into individual
components based on their spatially distinct electrophysiologic
sources. Specic components (i.e., fetal cardiac components) are
then reconstructed in sensor space to map the location of their
corresponding signals and to derive fetal HR and HRV from the R-R
intervals. Fiducial QRS points were automatically detected using a
template-matching algorithm. False positive and false negative
detections were manually corrected and abnormal beats were
removed from the subsequent analysis using software developed by
our team [37,38]. After normal R peaks were marked, fetal HRV was
analyzed in time and frequency domains. The time domain measures
used were: 1) the root mean square of successive differences
(RMSSD); a measure of short-term HRV and 2) the standard deviation
of normal to normal interbeat intervals (SDNN); a measure of overall
HRV. Short term variability represents fast changes in HR that are
mediated primarily by the parasympathetic nervous system while
overall HRV is inuenced by both sympathetic and parasympathetic
input [39].
For frequency domain measures, we applied a Fast Fourier
Transform to the HR plot and derived power in each of the following frequency bands: very low frequency (VLF, 0.020.08 Hz),
low frequency (LF, 0.080.2 Hz), intermediate frequency (IntF,
0.20.4 Hz) and high frequency (HF, 0.41.7 Hz). The ratio of LF/HF
was calculated as a measure of sympathovagal balance. The strength
of signal within these frequency ranges is described in terms of
power in milliseconds squared.
We chose these frequency bands based on the work of David, et al.
[40] and Van Leeuwen, et al., [41] who characterized the range of fetal
HR power in specic frequency bands and changes in power from the
second to third trimesters of pregnancy. It is generally accepted, based
on these studies, that VLF power reects primarily sympathetic
activity and the LF and IntF bands are a mix of sympathetic and
parasympathetic input [40]. In adults, the HF peak seen at the
respiratory frequency serves as a measure of parasympathetic or vagal
control. Others have shown that power in the fetal HF band increases
with GA and theorize that the elevated power is associated with
increasing ANS maturity and fetal breathing movements that are more
prevalent as the fetus matures [41,42]. However, it is important to
note that as a new area of study, there is not yet a standard regarding
frequency domain HRV for the fetus.
Fetal activity state was determined by two independent observers
(LEM/KMG) based on the fetal HR pattern [43]. States 1F (calm, nonREM) and 3F (calm wakefulness) were considered quiet state and
are associated with absent, sporadic or short-lasting HR accelerations.
States 2F (active REM) and 4F (active wakefulness) were considered
active state. HR patterns associated with the active states show
frequent, long-lasting HR accelerations that return to the baseline
[44].
2.4. Data analysis
We determined whether the data had a normal distribution by
using a normal probability plot. Variables with skewed distributions
were log-transformed such that their distributions were approximately normal. Descriptive statistics were computed for the outcome
measures and demographic factors (age, BMI, pre-pregnant-weight,
and height). For the outcome measures, we rst performed correlation analysis to assess the temporal correlations between gestation
ages. Since 44% of subjects missed 1 or 2 MCG exams, we applied a
mixed-effects model [45] which included the xed effects: 1) exercise
(exercise or control), 2) GA (28, 32, or 36 weeks), and 3) fetal activity

L.E. May et al. / Early Human Development 86 (2010) 213217

state (active or quiet); their interaction effects; and the random effects that account for temporal correlations. We also explored potential interactions among the factors.

3. Results
All women had uncomplicated pregnancies (29 males, 32
females). Baseline characteristics (mean SD) included age (29.0
4.0 years in the exercise group; 29.6 4.0 years in the control group),
height (sample means 64.5 in. in both groups), pre-pregnant weight
(134.7 14.7 lbs in the exercise group; 150.2 30.0 lb in the control
group), and BMI (22.8 2.6 in the exercise group; 25.2 4.6 in the
control group). Both groups had similar educational backgrounds,
ranging from high school diplomas to graduate degrees.
The distribution of HR was approximately normal, whereas all HRV
measures showed distributions skewed to the right (results not
shown) and thus were log-transformed. The transformation made
HRV distributions close to normal according to the normal probability
plot. HR and log-transformed HRV measures were used as the
response variables in data analysis. The mixed-effects models showed
signicant group differences in HR (p = 0.023), RMSSD (p = 0.024),
VLF (p = 0.026), LF (p = 0.035), IntF (p = 0.011), and HF (p = 0.021)
after adjusting for GA and fetal activity state which were both
signicant factors for all the aforementioned outcome variables. HR
was lower and measures of HRV were higher in the exercise group.
There was a trend for higher SDNN in the exercise group (p = 0.06).
For the LF/HF ratio, none of the factors (exercise, GA, or fetal activity
state) showed signicant effects at the 0.05 alpha level (data not
shown). Fetal HR had signicant interactions between factors: group
and GA (X2 = 12.1, df = 2, p = 0.002), group and fetal activity state
(X2 = 4.2, df = 1, p = 0.04), GA and fetal activity state (X2 = 11.8,
df = 2, p = 0.003), and a 3-way group-GA-fetal activity interaction
(X2 = 12.1, df = 2, p = 0.002). This indicates that the effect of exercise
on fetal HR depends on GA and fetal activity state. No interaction was
signicant for other outcome variables, indicating that exercise may
have the same effect on the HRV measures across GA periods in either
fetal activity state.

