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Intiation of lung ventilation at birth

Published online by Cambridge University Press:  10 October 2008

S Lee Adamson
S Lee Adamson*
Affiliation:
Samuel Lunenfeld Research Institute, Toronto, Canada
*
Dr Lee Adamson, Samuel Lunenfeld Research Institute, Room 138-P, Mount Sinai Hospital, 600 University Avenue, Toronto, Ontario M5G1X5, Canada.
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Extract

The newborn baby draws its first postnatal breath either during or within seconds of delivery. Within minutes, a regular breathing rhythm is established and this remains virtually continuous for the remainder of postnatal life. The mechanisms responsible for these sudden, dramatic and vital changes in the respiratory system at birth are only partially understood. Since fetuses make intermittent breathing movements long before birth, understanding the control of the fetal respiratory system may be essential to understanding the rapid onset of respiratory efforts at delivery. In this review the stimuli present at birth will be considered and, based on our current understanding of the fetal and neonatal respiratory control systems, those factors which are likely to play an important role in the initiation of lung ventilation at this time will be examined. Normal respiratory events in the early postnatal period will be concentrated on, but it is important to recognize that in some cases problems occur: a neonate may fail to initiate breathing efforts rapidly, or an apparently healthy premature neonate may suddenly stop breathing a few days after birth. In both cases, clinical intervention may be required to maintain adequate gas exchange and to prevent brain damage or death. Clearly, greater knowledge of respiratory control during this critical time of life would assist in the development of more appropriate and successful treatments for these life-threatening disorders.

Type
Articles
Information
Fetal and Maternal Medicine Review , Volume 3 , Issue 2 , July 1991 , pp. 133 - 145
Copyright
Copyright © Cambridge University Press 1991

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References

1Richardson, BS, Carmichael, L, Homan, J, Tanswell, K, Webster, AC. Regional blood flow change in the lamb during the perinatal period. Am J Obstet Gynecol 1989; 160: 919–25.CrossRefGoogle ScholarPubMed
2Engstrom, I, Karlberg, P, Rooth, G, Tunell, R. The onset of respiration. A study of respiration and changes in blood gases and acid-base balance. New York: Association for the Aid of Crippled Children, 1966.Google Scholar
3Karlberg, P. The first breaths of life. In: Gluck, L ed. Modern perinatal medicine. Chicago: Medical publishers, 1974: 391–408.Google Scholar
4Berger, PJ, Horne, RSC, Soust, M, Walker, AM, Maloney, JE. Breathing at birth and the associated blood gas and pH changes in the lamb. Respir physiol 1990; 82: 251–66.CrossRefGoogle ScholarPubMed
5Harned, HS, Herrington, RT, Griffin, CA, Berryhill, WS, Mackinney, LG. Respiratory effects of division of the carotid sinus nerve in the lamb soon after birth. Pediatr Res 1968; 2: 264–70.Google Scholar
6Pagtakhan, RD, Faridy, EE, Chernick, V. Interaction between PO2 and PCO2 in the initiation of respiration in fetal sheep. J Appl Physiol 1971; 30: 382–87.CrossRefGoogle ScholarPubMed
7Woodrum, DE, Parer, JT, Wennberg, RP, Hodson, WA. Chemoreceptor response in initiation of breathing in the fetal lamb. J Appl Physiol 1972; 33: 120–25.CrossRefGoogle ScholarPubMed
8Willis, DM, Anderson, DF, Thornburg, KL, Faber, JJ. Alteration of arterial gas composition by positive pressure ventilation in the unanesthetized fetal lamb in utero. Biol Neonate 1985; 47: 295–304.CrossRefGoogle ScholarPubMed
9Power, GG, Kawamura, T, Dale, PS, Schroder, H, Gilbert, RD. Temperature responses during ventilation of fetal sheep in utero. J Dev Physiol 1986; 8: 477–84.Google ScholarPubMed
