Advertisement

Perinatal Physiology

  • Carlos E. BlancoEmail author
  • Eduardo Villamor
Reference work entry

Abstract

This chapter will discuss the mechanisms preparing the fetus to be born, the transition at birth, and the successful adaptation to the air-breathing world. This chapter will review the respiratory system including lung development, maturation, and role of surfactant system and the respiratory drive and chemoreceptor role and the circulatory system including fetal circulation and its changes at birth.

Keywords

Fetus Fetal breathing Lung development Birth Pulmonary circulation Ductus arteriosus Control of breathing 

Notes

Acknowledgments

This chapter has been adapted from the author’s own chapter in the following publication: Copyright © 2011 From Newborn Surgery, Third Edition, by Prem Puri. Reproduced by permission of Taylor and Francis Group, LLC, a division of Informa plc.

References

  1. Aaronson PI, Robertson TP, Knock GA, Becker S, Lewis TH, Snetkov V, et al. Hypoxic pulmonary vasoconstriction: mechanisms and controversies. J Physiol. 2006;570(Pt 1):53–8.PubMedCrossRefPubMedCentralGoogle Scholar
  2. Abman SH. Abnormal vasoreactivity in the pathophysiology of persistent pulmonary hypertension of the newborn. Pediatr Rev. 1999;20(11):e103–9.PubMedCrossRefPubMedCentralGoogle Scholar
  3. Abman SH, Stevens T. Perinatal pulmonary vasoregulation: implications for the pathophysiology and treatment of neonatal pulmonary hypertension. In: Haddad G, Lister G, editors. Tissue oxygen deprivation: developmental, molecular and integrative function. New York: Marcel Dekker; 1996. p. 367–432.Google Scholar
  4. Abman SH, Accurso FJ, Wilkening RB, Meschia G. Persistent fetal pulmonary hypoperfusion after acute hypoxia. Am J Phys. 1987;253(4 Pt 2):H941–8.Google Scholar
  5. Abman SH, Chatfield BA, Rodman DM, Hall SL, McMurtry IF. Maturational changes in endothelium-derived relaxing factor activity of ovine pulmonary arteries in vitro. Am J Phys. 1991;260(4 Pt 1):L280–5.Google Scholar
  6. Adamson SL, Richardson BS, Homan J. Initiation of pulmonary gas exchange by fetal sheep in utero. J Appl Physiol. 1987;62(3):989–98.PubMedCrossRefPubMedCentralGoogle Scholar
  7. Adamson SL, Kuipers IM, Olson DM. Umbilical cord occlusion stimulates breathing independent of blood gases and pH. J Appl Physiol. 1991;70:1796–809.PubMedCrossRefPubMedCentralGoogle Scholar
  8. Alvaro RE, Hasan SU, Chemtob S, Qurashi M, Al-Saif S, Rigatto H. Prostaglandins are responsible for the inhibition of breathing observed with a placental extract in fetal sheep. Respir Physiol Neurobiol. 2004;144(1):35–44.PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bahoric A, Chernick V. Electrical activity of phrenic nerve and diaphragm in utero. J Appl Physiol. 1975;39:513–8.PubMedCrossRefPubMedCentralGoogle Scholar
  10. Barcroft J. The brain and its environment. New Haven: Yale University Press; 1938. p. 44.Google Scholar
  11. Barcroft J. Researches on pre-natal life. Springfield: Charles C Thomas Publisher; 1946. p. 261–6.Google Scholar
  12. Bartelds B, Van Bel F, Teitel DF, et al. Carotid, not aortic, chemoreceptors mediate the fetal cardiovascular response to acute hypoxemia in lambs. Pediatr Res. 1993;34(1):51–5.PubMedCrossRefGoogle Scholar
  13. Bennet L, Gluckman PD, Johnston BM. The effects of corticotrophin-releasing hormone on breathing movements and electrocortical activity of the fetal sheep. J Physiol. 1988;23:72–5.Google Scholar
  14. Bennet L, Johnston BM, Vale WW, et al. The central effects of thyrotropin-releasing factor and two antagonists on breathing movements in fetal sheep. J Physiol. 1990;421:1–11.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Blanco CE, Dawes GS, Hanson MA, et al. The arterial chemoreceptors in fetal sheep and newborn lambs. J Physiol. 1982;330:38P.Google Scholar
