Aerobic exercise during pregnancy influences fetal cardiac autonomic control of heart rate and heart rate variability

https://doi.org/10.1016/j.earlhumdev.2010.03.002Get rights and content

Abstract

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 influenced 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 influences fetal cardiac autonomic control of HR and heart rate variability (HRV) when compared to fetuses of non-exercising 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 (> 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 significantly lower in the exercise group (p = < 0.0006). Post-hoc comparisons showed significantly 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 significantly lower fetal HR and increased HRV.

Introduction

It is generally accepted that the intrauterine environment influences fetal development and may have implications for the long-term health of the child. Factors that influence fetal development can include maternal nutrition, gestational diabetes, obesity or psychosocial factors [1], [2], [3].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 benefits 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 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 [9], [10], [11], [12], [13], [14]. Earlier studies showed that moderate exercise during pregnancy does not increase risk to the fetus [15], [16], [17], [18]. 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 benefits 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 [19], [20], [21], [22], [23]. However, little is known about how maternal exercise affects fetal HR even though it is recognized that cardiac autonomic control may be influenced 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 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 [25], [26], [27]. Our aim was to determine if maternal exercise throughout pregnancy would influence fetal cardiac autonomic control as indexed by fetal HR and HRV.

Section snippets

Study population

This prospective, longitudinal non-blinded study was designed to determine the influence 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, 20–35 year-old women carrying singleton pregnancies that were up to 28 weeks GA.

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

Discussion

We found significantly 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 non-exercising 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

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 significantly lower fetal HR and increased fetal HRV in both time and frequency do These new findings suggest that regular maternal aerobic exercise during a healthy, low-risk pregnancy positively influences the development of fetal cardiac autonomic control. Therefore, a regular exercise program during pregnancy may provide

Conflict of interest

The authors do not have any financial and/or personal relationships with other people or organizations which could inappropriately influence their work. There are no conflicts 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

References (65)

  • R.T. Wakai et al.

    Spatiotemporal properties of the fetal magnetocardiogram

    Am J Obstet Gynecol

    (1994)
  • A. Delorme et al.

    EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis

    J Neurosci Methods

    (2004)
  • R.T. Wakai et al.

    Spectral analysis of antepartum fetal heart rate variability from fetal magnetocardiogram recordings

    Early Hum Dev

    (1993)
  • I.J. Nijhuis et al.

    Development of fetal heart rate and behavior: indirect measures to assess the fetal nervous system

    Eur J Obstet Gynecol Reprod Biol

    (1999)
  • J.F. Clapp

    The effects of maternal exercise on fetal oxygenation and feto-placental growth

    Eur J Obstet Gynecol Reprod Biol

    (2003)
  • J.F. Clapp et al.

    Effect of maternal exercise and fetoplacental growth rate on serum erythropoietin concentrations

    Am J Obstet Gynecol

    (2003)
  • M.M. Kennelly et al.

    Exercise-related changes in umbilical and uterine artery waveforms as assessed by Doppler ultrasound scans

    Am J Obstet Gynecol

    (2002)
  • W.E. Spinnewijn et al.

    Fetal heart rate and uterine contractility during maternal exercise at term

    Am J Obstet Gynecol

    (1996)
  • C. Collings et al.

    Fetal heart rate response to maternal exercise

    Am J Obstet Gynecol

    (1985)
  • M.A. Woo et al.

    Complex heart rate variability and serum norepinephrine levels in patients with advanced heart failure

    J Am Coll Cardiol

    (1994)
  • R.J. Sodha et al.

    Transfer and metabolism of norepinephrine studied from maternal-to-fetal and fetal-to-maternal sides in the in vitro perfused human placental lobe

    Am J Obstet Gynecol

    (1984)
  • J.F. Clapp

    Morphometric and neurodevelopmental outcome at age five years of the offspring of women who continued to exercise regularly throughout pregnancy

    J Pediatr

    (1996)
  • S. Johansson et al.

    Increased catecholamines and heart rate in children with low birth weight: perinatal contributions to sympathoadrenal overactivity

    J Int Med

    (2007)
  • P.D. Wadhwa et al.

    Stress and preterm birth: neuroendocrine, immune/inflammatory, and vascular mechanisms

    Matern Child Health J

    (2001)
  • H.K. Satpathy et al.

    Maternal obesity and pregnancy

    Postgrad Med

    (2008)
  • D.I. Phillips

    External influences on the fetus and their long-term consequences

    Lupus

    (2006)
  • R.A. Waterland et al.

    Epigenetic epidemiology of the developmental origins hypothesis

    Annu Rev Nutr

    (2007)
  • Clapp JF, III. Long-term outcome after exercising throughout pregnancy: fitness and cardiovascular risk. Am J Obstet...
  • B. Adamu et al.

    Physical exercise and health: a review

    Niger J Med

    (2006)
  • D.S. Downs et al.

    Determinants of pregnancy and postpartum depression: prospective influences of depressive symptoms, body image satisfaction, and exercise behavior

    Ann Behav Med

    (2008)
  • J.F. Clapp et al.

    Effects of pregnancy and exercise on concentrations of the metabolic markers tumor necrosis factor alpha and leptin

    Am J Obstet Gynecol

    (2000)
  • J.F. Clapp

    Effects of diet and exercise on insulin resistance during pregnancy

    Metab Syndr Relat Disord

    (2006)
  • Cited by (103)

    • Embryonic heart rate correlates with maternal temperature and developmental stage in viviparous snakes

      2021, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative Physiology
    View all citing articles on Scopus
    View full text