10Adamson, SL, Richardson, BS, Homan, J. Initiation of pulmonary gas exchange by fetal sheep in utero. J Appl Physiol 1987; 62: 989–98.Google Scholar
11Blanco, CE, Martin, CB Jr, Hanson, MA, McCooke, HB. Breathing activity in fetal sheep during mechanical ventilation of the lungs in utero. Eur J Obstet Gynecol Reprod Biol 1987; 26: 175–82.CrossRefGoogle ScholarPubMed
12Iwamoto, HS, Teitel, D, Rudolph, AM. Effects of birth-related events on blood flow distribution. Pediatr Res 1987; 22: 634–40.CrossRefGoogle ScholarPubMed
13Baier, RJ, 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.CrossRefGoogle ScholarPubMed
14Adamson, SL, Kuipers, IM, Olson, DM. Umbilical cord occlusion stimulates breathing independent of blood gases and pH. J Appl Physiol 1991 (in press).Google Scholar
15Morton, MJ, Pinson, CW, Thornburg, KL. In utero ventilation with oxygen augments left ventricular stroke volume in lambs. J Physiol 1987; 383: 413–24.CrossRefGoogle ScholarPubMed
16Teitel, DF, Iwamoto, HS, Rudolph, AM. Changes in the pulmonary circulation during birth-related events. Pediatr Res 1990; 27: 372–78.Google Scholar
17Power, GG, Gunn, TR, Johnston, BM, Nichols, G, Gluckman, PD. Umbilical cord occlusion but not increased plasma T3 or norepinephrine stimulate brown adipose tissue thermogenesis in the fetal lamb. J Dev Physiol 1989; 11: 171–77.Google Scholar
18Gluckman, PD, Gunn, TR, Johnston, BM. The effect of cooling on breathing and shivering in unanesthetized fetal lambs in utero. J Physiol (Lond) 1983; 343: 495–506.CrossRefGoogle Scholar
19Berger, AJ, Mitchell, RA, Severinghaus, JW. Regulation of respiration (second of 3 parts). N Engl J Med 1977; 297: 138–43.Google Scholar
20Lambertsen, CJ. Neural control of respiration. In: Mountcastle, VB ed. Medical Physiology, 2. St Louis: CV Mosby, 1980; 1749–73.Google Scholar
21Bystrzycka, E, Nail, BS, Purves, MJ. Central and peripheral neural respiratory activity in the mature sheep foetus and newborn lamb. Respir Physiol 1975; 25: 199–215.CrossRefGoogle ScholarPubMed
22Ioffe, S, Jansen, AH, Chernick, V. Chronic extracellular recording of fetal medullary neuronal activity. J Appl Physiol 1983; 55: 1361–64.CrossRefGoogle ScholarPubMed
23Ritchie, JWK, Lakhani, K. Fetal breathing movements in response to maternal inhalation of 5% carbon dioxide. Am J Obstet Gynecol 1980; 136: 386–88.CrossRefGoogle ScholarPubMed
24Boddy, K, Dawes, GS, Fisher, RL, Pinter, S, Robinson, JS. Fetal respiratory movements, electrocortical and cardiovascular responses to hypoxaemia and hypercapnia in sheep. J Physiol (Lond) 1974; 243: 599–618.CrossRefGoogle ScholarPubMed
25Patrick, J, Fetherston, W, Vick, H, Voegelin, R. Human fetal breathing movements and gross fetal body movements at weeks 34 to 35 of gestation. Am J Obstet Gynecol 1978; 130: 693–99.CrossRefGoogle ScholarPubMed
26Dawes, GS, Fox, HE, Leduc, BM, Liggins, GC, Richards, RT. Respiratory movements and rapid eye movement sleep in the fetal lamb. J Physiol (Lond) 1972; 220: 119–43.Google Scholar
27Bland, RD. Lung liquid clearance before and after birth. Semin Perinatol 1988; 12: 124–33.Google ScholarPubMed
28Liggins, GC, Campos, GA, Vilos, GA, Kitterman, JA, Lee, CC, Clements, JA. The effect of spinal cord transection on lung development in fetal sheep. J Dev Physiol 1981; 3: 267–74.Google Scholar
29Van Vliet, MAT, Martin, CB Jr, Nijhuis, JG, Prechtl, HFR. The relationship between fetal activity and behavioral state and fetal breathing movements in normal and growth-retarded fetuses. Am J Obstet Gynecol 1985; 153: 582–88.CrossRefGoogle ScholarPubMed
30Blanco, CE, Dawes, GS, Hanson, MA, McCooke, HB. The response to hypoxia of arterial chemoreceptors in fetal sheep and newborn lambs. J Physiol (Lond) 1984; 351: 25–37.Google Scholar
31Koos, BJ, Sameshima, H. Effects of hypoxemia and hypercapnia on breathing movements and sleep state in sino-aortic denervated fetal sheep. J Dev Physiol 1988; 10: 131–44.Google Scholar
