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Fetal Breathing Movements and Changes at Birth

Conference paper
First Online:
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 814)

Abstract

The fetus, which develops within a fluid-filled amniotic sac, relies on the placenta for respiratory gas exchange rather than the lungs. While not involved in fetal oxygenation, fetal breathing movements (FBM) nevertheless have an important role in lung growth and in development of respiratory muscles and neural regulation. FBM are regulated differently in many respects than postnatal respiration, which results from the unique intrauterine environment. Prominent distinctions of FBM include its episodic nature and apnea-sensitivity to hypoxia. The latter characteristic is the basis for using FBM in the assessment of fetuses at risk for hypoxic injury. At birth, the transition to continuous postnatal respiration involves a fall in temperature, gaseous distention of the lungs, activation of the Hering-Breuer reflexes, and functional connectivity of afferent O2 chemoreceptor activity with respiratory motoneurons and arousal centers. Importantly, exposure to drugs or adverse conditions in utero not only can change patterns of FBM but also can lead to epigenetic dysregulation in postnatal respiration. Such changes, can blunt respiratory and arousal defenses against hypoxic challenges in sleep. Thus, fetal hypoxia and/or drug exposure may in later life dispose sleeping infants, children, and adults to hypertension, diabetes mellitus, brain injury, and sudden death.

Keywords

Brain Carotid body Fetus Hypoxia Newborn Respiration Sleep 
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Notes

Acknowledgment

Supported in part by National Institute of Child Health and Human Development Grant HD-18478