  16. Blanco CE, Dawes GS, Walker DW. Effects of hypoxia on polysynaptic hind-limb reflexes of unanaesthetized fetal and new-born lambs. J Physiol. 1983a;339:453–66.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Blanco CE, Dawes GS, Walker DW. Effects of hypoxia on polysynaptic hind-limb reflexes in new-born lambs before and after carotid denervation. J Physiol. 1983b;339:467–74.PubMedPubMedCentralCrossRefGoogle Scholar
  18. Blanco CE, Dawes GS, Hanson MA, et al. The response to hypoxia of arterial chemoreceptors in fetal sheep and newborn lambs. J Physiol. 1984;351:25–37.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Blanco CE, Martin CB, Rankin J, Landauer M, Phernetton T. Changes in fetal organ flow during intrauterine mechanical ventilation with or without oxygen. J Dev Physiol. 1988a;10(1):53–62.PubMedGoogle Scholar
  20. Blanco CE, Hanson MA, McCoocke HB. Effects on carotid chemoreceptor resetting of pulmonary ventilation in the fetal lamb in utero. J Dev Physiol. 1988b;10:167–74.PubMedGoogle Scholar
  21. Boddy K, Dawes GS, Fisher R, et al. Foetal respiratory movements, electrocortical activity and cardiovascular responses to hypoxaemia and hypercapnia in sheep. J Physiol. 1974;243:599–618.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Bouayad A, Hou X, Varma DR, Clyman RI, Fouron J-C, Chemtob S. Cyclooxygenase isoforms and prostaglandin E2 receptors in the ductus arteriosus. Curr Ther Res. 2002;63(10):669–81.CrossRefGoogle Scholar
  23. Bowes G, Adamson TM, Ritchie BC, et al. Development of patterns of respiratory activity in unanaesthetized fetal sheep in utero. J Appl Physiol Respir Environ Exerc Physiol. 1981;50:693–700.PubMedGoogle Scholar
  24. Bystrzycka E, Nail B, Purves MJ. Central and peripheral neural respiratory activity in the mature sheep fetus and newborn lamb. Respir Physiol. 1975;25:199–215.PubMedCrossRefGoogle Scholar
  25. Clewlow R, Dawes GS, Johnston BM, Walker DW. Changes in breathing, electrocortical and muscle activity in unanaesthetized fetal lambs with age. J Physiol. 1983;341:463–76.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Clyman RI. Mechanisms regulating closure of the ductus arteriosus. In: Polin RA, Fox WW, Abman SH, editors. Fetal and neonatal physiology. Philadelphia: Saunders; 2004. p. 743–8.CrossRefGoogle Scholar
  27. Clyman RI. Mechanisms regulating the ductus arteriosus. Biol Neonate. 2006;89(4):330–5.PubMedCrossRefGoogle Scholar
  28. Coceani F, Baragatti B. Mechanisms for ductus arteriosus closure. Semin Perinatol. 2012;36(2):92–7.PubMedCrossRefGoogle Scholar
  29. Contratti G, Banzi C, Ghi T, Perolo A, Pilu G, Visentin A. Absence of the ductus venosus: report of 10 new cases and review of the literature. Ultrasound Obstet Gynecol. 2001;18(6):605–9.PubMedCrossRefGoogle Scholar
  30. Cooke IRC, Berger PH. Precursor of respiratory pattern in the early gestation mammalian fetus. Brain Res. 1990;522:333–6.PubMedCrossRefGoogle Scholar
  31. Cooper EJ, Wareing M, Greenwood SL, Baker PN. Oxygen tension and normalisation pressure modulate nifedipine-sensitive relaxation of human placental chorionic plate arteries. Placenta. 2006;27(4–5):402–10.PubMedCrossRefGoogle Scholar
  32. Crossley KJ, Nicol MB, Hirst JJ, et al. Suppression of arousal by progesterone in fetal sheep. Reprod Fertil Dev. 1997;9:767–73.PubMedCrossRefGoogle Scholar
  33. Cruz-Gonzalez I, Solis J, Kiernan TJ, Yan BP, Lam YY, Palacios IF. Clinical manifestation and current management of patent foramen ovale. Expert Rev Cardiovasc Ther. 2009;7(8):1011–22.PubMedCrossRefGoogle Scholar
