Aerobic exercise during pregnancy influences fetal cardiac autonomic control of heart rate and heart rate variability
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, 3x 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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Cites
Delorme, A., & Makeig, S. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2003.10.009 · Cited by 24,371 · see citing works
Decline in Physical Activity in Black Girls and White Girls during Adolescence
Kimm, S. Y. S., Glynn, N. W., Kriska, A. M., Barton, B. A., Kronsberg, S. S., Daniels, S. R., Crawford, P. B., Sabry, Z. I., & Liu, K. (2002) · New England Journal of Medicine · doi:10.1056/nejmoa003277 · Cited by 949 · see citing works
Nutrition and the developing brain: nutrient priorities and measurement
Georgieff, M. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/85.2.614s · Cited by 885 · see citing works
Epigenetic Epidemiology of the Developmental Origins Hypothesis
Waterland, R. A., & Michels, K. B. (2007) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.27.061406.093705 · Cited by 883 · see citing works
Kriska, A. M., Knowler, W. C., LaPorte, R. E., Drash, A. L., Wing, R. R., Blair, S. N., Bennett, P. H., & Kuller, L. H. (1990) · Diabetes Care · doi:10.2337/diacare.13.4.401 · Cited by 755 · cited 1× · see citing works
“TheMPAQ 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 pregnantwomen [28–35].”
MethodNoradrenaline is essential for mouse fetal development
THOMAS, S. A., Matsumoto, A. M., & Palmiter, R. D. (1995) · Nature · doi:10.1038/374643a0 · Cited by 534 · see citing works
Electronic fetal heart rate monitoring: Research guidelines for interpretation
(1997) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(97)70079-6 · Cited by 419 · see citing works
Stress and Preterm Birth: Neuroendocrine, Immune/Inflammatory, and Vascular Mechanisms
Wadhwa, P. D., Culhane, J. F., Rauh, V., & Barve, S. S. (2001) · Maternal and Child Health Journal · doi:10.1023/a:1011353216619 · Cited by 336 · see citing works
Impact of Physical Activity during Pregnancy and Postpartum on Chronic Disease Risk
(2006) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000218147.51025.8a · Cited by 283 · see citing works
Continuing regular exercise during pregnancy: Effect of exercise volume on fetoplacental growth
Clapp, J. F., Kim, H., Burciu, B., Schmidt, S., Petry, K., & Lopez, B. (2002) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2002.119109 · Cited by 252 · see citing works
Self-citationClapp, J. F. (2000) · Clinics in Sports Medicine · doi:10.1016/s0278-5919(05)70203-9 · Cited by 252 · see citing works
Self-citationClapp, J. F. (1996) · The Journal of Pediatrics · doi:10.1016/s0022-3476(96)70029-x · Cited by 240 · see citing works
Self-citationExercise Training in Obese Children and Adolescents
Watts, K., Jones, T. W., Davis, E. A., & GREEN, D. J. (2005) · Sports Medicine · doi:10.2165/00007256-200535050-00002 · Cited by 237 · see citing works
The epidemiology of leisure physical activity in an adolescent population
Aaron, D. J., Kriska, A. M., Dearwater, S. R., Anderson, R., Olsen, T., Cauley, J. A., & LaPorte, R. E. (1993) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199307000-00014 · Cited by 211 · see citing works
The effects of maternal exercise on fetal oxygenation and feto-placental growth
Clapp, J. F. (2003) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(03)00176-3 · Cited by 208 · see citing works
Self-citationWoo, M. A., Stevenson, W. G., Moser, D. K., & Middlekauff, H. R. (1994) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(94)90737-4 · Cited by 200 · see citing works
Maternal and fetal responses to a maternal aerobic exercise program
Collings, C. A., Curet, L. B., & Mullin, J. P. (1983) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(83)90576-8 · Cited by 192 · see citing works
Sensitivity Analysis for Nonrandom Dropout: A Local Influence Approach
Verbeke, G. N., Molenberghs, G., Thijs, H., Lesaffre, E. M. E. H., & Kenward, M. G. (2001) · Biometrics · doi:10.1111/j.0006-341x.2001.00007.x · Cited by 191 · see citing works
