Early Human Development
Volume 86, Issue 4 , Pages 213-217 , April 2010

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

  • Linda E. May

      Affiliations

    • Department of Anatomy, Kansas City University of Medicine and Biosciences (KCUMB) Kansas City, MO, USA
    • Corresponding Author InformationCorresponding author. 1750 Independence Ave, SEP 463, Kansas City, MO 64106. Tel.: +1 816 283 2228 (office); fax: +1 816 283 2373.
  • ,
  • Alan Glaros

      Affiliations

    • Department of Basic Medical Sciences, KCUMB, Kansas City, MO, USA
  • ,
  • Hung-Wen Yeh

      Affiliations

    • Department of Biostatistics, University of Kansas Medical Center (KUMC) Kansas City, KS, 66160, USA
  • ,
  • James F. Clapp III

      Affiliations

    • Department of Reproductive Biology, Case Western Reserve University, Cleveland, OH, USA
  • ,
  • Kathleen M. Gustafson

      Affiliations

    • Hoglund Brain Imaging Center, Department of Neurology, KUMC, Kansas City, KS, USA

Received 7 December 2009 ,Revised 5 March 2010 ,Accepted 8 March 2010.

References 

  1. Georgieff MK. Nutrition and the developing brain: nutrient priorities and measurement. Am J Clin Nutr. 2007;85(2):614S–620S
  2. Johansson S, Norman M, Legnevall L, Dalmaz Y, Lagercrantz H, Vanpee M. Increased catecholamines and heart rate in children with low birth weight: perinatal contributions to sympathoadrenal overactivity. J Int Med. 2007;261(5):480–487
  3. Wadhwa PD, Culhane JF, Rauh V, Barve SS. Stress and preterm birth: neuroendocrine, immune/inflammatory, and vascular mechanisms. Matern Child Health J. 2001;5(2):119–125
  4. Satpathy HK, Fleming A, Frey D, Barsoom M, Satpathy C, Khandalavala J. Maternal obesity and pregnancy. Postgrad Med. 2008;120(3):E01–E09
  5. Phillips DI. External influences on the fetus and their long-term consequences. Lupus. 2006;15(11):794–800
  6. Waterland RA, Michels KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007;27:363–388
  7. Clapp JF, III. Long-term outcome after exercising throughout pregnancy: fitness and cardiovascular risk. Am J Obstet Gynecol 2008;199(5):489 e1-6.
  8. Adamu B, Sani MU, Abdu A. Physical exercise and health: a review. Niger J Med. 2006;15(3):190–196
  9. Downs DS, DiNallo JM, Kirner TL. Determinants of pregnancy and postpartum depression: prospective influences of depressive symptoms, body image satisfaction, and exercise behavior. Ann Behav Med. 2008;36(1):54–63
  10. Clapp JF. Exercise during pregnancy, a clinical update. Clin Sports Med. 2000;19(2):273–286
  11. Clapp JF. Influence of endurance exercise and diet on human placental development and fetal growth. Placenta. 2006;27(6–7):527–534
  12. Clapp JF, Kiess W. Effects of pregnancy and exercise on concentrations of the metabolic markers tumor necrosis factor alpha and leptin. Am J Obstet Gynecol. 2000;182(2):300–306
  13. Clapp JF, Kim H, Burciu B, Schmidt S, Petry K, Lopez B. Continuing regular exercise during pregnancy: effect of exercise volume on fetoplacental growth. Am J Obstet Gynecol. 2002;186(1):142–147
  14. Clapp JF. Effects of diet and exercise on insulin resistance during pregnancy. Metab Syndr Relat Disord. 2006;4(2):84–90
  15. Veille JC. Maternal and fetal cardiovascular response to exercise during pregnancy. Semin Perinatol. 1996;20(4):250–262
  16. Jarski RW, Trippett DL. The risks and benefits of exercise during pregnancy. J Fam Pract. 1990;30(2):185–189
  17. Clapp JF. A clinical approach to exercise during pregnancy. Clin Sports Med. 1994;13(2):443–458
  18. Artal R. Exercise and pregnancy. Clin Sports Med. 1992;11(2):363–377
  19. Artal R, Wiswell R, Romem Y, Dorey F. Pulmonary responses to exercise in pregnancy. Am J Obstet Gynecol. 1986;154(2):378–383
  20. Collings CA, Curet LB, Mullin JP. Maternal and fetal responses to a maternal aerobic exercise program. Am J Obstet Gynecol. 1983;145(6):702–707