  34. Dawes GS. The central control of fetal breathing and skeletal muscle movements. J Physiol. 1984;346:1–18.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Dawes GS, Fox HE, Leduc BM, et al. Respiratory movements and rapid eye movements sleep in the fetal lamb. J Physiol. 1972;220(1):119–43.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Dawes GS, Gardner WN, Johnston BM, et al. Breathing in fetal lambs: the effects of brain stem section. J Physiol. 1983;335:535–53.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dzialowski EM, Sirsat T, van der Sterren S, Villamor E. Prenatal cardiovascular shunts in amniotic vertebrates. Respir Physiol Neurobiol. 2011;178(1):66–74.PubMedCrossRefGoogle Scholar
  38. Echtler K, Stark K, Lorenz M, Kerstan S, Walch A, Jennen L, et al. Platelets contribute to postnatal occlusion of the ductus arteriosus. Nat Med. 2010;16(1):75–82.PubMedCrossRefGoogle Scholar
  39. Everett TR, Peebles DM. Antenatal tests of fetal wellbeing. Semin Fetal Neonatal Med. 2015;20(3):138–43.PubMedCrossRefPubMedCentralGoogle Scholar
  40. Finnemore A, Groves A. Physiology of the fetal and transitional circulation. Semin Fetal Neonatal Med. 2015;20(4):210–6.PubMedCrossRefGoogle Scholar
  41. Fletcher DJ, Hanson MA, Moore PJ, et al. Stimulation of breathing movements by L-5-hydroxytryptophan in fetal sheep during normoxia and hypoxia. J Physiol. 1988;404:575–89.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Gao Y, Raj JU. Regulation of the pulmonary circulation in the fetus and newborn. Physiol Rev. 2010;90(4):1291–335.PubMedCrossRefGoogle Scholar
  43. Garcia-Delgado R, Garcia-Rodriguez R, Romero Requejo A, et al. Echographic features and perinatal outcomes in fetuses with congenital absence of ductus venosus. Acta Obstet Gynecol Scand. 2017;96(10):1205–13.PubMedCrossRefGoogle Scholar
  44. Giussani DA, Spencer JAD, Moore PJ, et al. Afferent and efferent components of the cardiovascular reflex responses to acute hypoxia in term fetal sheep. J Physiol. 1993;461:431–49.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Gluckman PD, Gunn TR, Johnston BM. The effect of cooling on breathing and shivering in unanaesthetized fetal lambs in utero. J Physiol. 1983;343:495–506.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Greer JJ, Martin-Caraballo M. Developmental plasticity of phrenic motoneuron and diaphragm properties with the inception of inspiratory drive transmission in utero. Exp Neurol. 2017;287(Pt 2):137–43.PubMedCrossRefGoogle Scholar
  47. Guerra FA, Savich RD, Clyman RI, et al. Meclofenamate increases ventilation in lambs. J Dev Physiol. 1989;11(1):1–6.PubMedGoogle Scholar
  48. Hampl V, Bibova J, Stranak Z, Wu X, Michelakis ED, Hashimoto K, et al. Hypoxic fetoplacental vasoconstriction in humans is mediated by potassium channel inhibition. Am J Physiol Heart Circ Physiol. 2002;283(6):H2440–9.PubMedCrossRefGoogle Scholar
  49. Hamrick SE, Hansmann G. Patent ductus arteriosus of the preterm infant. Pediatrics. 2010;125(5):1020–30.PubMedCrossRefGoogle Scholar
  50. Hanson MA. Peripheral chemoreceptor function before and after birth. In: Johnston BM, Gluckman P, editors. Respiratory control and lung development in the fetus and newborn. Ithaca: perinatology press; 1986. p. 311–30.Google Scholar
  51. Hanson MA, Moore PJ, Nijhuis JG, et al. Effects of pilocarpine on breathing movements in normal, chemodenervated and brain stem-transected fetal sheep. J Physiol. 1988;400:415–24.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Harding R, Bocking AD, Sigger JN. Influence of upper respiratory tract on liquid flow to and from fetal lungs. J Appl Physiol. 1985;61(1):68–74.CrossRefGoogle Scholar
  53. Hasan SU, Lee DS, Gibson DA, et al. Effect of morphine on breathing and behavior in fetal sheep. J Appl Physiol. 1988;64:2058–65.PubMedCrossRefGoogle Scholar
  54. Haworth SG, Hislop AA. Lung development-the effects of chronic hypoxia. Semin Neonatol. 2003;8(1):1–8.PubMedCrossRefGoogle Scholar