Physical activity and the initiation of high-risk health behaviors in adolescents
Aaron, D. J., Dearwater, S. R., Anderson, R., Olsen, T., Kriska, A. M., & LaPorte, R. E. (1995) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199512000-00010 · Cited by 176 · see citing works
The Development of Fetal Heart Rate Patterns During Normal Pregnancy
PILLAI, M., & James, D. K. (1990) · Obstetrics and Gynecology · doi:10.1097/00006250-199011000-00017 · Cited by 164 · see citing works
Fetal heart rate variability and complexity in the course of pregnancy
Leeuwen, P. V., Lange, S., Bettermann, H., Grönemeyer, D. H. W., & Hatzmann, W. (1999) · Early Human Development · doi:10.1016/s0378-3782(98)00102-9 · Cited by 153 · see citing works
Maternal and fetal responses to exercise during pregnancy
Lotgering, F. K., Gilbert, R. D., & Longo, L. D. (1985) · Physiological Reviews · doi:10.1152/physrev.1985.65.1.1 · Cited by 146 · see citing works
Kriska, A. M., & Bennett, P. H. (1992) · Diabetes/Metabolism Reviews · doi:10.1002/dmr.5610080404 · Cited by 141 · see citing works
Influence of Endurance Exercise and Diet on Human Placental Development and Fetal Growth
Clapp, J. F. (2005) · Placenta · doi:10.1016/j.placenta.2005.07.010 · Cited by 140 · see citing works
Self-citationAn estimate of fetal autonomic state by time-frequency analysis of fetal heart rate variability
David, M., Hirsch, M., Karin, J., Toledo, E., & AKSELROD, S. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00114.2006 · Cited by 138 · see citing works
Intrauterine growth restriction
Maršál, K. (2002) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-200204000-00005 · Cited by 134 · see citing works
Downs, D. S., DiNallo, J. M., & Kirner, T. L. (2008) · Annals of Behavioral Medicine · doi:10.1007/s12160-008-9044-9 · Cited by 134 · see citing works
Parer, J. T. (1997) · PubMed · Cited by 131 · see citing works
Cramp, A. G., & Bray, S. R. (2009) · Annals of Behavioral Medicine · doi:10.1007/s12160-009-9102-y · Cited by 129 · see citing works
Johansson, S., Norman, M., Legnevall, L., Dalmaz, Y., Lagercrantz, H., & Vanpée, M. (2007) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2007.01776.x · Cited by 127 · see citing works
Maternal Obesity and Pregnancy
Satpathy, H. K. (2008) · Postgraduate Medicine · doi:10.3810/pgm.2008.09.1920 · Cited by 126 · see citing works
Changes in the frequency power spectrum of fetal heart rate in the course of pregnancy
Leeuwen, P. V., Geue, D., Lange, S., Hatzmann, W., & Grönemeyer, D. H. W. (2003) · Prenatal Diagnosis · doi:10.1002/pd.723 · Cited by 118 · see citing works
Clapp, J. F., & Kieß, W. (2000) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(00)70215-8 · Cited by 101 · see citing works
Self-citationPulmonary responses to exercise in pregnancy
Artal, R., WISWELL, R. A., Romem, Y., & Dorey, F. J. (1986) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(86)90675-7 · Cited by 100 · see citing works
Schulz, L. O., Harper, I. T., Smith, C. J., Kriska, A. M., & Ravussin, É. (1994) · Obesity Research · doi:10.1002/j.1550-8528.1994.tb00103.x · Cited by 99 · see citing works
Effects of Diet and Exercise on Insulin Resistance during Pregnancy
Clapp, J. F. (2006) · Metabolic Syndrome and Related Disorders · doi:10.1089/met.2006.4.84 · Cited by 93 · see citing works
Self-citationPlacental transfer of catecholamines in vitro and in vivo
Morgan, C., Sandler, M. B., & Panigel, M. (1972) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(72)90182-2 · Cited by 81 · see citing works
Heart rate variability and cardiac reflexes in small for gestational age infants
Galland, B. C., Taylor, B. J., Bolton, D., & Sayers, R. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01275.2005 · Cited by 80 · see citing works
Antenatal origins of individual differences in heart rate
DiPietro, J. A., Costigan, K. A., Pressman, E. K., & Doussard-Roosevelt, J. A. (2000) · Developmental Psychobiology · doi:10.1002/1098-2302(2000)37:4 · Cited by 71 · see citing works