  21. Cooper KA, Hunyor SN, Boyce ES, O'Neill ME, Frewin DB. Fetal heart rate and maternal cardiovascular and catecholamine responses to dynamic exercise. Aust NZ J Obstet Gynaecol. 1987;27(3):220–223
  22. Hatoum N, Clapp JF, Newman MR, Dajani N, Amini SB. Effects of maternal exercise on fetal activity in late gestation. J Matern Fetal Med. 1997;6(3):134–139
  23. Lotgering FK, Gilbert RD, Longo LD. Maternal and fetal responses to exercise during pregnancy. Physiol Rev. 1985;65(1):1–36
  24. Galland BC, Taylor BJ, Bolton DP, Sayers RM. Heart rate variability and cardiac reflexes in small for gestational age infants. J Appl Physiol. 2006;100(3):933–939
  25. Van Leeuwen P, Lange S, Bettermann H, Gronemeyer D, Hatzmann W. Fetal heart rate variability and complexity in the course of pregnancy. Early Hum Dev. 1999;54(3):259–269
  26. Wakai RT, Wang M, Martin CB. Spatiotemporal properties of the fetal magnetocardiogram. Am J Obstet Gynecol. 1994;170(3):770–776
  27. Verklan MT, Padhye NS, Brazdeikis A. Analysis of fetal heart rate variability obtained by magnetocardiography. J Perinat Neonatal Nurs. 2006;20(4):343–348
  28. Kriska AM, Bennett PH. An epidemiological perspective of the relationship between physical activity and NIDDM: from activity assessment to intervention. Diabetes Metab Rev. 1992;8(4):355–372
  29. Kriska AM, Knowler WC, LaPorte RE, Drash AL, Wing RR, Blair SN, et al. Development of questionnaire to examine relationship of physical activity and diabetes in Pima Indians. Diabetes Care. 1990;13(4):401–411
  30. Aaron DJ, Kriska AM, Dearwater SR, Anderson RL, Olsen TL, Cauley JA, et al. The epidemiology of leisure physical activity in an adolescent population. Med Sci Sports Exerc. 1993;25(7):847–853
  31. Aaron DJ, Dearwater SR, Anderson R, Olsen T, Kriska AM, Laporte RE. Physical activity and the initiation of high-risk health behaviors in adolescents. Med Sci Sports Exerc. 1995;27(12):1639–1645
  32. Schulz LO, Harper IT, Smith CJ, Kriska AM, Ravussin E. Energy intake and physical activity in Pima Indians: comparison with energy expenditure measured by doubly-labeled water. Obes Res. 1994;2(6):541–548
  33. Kimm SY, Glynn NW, Kriska AM, Barton BA, Kronsberg SS, Daniels SR, et al. Decline in physical activity in black girls and white girls during adolescence. N Engl J Med. 2002;347(10):709–715
  34. Cramp AG, Bray SR. A prospective examination of exercise and barrier self-efficacy to engage in leisure-time physical activity during pregnancy. Ann Behav Med. 2009;37(3):325–334
  35. Cramp AG, Bray SR. Pre- and postnatal women's leisure time physical activity patterns: a multilevel longitudinal analysis. Res Q Exerc Sport. 2009;80(3):403–411
  36. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods. 2004;134(1):9–21
  37. Popescu EA, Popescu M, Bennett TL, Lewine JD, Drake WB, Gustafson KM. Magnetographic assessment of fetal hiccups and their effect on fetal heart rhythm. Physiol Meas. 2007;28:665–676
  38. Popescu EA, Popescu M, Wang J, Barlow SM, Gustafson KM. Non-nutritive sucking recorded in utero via fetal magnetography. Physiol Meas. 2008;29(1):127–139
  39. Electronic fetal heart rate monitoring: research guidelines for interpretation. National Institute of Child Health and Human Development Research Planning Workshop. Am J Obstet Gynecol. 1997;177(6):1385–1390
  40. David M, Hirsch M, Karin J, Toledo E, Akselrod S. An estimate of fetal autonomic state by time-frequency analysis of fetal heart rate variability. J Appl Physiol. 2007;102(3):1057–1064
  41. Van Leeuwen P, Geue D, Lange S, Hatzmann W, Gronemeyer D. Changes in the frequency power spectrum of fetal heart rate in the course of pregnancy. Prenat Diagn. 2003;23(11):909–916
  42. Wakai RT, Wang M, Pedron SL, Reid DL, Martin CB. Spectral analysis of antepartum fetal heart rate variability from fetal magnetocardiogram recordings. Early Hum Dev. 1993;35(1):15–24