  55. Hohimer AR, Bissonnette JM. Effects of metabolic acidosis on fetal breathing movements in utero. Respir Physiol. 1981;43(2):99–106.CrossRefGoogle Scholar
  56. Honest H, Bachmann LM, Sengupta R, et al. Accuracy of absence of fetal breathing movements in predicting preterm birth: a systematic review. Ultrasound Obstet Gynecol. 2004;24(1):94–100.PubMedCrossRefGoogle Scholar
  57. Inanlou MR, Baguma-Nibasheka M, Kablar B. The role of fetal breathing-like movements in lung organogenesis. Histol Histopathol. 2005;20(4):1261–6.PubMedGoogle Scholar
  58. Ioffe S, Jansen AH, Chernick V. Maturation of spontaneous fetal diaphragmatic activity and fetal response to hypercapnia and hypoxemia. J Appl Physiol. 1987;62:609–22.CrossRefGoogle Scholar
  59. Jansen AH, Ioffe S, Chernick V. Stimulation of fetal breathing activity by beta-adrenergic mechanisms. J Appl Physiol. 1986;60:1938–45.PubMedCrossRefGoogle Scholar
  60. Johnston BM, Gluckman PD. Lateral pontine lesion affects central chemosensitivity in unanaesthetized fetal lambs. J Physiol. 1989;67:1113–8.Google Scholar
  61. Khong TY, Tee JH, Kelly AJ. Absence of innervation of the uteroplacental arteries in normal and abnormal human pregnancies. Gynecol Obstet Investig. 1997;43(2):89–93.CrossRefGoogle Scholar
  62. Kinsella JP, Abman SH. Recent developments in the pathophysiology and treatment of persistent pulmonary hypertension of the newborn. J Pediatr. 1995;126(6):853–64.PubMedCrossRefGoogle Scholar
  63. Kiserud T, Ozaki T, Nishina H, Rodeck C, Hanson MA. Effect of NO, phenylephrine, and hypoxemia on ductus venosus diameter in fetal sheep. Am J Physiol Heart Circ Physiol. 2000;279(3):H1166–71.PubMedCrossRefGoogle Scholar
  64. Kitterman JA, Liggins GC, Clements JA, et al. Stimulation of breathing movements in fetal sheep by inhibitors of prostaglandin synthesis. J Dev Physiol. 1979;1:453–66.PubMedGoogle Scholar
  65. Kitterman JA, Liggins GC, Fewell JE, et al. Inhibition of breathing movements in fetal sheep of sodium meclofenamate. J Appl Physiol Respir Environ Exerc Physiol. 1983;54:687–92.PubMedGoogle Scholar
  66. Koos BJ. Central effects on breathing in fetal sheep of sodium meclofenamate. J Physiol. 1982;330:50–1P.Google Scholar
  67. Koos BJ. Central stimulation of breathing movements in fetal lambs by prostaglandin synthetase inhibitors. J Physiol. 1985;362:455–66.PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kozuma S, Nishina H, Unno N, et al. Goat fetuses disconnected from the placenta, but reconnected to an artificial placenta, display intermittent breathing movements. Biol Neonate. 1999;75(6):388–97.PubMedCrossRefGoogle Scholar
  69. Kuipers IM, Maertzdorf WM, De Jong DS, et al. Effects of mild hypocapnia on fetal breathing and behavior in unanaesthetized normoxic fetal lambs. J Appl Physiol. 1994;76:1476–80.PubMedCrossRefGoogle Scholar
  70. Kuipers IM, Maertzdorf EJ, De Jong DS, et al. Initiation and maintenance of continuous breathing at birth. Pediatr Res. 1997;42(2):163–8.PubMedCrossRefPubMedCentralGoogle Scholar
  71. Kumar P, Hanson MA. Re-setting of the hypoxic sensitivity of aortic chemoreceptors in the newborn lamb. J Dev Physiol. 1989;11:199–206.PubMedPubMedCentralGoogle Scholar
  72. Lagercrantz H, Pequignot JM, Hertzberg T, et al. Birth-related changes of expression and turnover of some neuroactive agents and respiratory control. Biol Neonate. 1994;65(3–4):145–8.PubMedCrossRefPubMedCentralGoogle Scholar
  73. Lai J, Nowlan NC, Vaidyanathan R, Shaw CJ, Lees CC. Fetal movements as a predictor of health. Acta Obstet Gynecol Scand. 2016;95(9):968–75.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Lalor JG, Fawole B, Alfirevic Z, Devane D. Biophysical profile for fetal assessment in high risk pregnancies. Cochrane Database Syst Rev. 2008;1:CD000038.Google Scholar