32Koos, BJ, Sameshima, H, Power, GG. Fetal breathing, sleep state, and cardiovascular responses to graded hypoxia in sheep. J Appl Physiol 1987; 62: 1033–39.CrossRefGoogle ScholarPubMed
33Dawes, GS, Gardner, WN, Johnston, BM, Walker, DW. Breathing in fetal lambs: the effect of brain stem section. J Physiol (Lond) 1983; 335: 535–53.CrossRefGoogle ScholarPubMed
34Gluckman, PD, Johnston, BM. Lesions in the upper lateral pons abolish the hypoxic depression of breathing in unanesthetized fetal lambs in utero. J Physiol (Lond) 1987; 382: 373–83.CrossRefGoogle Scholar
35Haddad, GG, Mellins, RB. Hypoxia and respiratory control in early life. Ann Rev Physiol 1984; 46: 629–43.Google Scholar
36Carmichael, L, Campbell, K, Patrick, J. Fetal breathing, gross fetal body movements, and maternal and fetal heart rates before spontaneous labor at term. Am J Obstet Gynecol 1984; 148: 675–79.CrossRefGoogle ScholarPubMed
37Boddy, K, Dawes, GS. Fetal breathing. Br Med Bull 1975; 31: 3–7.Google Scholar
38Berger, PJ, Walker, AM, Horne, R et al. Phasic respiratory activity in the fetal lamb during late gestation and labour. Respir Physiol 1986; 65: 55–68.Google Scholar
39Karlberg, P, Cherry, RB, Escardo, FE, Koch, G. Respiratory studies in newborn infants. II: Pulmonary ventilation and mechanics of breathing in the first minutes of life, including the onset of respiration. Acta Paediatr Scand 1962; 51: 121–36.Google Scholar
40Karlberg, P. The adaptive changes in the immediate postnatal period, with particular reference to respiration. J Pediatr 1969; 56: 585–604.Google Scholar
41Scarpelli, EM. Intrapulmonary foam at birth: an adaptational phenomenon. Pediatr Res 1978; 12: 1070–73.CrossRefGoogle ScholarPubMed
42Mortola, JP, Fisher, JT, Smith, JB, Fox, GS, Weeks, S, Willis, D. Onset of respiration in infants delivered by caesarean section. J Appl Physiol 1982; 52: 716–24.Google Scholar
43Vyas, H, Milner, AD, Hopkin, IE. Intrathoracic pressure and volume changes during the spontaneous onset of respiration in babies born by caesarean section and by vaginal delivery. J Pediatr. 1981; 99: 787–91.Google Scholar
44Ullrich, JR, Ackerman, BD. Changes in umbilical artery blood gas values with the onset of respiration. Biol Neonate 1972; 20: 466–74.Google Scholar
45McCallum, WD, McAreavey, DRM. Human umbilical vessel diameters and blood gas tensions in the first two minutes after delivery. Gynecol Obstet invest 1976; 7: 201–12.CrossRefGoogle ScholarPubMed
46Huch, A, Huch, R, Schneider, H, Rooth, G. Continuous transcutaneous monitoring of fetal oxygen tension during labour. Br J Obstet Gynaecol 1977; 84(suppl): 1–39.CrossRefGoogle ScholarPubMed
47Chou, PJ, Ullrich, JR, Ackerman, BD. Time of onset of effective ventilation at birth. Biol Neonate 1974; 24: 74–81.Google Scholar
48Tunell, R. The influence of different environmental temperatures on pulmonary gas exchange and blood gas changes after birth. Acta Paediatr Scand 1975; 64: 57–68.Google Scholar
49Harris, AP, Sendak, MJ, Donham, RT. Changes in arterial oxygen saturation immediately after birth in the human neonate. J Pediatr 1986; 109: 117–19.Google Scholar
50Itskovitz, J, LaGamma, EF, Rudolph, AM. Effects of cord compression on fetal blood flow distribution and O2 delivery. Am J Physiol 1987; 252: H100–109.Google Scholar
51McCallum, WD. Qualitative estimation of blood velocity changes in human umbilical arteries after delivery. Early Hum Dev 1977; 1: 99–106.Google Scholar
52McCallum, WD. Thermodilution measurements of human umbilical blood flow at delivery. Am J Obstet Gynecol 1977; 127: 491–96.CrossRefGoogle ScholarPubMed
53Koch, G, Wendel, H. Adjustment of arterial blood gases and acid base balance in the normal newborn infant during the first week of life. Biol Neonate 1968; 12: 136–61.Google Scholar