  43. Nijhuis IJ, ten Hof J. Development of fetal heart rate and behavior: indirect measures to assess the fetal nervous system. Eur J Obstet Gynecol Reprod Biol. 1999;87(1):1–2
  44. Ten Hof J, Nijhuis IJ, Mulder EJ, Nijhuis JG, Narayan H, Taylor DJ, et al. Longitudinal study of fetal body movements: nomograms, intrafetal consistency, and relationship with episodes of heart rate patterns A and B. Pediatr Res. 2002;52(4):568–575
  45. Verbeke G, Molenberghs G, Thijs H, Lesaffre E, Kenward MG. Sensitivity analysis for nonrandom dropout: a local influence approach. Biometrics. 2001;57(1):7–14
  46. Brenner IK, Wolfe LA, Monga M, McGrath MJ. Physical conditioning effects on fetal heart rate responses to graded maternal exercise. Med Sci Sports Exerc. 1999;31(6):792–799
  47. Clapp JF. Exercise and fetal health. J Dev Physiol. 1991;15(1):9–14
  48. Clapp JF. The effects of maternal exercise on fetal oxygenation and feto-placental growth. Eur J Obstet Gynecol Reprod Biol. 2003;110(Suppl 1):S80–S85
  49. Clapp JF, Little KD, Widness JA. Effect of maternal exercise and fetoplacental growth rate on serum erythropoietin concentrations. Am J Obstet Gynecol. 2003;188(4):1021–1025
  50. Gilbert RD, Lis L, Longo LD. Temperature effects on oxygen affinity of human fetal blood. J Dev Physiol. 1985;7(5):299–304
  51. Kennelly MM, Geary M, McCaffrey N, McLoughlin P, Staines A, McKenna P. Exercise-related changes in umbilical and uterine artery waveforms as assessed by Doppler ultrasound scans. Am J Obstet Gynecol. 2002;187(3):661–666
  52. Marsal K. Intrauterine growth restriction. Curr Opin Obstet Gynecol. 2002;14(2):127–135
  53. Spinnewijn WE, Lotgering FK, Struijk PC, Wallenburg HC. Fetal heart rate and uterine contractility during maternal exercise at term. Am J Obstet Gynecol. 1996;174(1 Pt 1):43–48
  54. Giroux I, Inglis SD, Lander S, Gerrie S, Mottola MF. Dietary intake, weight gain, and birth outcomes of physically active pregnant women: a pilot study. Appl Physiol Nutr Metab. 2006;31(5):483–489
  55. Collings C, Curet LB. Fetal heart rate response to maternal exercise. Am J Obstet Gynecol. 1985;151(4):498–501
  56. DiPietro JA, Costigan KA, Pressman EK, Doussard-Roosevelt JA. Antenatal origins of individual differences in heart rate. Dev Psychobiol. 2000;37(4):221–228
  57. Pillai M, James D. The development of fetal heart rate patterns during normal pregnancy. Obstet Gynecol. 1990;76(5 Pt 1):812–816
  58. Woo MA, Stevenson WG, Moser DK, Middlekauff HR. Complex heart rate variability and serum norepinephrine levels in patients with advanced heart failure. J Am Coll Cardiol. 1994;23(3):565–569
  59. Thomas SA, Matsumoto AM, Palmiter RD. Noradrenaline is essential for mouse fetal development. Nature. 1995;374(6523):643–646
  60. Sodha RJ, Proegler M, Schneider H. 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;148(4):474–481
  61. Nandakumaran M, Gardey C, Rey E, Challier JC, Panigel M, Olive G. Transfer of ritodrine and norepinephrine in human placenta: in vitro study. Dev Pharmacol Ther. 1982;4(1–2):71–80
  62. Morgan CD, Sandler M, Panigel M. Placental transfer of catecholamines in vitro and in vivo. Am J Obstet Gynecol. 1972;112(8):1068–1075
  63. Clapp JF. Morphometric and neurodevelopmental outcome at age five years of the offspring of women who continued to exercise regularly throughout pregnancy. J Pediatr. 1996;129(6):856–863
  64. Impact of physical activity during pregnancy and postpartum on chronic disease risk. Med Sci Sports Exerc. 2006;38(5):989–1006
  65. Watts K, Jones TW, Davis EA, Green D. Exercise training in obese children and adolescents: current concepts. Sports Med. 2005;35(5):375–392

PII: S0378-3782(10)00061-7

doi: 10.1016/j.earlhumdev.2010.03.002

Early Human Development
Volume 86, Issue 4 , Pages 213-217 , April 2010