References

  1. 1.
    Preyer W. Specielle physiologie des embryos: untersuchungenüber die lebenserscheiunungen vor de gebart. Leipzig: T Grieban; 1885.Google Scholar
  2. 2.
    Rosenfeld M, Snyder FF. Fetal respiration in rabbits. Proc Soc Exp Biol Med. 1936;33:576–8.CrossRefGoogle Scholar
  3. 3.
    Bonar BE, Blumenfeld CM, Fenning C. Studies of fetal respiratory movements 1. Historical and present day observations. Am J Dis Child. 1938;55:1–11.CrossRefGoogle Scholar
  4. 4.
    Barcroft J, Barron DH. The genesis of respiratory movements in the fetus of the sheep. J Physiol. 1936;88:56–61.PubMedCentralPubMedGoogle Scholar
  5. 5.
    Dawes GS. Foetal and neonatal physiology. Chicago, IL: Yearbook Medical; 1968. p. 129–36.Google Scholar
  6. 6.
    Windle WF, Becker RF, Barth EE, Schultz MD. Aspiration of amniotic fluid by the fetus. An experimental roentgenological study in the guinea pig. Surg Gynecol Obstet. 1939;69:705–12.Google Scholar
  7. 7.
    Dawes GS, Fox HE, Leduc BM, Liggins GC, Richards RT. Respiratory movements and rapid eye movement sleep in the foetal lamb. J Physiol. 1972;220:119–43.PubMedCentralPubMedGoogle Scholar
  8. 8.
    von Ahlfeld F. Die intrauterine tatigkeit der thorax-und zwerchfellmus kulatur: intrauterine atmung. Monatsschr Geburtshilfe Gynakol. 1905;21:143–69.Google Scholar
  9. 9.
    Reifferscheid K. Ueber intrauterine Atembewegungen des foetus. Dtsch Med Wochenschr. 1911;37:877–80.CrossRefGoogle Scholar
  10. 10.
    Dawes GS. The central control of fetal breathing and skeletal movements. J Physiol. 1984;346:1–18.PubMedCentralPubMedGoogle Scholar
  11. 11.
    Boddy K, Mantell CD. Observations of fetal breathing movements transmitted through maternal abdominal wall. Lancet. 1972;2:1219–20.PubMedCrossRefGoogle Scholar
  12. 12.
    Boddy K, Robinson JS. External method for detection of fetal breathing in utero. Lancet. 1971;2:1231–3.PubMedCrossRefGoogle Scholar
  13. 13.
    Boyce ES, Dawes GS, Gough JD, Poore ER. Doppler ultrasound method for detecting human fetal breathing in utero. Br Med J. 1976;2:17–8.PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Marsál K, Gennser G, Hansson GA, Lindstrom K, Mauritzsson L. New ultrasonic device for monitoring fetal breathing movements. Biomed Eng. 1976;11:47–52.PubMedGoogle Scholar
  15. 15.
    Bissonnette JM. Mechanisms regulating hypoxic respiratory depression during fetal and postnatal life. Am J Physiol Regul Integr Comp Physiol. 2000;278:R1391–400.PubMedGoogle Scholar
  16. 16.
    Koos BJ. Breathing and sleep states in the fetus and at birth. In: Marcus CL, Carroll JL, Donnelly DF, Loughlin GM, editors. Sleep and breathing in children: developmental changes in breathing during sleep. 2nd ed. New York, NY: Informa Healthcare; 2008. p. 1–17.Google Scholar
  17. 17.
    Harding R, Hooper SB. Regulation of lung expansion and lung growth before birth. J Appl Physiol. 1996;81:209–24.PubMedGoogle Scholar
  18. 18.
    Houghton DC, Walker DW, Young IR, McMillen IC. Melatonin and the light-dark cycle separately influence daily behavioral and hormonal rhythms in the pregnant ewe and sheep fetus. Endocrinology. 1993;133:90–8.PubMedGoogle Scholar
  19. 19.
    McMillen IC, Nowak R, Walker DW, Young IR. Maternal pinealectomy alters the daily pattern of fetal breathing in sheep. Am J Physiol. 1990;258:R284–7.PubMedGoogle Scholar
  20. 20.
    Richardson B, Hohimer AR, Mueggler P, Bissonnette J. Effects of glucose concentration on fetal breathing movements and electrocortical activity in fetal lambs. Am J Obstet Gynecol. 1982;142:678–83.PubMedGoogle Scholar
  21. 21.
    Koos BJ, Matsuda K, Power GG. Fetal breathing and cardiovascular responses to graded methemoglobinemia in sheep. J Appl Physiol. 1990;69:136–40.PubMedGoogle Scholar
  22. 22.
    Koos BJ, Chau A, Matsuura M, Punla O, Kruger L. Thalamic locus mediates hypoxic inhibition of breathing in fetal sheep. J Neurophysiol. 1998;79:2383–93.PubMedGoogle Scholar
  23. 23.
    Koos BJ, Kawasaki Y, Hari A, Bohorquez F, Jan C, Roostaeian J, et al. Electrical stimulation of the posteromedial thalamus modulates breathing in unanesthetized fetal sheep. J Appl Physiol. 2004;96:115–23.PubMedCrossRefGoogle Scholar
  24. 24.
    Hooper SB, Harding R. Changes in lung liquid dynamics induced by prolonged fetal hypoxemia. J Appl Physiol. 1990;69:127–35.PubMedGoogle Scholar
  25. 25.
    Tiktinsky-Rupp MH, Hasan SU, Bishop B, Morin III FC. Hyperbaric oxygenation increases arousal and breathing movements in fetal lambs. J Appl Physiol. 1994;77:902–11.PubMedGoogle Scholar
  26. 26.
    Blanco CE, Chen V, Maertzdorf W, Bamford OS, Hanson M. Effect of hyperoxia (PaO2 50–90 mmHg) on fetal breathing movements in the unanesthetized fetal sheep. J Dev Physiol. 1990;14:235–41.PubMedGoogle Scholar