Long-term outcome after exercising throughout pregnancy: fitness and cardiovascular risk
Clapp, J. F. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2008.05.006 · Cited by 67 · see citing works
Self-citationPhysical conditioning effects on fetal heart rate responses to graded maternal exercise
Brenner, I., Wolfe, L. A., Monga, M., et al. (1999) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199906000-00006 · Cited by 64 · see citing works
Sodha, R. J., Proegler, M., & Schneider, H. (1984) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(84)90729-4 · Cited by 63 · see citing works
ten Hof, J., Nijhuis, I. J. M., Mulder, E. J. H., et al. (2002) · Pediatric Research · doi:10.1203/00006450-200210000-00017 · Cited by 63 · see citing works
Artal, R. (1992) · Clinics in Sports Medicine · doi:10.1016/s0278-5919(20)30537-8 · Cited by 60 · see citing works
Spatiotemporal properties of the fetal magnetocardiogram
Wakai, R. T., Wang, M., & Martin, C. B. (1994) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(94)70280-2 · Cited by 55 · see citing works
Fetal heart rate response to maternal exercise
Collings, C. A., & Curet, L. B. (1985) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(85)90277-7 · Cited by 55 · see citing works
Physical exercise and health: A review
Adamu, B., Sani, M. U., & Abdu, A. (2007) · Nigerian Journal of Medicine · doi:10.4314/njm.v15i3.37214 · Cited by 54 · see citing works
Fetal heart rate and uterine contractility during maternal exercise at term
Spinnewijn, W. E., Lotgering, F. K., Struijk, P. C., et al. (1996) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(96)70371-x · Cited by 50 · see citing works
External influences on the fetus and their long-term consequences
Phillips, D. I. (2006) · Lupus · doi:10.1177/0961203306069354 · Cited by 49 · see citing works
Development of fetal heart rate and behavior: indirect measures to assess the fetal nervous system
Nijhuis, I. J. M., & ten Hof, J. (1999) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(99)00143-8 · Cited by 46 · see citing works
Clapp, J. F. (1991) · PubMed · Cited by 44 · see citing works
Self-citationA Clinical Approach to Exercise During Pregnancy
Clapp, J. F. (1994) · Clinics in Sports Medicine · doi:10.1016/s0278-5919(20)30340-9 · Cited by 44 · see citing works
Self-citationKennelly, M., Geary, M. P., McCaffrey, N., et al. (2002) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2002.125741 · Cited by 41 · see citing works
Spectral analysis of antepartum fetal heart rate variability from fetal magnetocardiogram recordings
Wakai, R. T., Wang, M., Pedron, S. L., et al. (1993) · Early Human Development · doi:10.1016/0378-3782(93)90134-g · Cited by 39 · see citing works
The risks and benefits of exercise during pregnancy.
Jarski, R. W., & Trippett, D. L. (1990) · PubMed · Cited by 33 · see citing works
Dietary intake, weight gain, and birth outcomes of physically active pregnant women: a pilot study
Giroux, I., Inglis, S. D., Lander, S., Gerrie, S., & Mottola, M. F. (2006) · Applied Physiology Nutrition and Metabolism · doi:10.1139/h06-024 · Cited by 31 · see citing works
Pre- and Postnatal Women's Leisure Time Physical Activity Patterns
Cramp, A. G., & Bray, S. R. (2009) · Research Quarterly for Exercise and Sport · doi:10.1080/02701367.2009.10599578 · Cited by 29 · see citing works
Magnetographic assessment of fetal hiccups and their effect on fetal heart rhythm
Popescu, E.-A., Popescu, M., Bennett, T. L., et al. (2007) · Physiological Measurement · doi:10.1088/0967-3334/28/6/005 · Cited by 27 · see citing works
Non-nutritive sucking recordedin uterovia fetal magnetography
Popescu, E.-A., Popescu, M., Wang, J., et al. (2008) · Physiological Measurement · doi:10.1088/0967-3334/29/1/009 · Cited by 23 · see citing works
Fetal Heart Race and Maternal Cardiovascular and Catecholamine Responses to Dynamic Exercise
Cooper, K. A., Hunyor, S. N., Boyce, E. S., et al. (1987) · Australian and New Zealand Journal of Obstetrics and Gynaecology · doi:10.1111/j.1479-828x.1987.tb00991.x · Cited by 23 · see citing works