215

Post-hoc comparisons showed signicantly different fetal HR

between the groups at 36 weeks GA in the active fetal state
(p = 0.0006) but not at other combinations of GA and fetal activity
state (Table 1). Post-hoc comparisons indicated between-group
differences for the following HRV outcomes in the active fetal state
at 36 weeks GA: SDNN (p = 0.03), RMSSD (p = 0.03), VLF (p = 0.04),
LF (p = 0.03), IntF (p = 0.02), and HF (p = 0.01). During the quiet
state, VLF and HF were signicantly higher in the exercise group (0.04
and 0.02 respectively), however, these results should be interpreted
with caution since we did not control the experiment-wise Type I
error rate. Additionally, the sample size is smaller as the majority of
MCGs were recorded while the fetus was in an active state.

4. Discussion
We found signicantly lower fetal HR and increased fetal HRV
during the active fetal state at 36 weeks GA in women who performed
moderate aerobic exercise during their pregnancy compared to nonexercising women. Similar to previous reports [40,41], HRV in both
time and frequency domains increases with gestational age. This
study demonstrates the utility of fetal MCG as a method that allows
surveillance of the developing ANS and as a tool sensitive enough to
detect group differences.
Some have suggested that decreased fetal HR associated with
maternal exercise is due to chronic fetal hypoxia [16]. However,
studies measuring uteroplacental blood ow parameters, fetal
oxygenation and markers of fetal stress have determined that the
fetus is not compromised during maternal exercise [15,4653].
Moreover, birth outcomes and neonatal morphometric measurements demonstrate maternal exercise does not have adverse effects
on fetal growth and development [20,54,55]. Additionally, if hypoxia
were the cause of the lower fetal HR in the exercise group then it
would most likely be accompanied by decreased HRV indicating an
effect on fetal ANS development. Since normal healthy development
of the cardiac ANS is indicated by lower fetal HR coupled with
measures of increased HRV, this cannot be a viable explanation the
lower fetal HR in the exercise group.

Table 1
Post-hoc comparisons of group by GA by fetal activity state. Fetal HR is lower in the exercise group at all gestational ages, reaching signicance at 36 weeks (p = 0.0006). Fetal HRV in
the time and frequency domain is signicantly increased in the exercise group at 36 weeks for all measures in the active state (p b 0.05) and for log LF and log HF during the quiet state
(p b 0.05).
Active fetal state
28 weeks GA [mean SD]

32 weeks GA [mean SD]

36 weeks GA [mean SD]

Outcome

Exercise n = 16

Control n = 23

Exercise n = 17

Control n = 20

Exercise n = 14

Control n = 15

HR (bpm)
logRMSSD (ms)
logSDNN (ms)
logVLF power (ms2)
logLF power (ms2)
logIntF power (ms2)
logHF power (ms2)

140.6 9.1
1.8 0.3
3.1 0.3
4.2 0.5
4.2 0.5
2.3 0.6
2.2 0.5

143.7 5.5
1.6 0.3
2.9 0.2
3.9 0.5
3.9 0.5
1.7 0.9
1.8 0.5

0.35
0.05
0.21
0.36
0.36
0.05
0.07

139.4 10.2
1.8 0.3
3.2 0.3
4.6 0.6
4.6 0.6
1.9 0.8
2.2 0.6

144.9 7.0
1.6 0.3
3.1 0.3
4.1 0.5
4.1 0.5
1.3 0.6
1.9 0.5

0.09
0.18
0.69
0.12
0.12
0.12
0.23

136.5 6.8
2.0 0.5
3.4 0.3
4.8 0.6
4.8 0.6
2.3 0.9
2.6 0.8

148.1 8.2
1.7 0.3
3.1 0.3
4.2 0.6
4.2 0.6
1.4 0.7
2.0 0.4

0.0006
0.03
0.03
0.04
0.03
0.02
0.01

Quiet fetal state

28 weeks GA [mean SD]

32 weeks GA [mean SD]

36 weeks GA [mean SD]

Outcome

Exercise n = 7

Control n = 7

Exercise n = 8

Control n = 8

Exercise n = 6

Control n = 5

HR (bpm)
logRMSSD (ms)
logSDNN (ms)
logVLF power (ms2)
logLF power (ms2)
logIntF power (ms2)
logHF power (ms2)