  27. 27.
    Hohimer AR, Bissonnette JM, Richardson BS, Machida CM. Central chemical regulation of breathing movements in fetal lambs. Respir Physiol. 1983;52:99–111.PubMedCrossRefGoogle Scholar
  28. 28.
    Koos BJ. Central stimulation of breathing movements in fetal lambs by prostaglandin synthetase inhibitors. J Physiol. 1985;362:455–66.PubMedCentralPubMedGoogle Scholar
  29. 29.
    Koos BJ, Sameshima H. Effects of hypoxaemia and hypercapnia on breathing movements and sleep state in sinoaortic-denervated fetal sheep. J Dev Physiol. 1988;10:131–44.PubMedGoogle Scholar
  30. 30.
    Gluckman PD, Johnston BM. Lesions in the upper lateral pons abolish hypoxic depression of breathing in unanesthetized fetal lambs. J Physiol. 1987;382:373–83.PubMedCentralPubMedGoogle Scholar
  31. 31.
    Koos BJ. Adenosine A2a receptors and O2 signaling in development. Am J Physiol Regul Integr Comp Physiol. 2011;301:R601–22.PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Koos BJ, Chau A. Fetal cardiovascular and breathing responses to an adenosine A2a receptor agonist in sheep. J Appl Physiol. 1998;72:94–9.Google Scholar
  33. 33.
    Koos BJ, Maeda T, Lopez G. Adenosine A2A receptors mediate hypoxic inhibition of fetal breathing in sheep. Am J Obstet Gynecol. 2002;186:663–8.PubMedCrossRefGoogle Scholar
  34. 34.
    Koos BJ, Mason B, Ogunyemi D, Punla O, Adinolfi A. Hypoxic inhibition of breathing in fetal sheep: relation to brain adenosine concentrations. J Appl Physiol. 1994;77:2734–9.PubMedGoogle Scholar
  35. 35.
    Blanco CE, Dawes GS, Hanson MA, McCooke MB. The response to hypoxia of arterial chemoreceptors in fetal sheep and new-born lambs. J Physiol. 1984;351:25–37.PubMedCentralPubMedGoogle Scholar
  36. 36.
    Murai DT, Lee CC, Wallen LD, Kitterman JA. Denervation of peripheral chemoreceptors decreases breathing movements in fetal sheep. J Appl Physiol. 1985;59:575–9.PubMedGoogle Scholar
  37. 37.
    Johnston BM, Gluckman PD. Peripheral chemoreceptors respond to hypoxia in pontine-lesioned fetal lambs in utero. J Appl Physiol. 1993;75:1027–34.PubMedGoogle Scholar
  38. 38.
    Koos BJ, Chao A, Doany W. Adenosine stimulates breathing in fetal sheep with brain stem section. J Appl Physiol. 1992;72:94–9.PubMedGoogle Scholar
  39. 39.
    Kitterman JA, Liggins GC, Clements JA, Tooley WH. Stimulation of breathing movements in fetal sheep by inhibitors of prostaglandin synthesis. J Dev Physiol. 1979;1:453–66.PubMedGoogle Scholar
  40. 40.
    Gluckman PD, Gunn TR, Johnston BM. The effect of cooling on breathing and shivering in unanesthetized fetal lambs in utero. J Physiol. 1983;343:495–506.PubMedCentralPubMedGoogle Scholar
  41. 41.
    Baier FJ, Hasan SU, Cates DB, Hooper D, Nowaczyk B, Rigatto H. Effects of various concentrations of O2 and umbilical cord occlusion on fetal breathing and behavior. J Appl Physiol. 1990;68:1597–604.PubMedGoogle Scholar
  42. 42.
    Hasan SU, Rigaux A. Effect of bilateral vagotomy on oxygenation, arousal, and breathing movements in fetal sheep. J Appl Physiol. 1992;73:1402–12.PubMedGoogle Scholar
  43. 43.
    Nijhuis JG, Prechtl HF, Martin Jr CB, Bots RS. Are there behavioural states in the human fetus? Early Hum Dev. 1982;6:177–95.PubMedCrossRefGoogle Scholar
  44. 44.
    Arduini D, Rizzo G, Giorlandino C, Valensise H, Dell’Acqua S, Romanini C. The development of fetal behavioural states: a longitudinal study. Prenat Diagn. 1986;6:117–24.PubMedCrossRefGoogle Scholar
  45. 45.
    Cosmi EV, Cosmi E, La Torre R. The effects of fetal breathing movements on the utero-fetal-placental circulation. Early Pregnancy. 2001;5:51–2.PubMedGoogle Scholar
  46. 46.
    Nyberg MK, Johnsen SL, Rasmussen S, Kiserud T. Hemodynamics of fetal breathing movements: the inferior vena cava. Ultrasound Obstet Gynecol. 2011;38:658–64.PubMedCrossRefGoogle Scholar
  47. 47.
    Patrick J, Campbell K, Carmichael L, Natale R, Richardson B. Patterns of human fetal breathing during the last 10 weeks of pregnancy. Obstet Gynecol. 1980;56:24–30.PubMedGoogle Scholar
  48. 48.
    Patrick J, Campbell K, Carmichael L, Natale R, Richardson B. A definition of human apnea and the distribution of fetal apneic intervals during the last ten weeks of pregnancy. Am J Obstet Gynecol. 1980;136:471–7.PubMedGoogle Scholar
  49. 49.
    Yeoshoua E, Goldstein I, Zlozover M, Wiener Z. Sonographic study of the relationship between gestational diabetes and fetal activity. J Matern Fetal Neonatal Med. 2012;25:623–6.PubMedCrossRefGoogle Scholar
  50. 50.
    Platt LD, Manning FA, Lemay M, Sipos L. Human fetal breathing: relationship to fetal condition. Am J Obstet Gynecol. 1978;132:514–8.PubMedGoogle Scholar
  51. 51.
    Herrington RT, Harned Jr HS, Ferreiro JI, Griffin III CA. The role of the central nervous system in perinatal respiration: studies of chemoregulatory mechanisms in the term lamb. Pediatrics. 1971;47:857–64.PubMedGoogle Scholar