  75. Lee DS, Choy P, Davi M, et al. Decrease in plasma prostaglandin E 2 is not essential for the establishment of continuous breathing at birth in sheep. J Dev Physiol. 1989;12(3):145–51.PubMedGoogle Scholar
  76. Long WA. Prostaglandins and control of breathing in newborn piglets. J Appl Physiol. 1988;64(1):409–18.PubMedCrossRefGoogle Scholar
  77. Maruotti GM, Saccone G, Ciardulli A, et al. Absent ductus venosus: case series from two tertiary centres. J Matern Fetal Neonatal Med. 2018;31(18):2478–83.PubMedCrossRefGoogle Scholar
  78. Molteni RA, Melmed MH, Sheldon RE, et al. Induction of fetal breathing by metabolic acidemia and its effects on blood flow to the respiratory muscles. Am J Obstet Gynecol. 1980;136:609–20.PubMedCrossRefGoogle Scholar
  79. Murai DT, Wallen LD, Lee CC, et al. Effects of prostaglandins in fetal breathing do not involve peripheral chemoreceptors. J Appl Physiol. 1987;62(1):271–7.PubMedCrossRefGoogle Scholar
  80. Murayama K, Nagasaka H, Tate K, Ohsone Y, Kanazawa M, Kobayashi K, et al. Significant correlations between the flow volume of patent ductus venosus and early neonatal liver function: possible involvement of patent ductus venosus in postnatal liver function. Arch Dis Child Fetal Neonatal Ed. 2006;91(3):F175–9.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Nicol MB, Hirst JJ, Walker D, et al. Effect of alteration of maternal plasma progesterone concentrations on fetal behavioural state during late gestation. J Endocrinol. 1997;152(3):379–86.PubMedCrossRefGoogle Scholar
  82. Noori S, Friedlich PS, Seri I. Pathophysiology of shock in the fetus and neonate. In: Polin RA, Fox WW, Abman SH, editors. Fetal and neonatal physiology. Philadelphia: Saunders; 2004. p. 772–81.CrossRefGoogle Scholar
  83. Parkes MJ, Moore PJ, Hanson MA. The effects of inhibition of 3-B hydroxysteroid dehydrogenase activity in sheep fetuses in utero. Proc Society Study Fetal Physiol Cairn. 1988;58Google Scholar
  84. Patrick J, Challis JRG, Cross J. Effects of maternal indomethacin administration on fetal breathing movements in sheep. J Dev Physiol. 1987;9(3):295–300.PubMedGoogle Scholar
  85. Phillipson EA, Bowes G, Townsend ER, et al. Carotid chemoreceptors in ventilatory response to changes in venous CO2 load. J Appl Physiol Respir Environ Exerc Physiol. 1981;51:1398–403.PubMedGoogle Scholar
  86. Quilligan EJ, Clewlow F, Johnston BM, et al. Effects of 5-hydroxytryptophan on electrocortical activity and breathing movements of fetal sheep. Am J Obstet Gynecol. 1981;141(3):271–5.PubMedCrossRefGoogle Scholar
  87. Reese J. Death, dying, and exhaustion in the ductus arteriosus: prerequisites for permanent closure. Am J Physiol Regul Integr Comp Physiol. 2006;290(2):R357–8.PubMedCrossRefPubMedCentralGoogle Scholar
  88. Reuss ML, Rudolph AM. Distribution and recirculation of umbilical and systemic venous blood flow in fetal lambs during hypoxia. J Dev Physiol. 1980;2(1–2):71–84.PubMedPubMedCentralGoogle Scholar
  89. Russell MJ, Dombkowski RA, Olson KR. Effects of hypoxia on vertebrate blood vessels. J Exp Zool A Ecol Genet Physiol. 2008;309A(2):55–63.CrossRefGoogle Scholar
  90. Sanchez-Esteban J, Tsai SW, Sang J, et al. Effects of mechanical forces on lung-specific gene expression. Am J Med Sci. 1998;316:200–4.PubMedGoogle Scholar
  91. Sawa R, Asakura H, Power G. Changes in plasma adenosine during simulated birth of fetal sheep. J Appl Physiol. 1991;70:1524–8.PubMedCrossRefGoogle Scholar
  92. Sebire NJ, Talbert D. The role of intraplacental vascular smooth muscle in the dynamic placenta: a conceptual framework for understanding uteroplacental disease. Med Hypotheses. 2002;58(4):347–51.PubMedCrossRefGoogle Scholar