144.3 4.7
1.5 0.5
2.7 0.4
4.0 1.0
3.1 1.3
1.4 1.5
1.4 0.5

143.0 6.2
1.4 0.3
2.6 0.4
3.7 0.8
2.6 1.0
1.1 1.2
1.4 0.5

0.85
0.59
0.63
0.38
0.24
0.56
0.78

141.6 6.6
1.4 0.5
2.7 0.2
3.5 0.9
2.5 1.2
0.9 1.3
1.6 0.6

144.4 6.2
1.6 0.4
2.7 0.3
3.5 0.6
2.6 0.9
1.1 1.1
1.8 0.6

0.14
0.67
0.54
0.61
0.36
0.44
0.48

135.7 6.6
1.9 0.5
3.1 0.5
4.5 0.7
3.3 0.9
1.8 1.0
2.5 0.8

136.0 5.2
1.7 0.4
3.0 0.4
3.9 1.0
3.0 1.0
1.5 0.7
1.8 0.6

0.51
0.09
0.35
0.04
0.17
0.09
0.02

Abbreviations: HR = heart rate, Time domain HRV measures: RMSSD = root mean square of successive difference (short term HRV), SDNN = standard deviation of normal to normal RR
intervals (overall HRV) Frequency domain HRV measures: VLF = very low frequency (0.020.08 Hz), LF = low frequency (0.080.2 Hz), IntF = intermediate frequency (0.020.4 Hz),
HF = high frequency (0.41.7 Hz).

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L.E. May et al. / Early Human Development 86 (2010) 213217

Trends in fetal HR and HRV are also inuenced by non-neural and

neural components to meet changing cardiovascular needs and
function over time [56]. During the second and third trimesters, the
parasympathetic and sympathetic nervous systems are maturing,
which leads to decreased fetal HR and increased fetal HRV [57]. Thus,
changes in HR and HRV represent maturation of components of the
central nervous system, such as the ANS and the brainstem [58].
Chronic exposure to maternal hormones of exercise can inuence
development of the ANS in the 2nd and 3rd trimesters.
During maternal exercise, there is a rise in circulating catecholamines (i.e, norepinephrine) that cross the placenta to the fetal
compartment [5962]. Norepinephrine is essential for fetal development [5962] and it is possible that chronic exposure to norephinephrine and other catecholamines throughout gestation may
inuence fetal cardiac autonomic control. If this is true, then the
amount of exposure (i.e., intensity and duration of exercise) may
determine the extent to which the fetal heart development is
inuenced. Additionally, one would presume that other systems
which respond to catecholamines (i.e., respiratory) could also be
inuenced.
Given that regular moderate to vigorous aerobic exercise is known
to lower HR and improve cardiovascular health, these ndings suggest
maternal exercise has positive cardiovascular benets for the fetus.
Currently, we are analyzing postnatal data to determine if these
differences persist after birth. Previous studies by Clapp have
determined that persistent improvements in sports performance
exist in children born to mothers who exercised during pregnancy
[63,64]. This evidence, together with the hypothesis that the fetus
makes adaptations in response to the in utero environment (i.e., the
developmental origins hypothesis), we propose that the prenatal
differences in HR and HRV reported here may continue after birth and
into adulthood. Exercise has been shown to attenuate cardiovascular
risk and comorbidites associated with diabetes and hypertension
through lowering of blood pressure, improved glucose tolerance,
reduced obesity, improved lipid prole, enhanced brinolysis,
improved endothelial function and enhanced autonomic tone [8] in
children and adolescents [65]. Therefore, exercise during pregnancy
may be the earliest intervention to improve cardiovascular health.
The capability of MCG to accurately detect and separate the fetal
cardiac signal provides a unique opportunity to investigate fetal HR
and HRV as indices of autonomic development. This precision is not
possible with fetal ECG or ultrasound techniques. MCG is therefore an
excellent tool to assess differences between two healthy normal
populations. Additionally, the non-invasive nature of this technology
allows for repeated measures during and after pregnancy. Our use of
this technology while the mother is at rest avoids exercise artifacts
and allows us to determine the effects of chronic exercise exposure to
fetal development as opposed to the acute effects.
Though we did not assess maternal tness level before pregnancy
and there is an inherent selection bias since group classication was
based on women choosing to exercise or not, the results of this pilot
study are encouraging and exciting. Compliance in completing all
three evaluations was low which compromised our ability to
meaningfully analyze longitudinal data. Lastly, we did not control
for other potential confounding variables known to affect fetal activity
state such as time of day of recording and maternal food intake. These
preliminary ndings require conrmation in a larger, controlled,
randomized study.
5. Conclusion
This longitudinal, observational pilot study is unique in that we
used non-invasive, fetal MCG to provide evidence that maternal
exercise throughout gestation results in signicantly lower fetal HR
and increased fetal HRV in both time and frequency do These new
ndings suggest that regular maternal aerobic exercise during a

healthy, low-risk pregnancy positively inuences the development of

fetal cardiac autonomic control. Therefore, a regular exercise program
during pregnancy may provide cardiovascular health benets in later
life, reducing health care costs and increasing quality of life.
Conict of interest
The authors do not have any nancial and/or personal relationships with other people or organizations which could inappropriately
inuence their work. There are no conicts of interest to report.
Acknowledgements
The authors thank Mihai Popescu, PhD and E. A. Popescu, PhD for
their contribution and expertise in designing the MatLab routines for
fetal HR and HRV analyses. We acknowledge Lori Blanck, R. EEG/EP T
and JoAnn Liermann, RN, PhD, for the assistance in data collection and
processing. We are grateful to the women who gave their time to
participate in this study. This project was supported by the Hoglund
Brain Imaging Center and the Kansas City University of Medicine and
Biosciences intramural grants.
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