  52. 52.
    Chou PJ, Ullrich JR, Ackerman BD. Time of onset of effective respiration at birth. Biol Neonate. 1974;24:74–81.PubMedCrossRefGoogle Scholar
  53. 53.
    Barcroft J. Researches on pre-natal life, vol. 1. Oxford: Blackwell Scientific; 1946. p. 267–76.Google Scholar
  54. 54.
    Rosen CL. Maturation of breathing during sleep. In: Marcus CL, Carroll JL, Donnelly DF, Loughlin GM, editors. Sleep and breathing in children: developmental changes in breathing during sleep. 2nd ed. New York, NY: Informa Healthcare; 2008. p. 117–30.Google Scholar
  55. 55.
    Carroll JL, Donnelly DF. Postnatal development of carotid chemoreceptor function. In: Marcus CL, Carroll JL, Donnelly DF, Loughlin GM, editors. Sleep and breathing in children: developmental changes in breathing during sleep. 2nd ed. New York, NY: Informa Healthcare; 2008. p. 47–73.Google Scholar
  56. 56.
    Gozal D, Harper RM. Maturation and plasticity of central components in cardiovascular and respiratory control. In: Marcus CL, Carroll JL, Donnelly DF, Loughlin GM, editors. Sleep and breathing in children: developmental changes in breathing during sleep. 2nd ed. New York, NY: Informa Healthcare; 2008. p. 83–104.Google Scholar
  57. 57.
    Isono S. Interaction between upper airway muscles and structures during sleep. In: Marcus CL, Carroll JL, Donnelly DF, Loughlin GM, editors. Sleep and breathing in children: developmental changes in breathing during sleep. 2nd ed. New York, NY: Informa Healthcare; 2008. p. 131–52.Google Scholar
  58. 58.
    Alvaro R, Rigatto H. Breathing and sleep in preterm infants. In: Marcus CL, Carroll JL, Donnelly DF, Loughlin GM, editors. Sleep and breathing in children: developmental changes in breathing during sleep. 2nd ed. New York, NY: Informa Healthcare; 2008. p. 177–210.Google Scholar
  59. 59.
    Carroll JL, Canet E, Bureau MA. Dynamic ventilatory responses to CO2 in the awake lamb: role of the carotid chemoreceptors. J Appl Physiol. 1991;71:2198–205.PubMedGoogle Scholar
  60. 60.
    Kawai A, Onimaru H, Homma I. Mechanisms of CO2/H+ chemoreception by respiratory rhythm generator neurons in the medulla from newborn rats in vitro. J Physiol. 2006;572:525–37.PubMedCentralPubMedCrossRefGoogle Scholar
  61. 61.
    Koos BJ, Kawasaki Y, Kim YH, Bohorquez F. Adenosine A2A receptor blockade abolishes the roll-off respiratory response to hypoxia in awake lambs. Am J Physiol Regul Integr Comp Physiol. 2005;288:R1185–94.PubMedCrossRefGoogle Scholar
  62. 62.
    Rajaee A, Ibe B, Guerra C, Husain S, Kruger L, Koos BJ. Thalamic locus mediates hypoxic respiratory depression in lambs. Reprod Sci. 2013;20(Suppl):221A.Google Scholar
  63. 63.
    Blyton DM, Skilton MR, Edwards N, Hennessy A, Celermajer DS, Sullivan CE. Treatment of sleep disordered breathing reverses low fetal activity levels in preeclampsia. Sleep. 2013;36:15–21.PubMedCentralPubMedGoogle Scholar
  64. 64.
    Bourjeily G, Barbara N, Larson L, He M. Clinical manifestations of obstructive sleep apnoea in pregnancy: more than snoring and witnessed apnoeas. J Obstet Gynaecol. 2012;32:434–8.PubMedCrossRefGoogle Scholar
  65. 65.
    O’Brien LM. Positive airway pressure as a therapy for preeclampsia? Sleep. 2013;36:5–6.PubMedCentralPubMedGoogle Scholar
  66. 66.
    Reid J, Skomro R, Cotton D, Ward H, Olatunbosun F, Gjevre J, et al. Pregnant women with gestational hypertension may have a high frequency of sleep disordered breathing. Sleep. 2011;34:1033–8.PubMedCentralPubMedGoogle Scholar
  67. 67.
    Tauman R, Many A, Deutsch V, Arvas S, Ascher-Landsberg J, Greenfeld M, et al. Maternal snoring during pregnancy is associated with enhanced fetal erythropoiesis—a preliminary study. Sleep Med. 2011;12:518–22.PubMedCrossRefGoogle Scholar
  68. 68.
    Fleming P, Blair PS. Sudden infant deaths: risk factors, contributory factors, and causal factors. In: Marcus CL, Carroll JL, Donnelly DF, Loughlin GM, editors. Sleep and breathing in children, second edition: developmental changes in breathing during sleep. New York, NY: Informa Healthcare; 2008. p. 47–73.Google Scholar
  69. 69.
    Thach BT. Pathophysiology of sudden infant death syndrome. In: Marcus CL, Carroll JL, Donnelly DF, Loughlin GM, editors. Sleep and breathing in children, second edition: developmental changes in breathing during sleep. New York, NY: Informa Healthcare; 2008. p. 255–68.Google Scholar

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© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of Obstetrics and Gynecology, Brain Research Institute, David Geffen School of MedicineUniversity of California Los AngelesLos AngelesUSA

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