Effect of maternal exercise and fetoplacental growth rate on serum erythropoietin concentrations
Clapp, J. F., Little, K. D., & Widness, J. A. (2003) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2003.232 · Cited by 20 · see citing works
Self-citationMaternal and fetal cardiovascular response to exercise during pregnancy
Veille, J. (1996) · Seminars in Perinatology · doi:10.1016/s0146-0005(96)80018-8 · Cited by 19 · see citing works
Relationship between plasma glucose levels in glucose-intolerant women and newborn macrosomia
Verma, A., Mitchell, B. F., Demianczuk, N. N., Flowerdew, G. J., & Okun, N. B. (1997) · The Journal of Maternal-Fetal Medicine · doi:10.1002/(sici)1520-6661(199705/06)6:3 · Cited by 17 · see citing works
Transfer of Ritodrine and Norepinephrine in Human Placenta: in vitro Study
Nandakumarana, M., Gardey, C., Rey, E., et al. (2017) · Developmental Pharmacology and Therapeutics · doi:10.1159/000457392 · Cited by 17 · see citing works
Analysis of Fetal Heart Rate Variability Obtained by Magnetocardiography
Verklan, M. T., Padhye, N. S., & Brazdeikis, A. (2006) · The Journal of Perinatal & Neonatal Nursing · doi:10.1097/00005237-200610000-00014 · Cited by 13 · see citing works
Cramp, A. G., & Bray, S. R. (2009) · Research Quarterly for Exercise and Sport · doi:10.5641/027013609x13088500158968 · Cited by 12 · see citing works
Temperature effects on oxygen affinity of human fetal blood.
Gilbert, R. D., Lis, L., & Ld, L. (1985) · PubMed · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Marques, A. H., Bjørke-Monsen, A.-L., Teixeira, A. L., & Silverman, M. N. (2015) · Brain Research · doi:10.1016/j.brainres.2014.10.051 · Cited by 166 · see citing works
Kemp, A. H., Koenig, J., & Thayer, J. F. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.09.006 · Cited by 114 · see citing works
Aerobic exercise during pregnancy influences infant heart rate variability at one month of age
May, L. E., Scholtz, S. A., Suminski, R., & Gustafson, K. M. (2014) · Early Human Development · doi:10.1016/j.earlhumdev.2013.11.001 · Cited by 82 · see citing works
Self-citationEffects of exercise during pregnancy on maternal heart rate and heart rate variability
May, L. E., Knowlton, J., Hanson, J., Suminski, R., Paynter, C., Fang, X., & Gustafson, K. M. (2016) · PM&R · doi:10.1016/j.pmrj.2015.11.006 · Cited by 49 · see citing works
Self-citationThe transition to parenthood in obstetrics: enhancing prenatal care for 2-generation impact
Monk, C., Dimidjian, S., Galinsky, E., Gregory, K. D., Hoffman, M. C., Howell, E. A., Miller, E. S., Osborne, C., Rogers, C. E., Saxbe, D. E., et al. (2022) · American Journal of Obstetrics & Gynecology MFM · doi:10.1016/j.ajogmf.2022.100678 · Cited by 19 · see citing works
- Authors
- May, L. E., Glaros, A., Yeh, H.-W., Clapp, J. F., & Gustafson, K. M.
- Affiliations
- Kansas City University (US)
- University of Kansas Medical Center (US)
- Case Western Reserve University (US)
- Corresponding author
- May, Linda E.
- Venue
- Early Human Development
- Publisher
- Elsevier BV
- Published
- 2010-04
- Volume
- 86
- Issue
- 4
- Pages
- 213-217
- ISSN
- 0378-3782 (ISSN-L)
- OpenAlex
- W2032721430
- Cited by
- 140
- References
- 67
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 4 · 2023: 8 · 2022: 9 · 2021: 7 · 2020: 12 · 2019: 9 · 2018: 5 · 2017: 11 · 2016: 13 · 2015: 11 · 2014: 16 · 2013: 8 · 2012: 8
- FWCI
- 4.99
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Early Human Development (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Kansas
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Health Sciences › Medicine › Physiology › Physical Activity and Health
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- pregnancy, fetal heart rate, heart rate variability, fetal magnetocardiography, fetal heart development, gestational age
- MeSH terms
- Autonomic Nervous System, Female, Heart Rate, Fetal, Humans, Longitudinal Studies, Male, Pregnancy, Prospective Studies, Surveys and Questionnaires, Exercise, Magnetocardiography
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review