  93. Seravalli V, Miller JL, Bloc-Abraham D, et al. Ductus venosus Doppler in the assessment of fetal cardiovascular health: an updated practical approach. Acta Obstet Gynecol Scand. 2016;95(6):635–44.PubMedCrossRefGoogle Scholar
  94. Shaul PW. Regulation of vasodilator synthesis during lung development. Early Hum Dev. 1999;54(3):271–94.PubMedCrossRefGoogle Scholar
  95. Smith GC. The pharmacology of the ductus arteriosus. Pharmacol Rev. 1998;50(1):35–58.PubMedGoogle Scholar
  96. Smith GN, Brien JF, Homan J, et al. Effect of ethanol on ovine fetal and maternal plasma prostaglandin E2 concentrations and fetal breathing movements. J Dev Physiol. 1990a;14(1):23–8.PubMedGoogle Scholar
  97. Smith GN, Brien JF, Homan J, et al. Indomethacin reversal of ethanol-induced suppression of ovine fetal breathing movements and relationship to prostaglandin E2. J Dev Physiol. 1990b;14(1):29–35.PubMedGoogle Scholar
  98. Sommer RJ, Hijazi ZM, Rhodes JF Jr. Pathophysiology of congenital heart disease in the adult: part I: shunt lesions. Circulation. 2008;117(8):1090–9.PubMedCrossRefGoogle Scholar
  99. Stephan-Blanchard E, Chardon K, Leke A, et al. In utero exposure to smoking and peripheral chemoreceptor function in preterm neonates. Pediatrics. 2010;125(3):e592–9.PubMedCrossRefGoogle Scholar
  100. Steriade M, Contreras D, Amzica F. Synchronized sleep oscillations and their paroxysmal developments. Trends Neurosci. 1994;17:199–208.PubMedCrossRefGoogle Scholar
  101. Stoller JZ, DeMauro SB, Dagle JM, Reese J. Current perspectives on pathobiology of the ductus arteriosus. J Clin Exp Cardiolog. 2012;8(1):S8–001.PubMedPubMedCentralGoogle Scholar
  102. Szeto HH. Spectral edge frequency as a simple quantitative measure of maturation of electrocortical activity. Pediatr Res. 1990;27:289–92.PubMedCrossRefGoogle Scholar
  103. Szeto HH, Vo TDH, Dwyer G, et al. The ontogeny of fetal lamb electrocortical activity: a power spectral analysis. Am J Obstet Gynecol. 1985;153:462–6.PubMedCrossRefGoogle Scholar
  104. Szeto HH, Cheng PY, Decena JA, et al. Developmental changes in continuity and stability of breathing in the fetal lamb. Am J Phys. 1992;262:R452–8.Google Scholar
  105. Talbert D, Sebire NJ. The dynamic placenta: I. hypothetical model of a placental mechanism matching local fetal blood flow to local intervillus oxygen delivery. Med Hypotheses. 2004;62(4):511–9.PubMedCrossRefGoogle Scholar
  106. Vries de JIP, Visser GHA, Prechtl HFR. The emergence of fetal behavior 1. Qualitative aspects. Early Hum Dev. 1982;7:301–22.CrossRefGoogle Scholar
  107. Wallen LD, Murai DT, Clyman RI, et al. Regulation of breathing movements in fetal sheep by prostaglandin E2. J Appl Physiol. 1986;60:526–31.PubMedCrossRefGoogle Scholar
  108. Wallen LD, Murai DT, Clyman RI, et al. Effects of meclofenamate on breathing movements in fetal sheep before delivery. J Appl Physiol. 1988;64(2):759–66.PubMedCrossRefGoogle Scholar
  109. Ward JP. Oxygen sensors in context. Biochim Biophys Acta. 2008;1777(1):1–14.PubMedCrossRefGoogle Scholar
  110. Watson CS, White SE, Homan JH, et al. Increase cerebral extracellular adenosine and decreased PGE2 during ethanol-induced inhibition of FBM. J Appl Physiol. 1999;86:1410–20.PubMedCrossRefPubMedCentralGoogle Scholar
  111. Weir E, Lopez-Barneo J, Buckler K, Archer SL. Acute oxygen-sensing mechanisms. N Engl J Med. 2005;353(19):2042–55.PubMedPubMedCentralCrossRefGoogle Scholar
  112. Ziegler JW, Ivy DD, Kinsella JP, Abman SH. The role of nitric oxide, endothelin, and prostaglandins in the transition of the pulmonary circulation. Clin Perinatol. 1995;22(2):387–403.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Department of NeonatologyNational Maternity HospitalDublinIreland
  2. 2.Department of Pediatrics, School for Oncology and Developmental Biology (GROW)Maastricht University Medical Center (MUMC+)MaastrichtThe Netherlands

Personalised recommendations