54Lee, DS, Choy, P, Davi, M et al. Decrease in plasma prostaglandin E2 is not essential for the establishment of continuous breathing at birth in sheep. J Dev Physiol 1989; 12: 145–51.Google Scholar
55Rigatto, H, Hasan, SU, Jansen, A, Gibson, D, Nowaczyk, B, Cates, D. The effect of total peripheral chemodenervation on fetal breathing and on the establishment of breathing at birth in sheep. In: Jones, CT ed. Fetal and neonatal development. New York: Perinatology Press, 1988: 613–21.Google Scholar
56Marsland, DW, Callahan, BJ, Shannon, DC. The afferent vagus and regulation of breathing in response to inhaled CO2 in awake newborn lambs. Biol Neonate 1975; 27: 102–107.CrossRefGoogle ScholarPubMed
57Krauss, AN, Klain, DB, Waldman, S, Auld, PAM. Ventilatory response to carbon dioxide in newborn infants. Pediatr Res 1975; 9: 46–50.Google Scholar
58Chapman, RLK, Dawes, GS, Rurak, DW, Wilds, PL. Breathing movements in fetal lambs and the effect of hypercapnia. J Physiol (Lond) 1980; 302: 19–29.Google Scholar
59Rigatto, H, Lee, D, Davi, M, Moore, M, Rigatto, E, Cates, D. Effect of increased arterial CO2 on fetal breathing and behavior in sheep. J Appl Physiol 1988; 64: 982–87.Google Scholar
60Jansen, AH, Ioffe, S, Russell, BJ, Chernick, V. Influence of sleep state on the response to hypercapnia in fetal lambs. Respir Physiol 1982; 48: 125–42.CrossRefGoogle ScholarPubMed
61Comline, RS, Silver, M. The composition of fetal and maternal blood during parturition in the ewe. J Physiol (Lond) 1972; 222: 233–56.Google Scholar
62Leffler, CW, Hessler, JR, Green, RS. The onset of breathing at birth stimulates pulmonary vascular prostacyclin synthesis. Pediatr Res 1984; 18: 938–42.CrossRefGoogle ScholarPubMed
63Leffler, CW, Crofton, J, Brooks, DP, Share, L, Hessler, JR. Changes in plasma arginine vasopressin during transition from fetus to newborn following minimal trauma delivery of lambs and goats. Biol Neonate 1985; 48: 43–48.Google Scholar
64Davidson, D. Circulating vasoactive substances and hemodynamic adjustments at birth in lambs. J Appl Physiol 1987; 63: 676–84.Google Scholar
65Davidson, D. Pulmonary hemodynamics at birth: effect of acute cyclooxygenase inhibition in the lamb. J Appl Physiol 1988; 64: 1676–82.CrossRefGoogle Scholar
66Molteni, RA, Melmed, MH, Sheldon, RE, Jones, MD, Meschia, G. Induction of fetal breathing by metabolic acidemia and its effect on blood flow to the respiratory muscles. Am J Obstet Gynecol 1980; 136: 609–20.CrossRefGoogle Scholar
67Hohimer, AR, Bissonnette, JM. Effect of metabolic acidosis on fetal breathing movements in utero. Respir Physiol 1981; 43: 99–106.CrossRefGoogle Scholar
68Bureau, MA, Begin, R. Depression of respiration induced by metabolic acidosis in newborn lambs. Biol Neonate 1982; 42: 279–83.Google Scholar
69Maloney, JE, Alcorn, D, Wilkinson, M. Development of the future respiratory system before birth. Semin Perinatol 1980; 4: 251–60.Google ScholarPubMed
70Takahashi, E, Menon, AS, Kato, H, Slutsky, AS, Phillipson, EA. Control of expiratory duration by arterial CO2 oscillations in vagotomized dogs. Respir Physiol 1990; 79: 45–56.CrossRefGoogle ScholarPubMed
71Takahashi, E, Ashe, KA. Role of carbon dioxide oscillation in the control of respiration in the anesthetized dog. Jpn J Physiol 1989; 39: 267–81.CrossRefGoogle ScholarPubMed
72Ritchie, JWK, Lakhani, K. Fetal breathing movements and maternal hyperoxia. Br J Obstet Gynaecol 1980; 87: 1084–86.CrossRefGoogle ScholarPubMed
73Devoe, LD, Abduljabbar, H, Carmichael, L, Probert, C, Patrick, J. The effect of maternal hyperoxia on fetal breathing movements in third-trimester pregnancies. Am J Obstet Gynecol 1984; 148: 790–94.Google Scholar
74Hohimer, AR, Bissonnette, JM, Richardson, BS, Machida, CM. Central chemical regulation of breathing movements in fetal lambs. Respir Physiol 1983; 52: 99–111.Google Scholar
75Berger, AJ, Mitchell, RA, Severinghaus, JW. Regulation of respiration (first of 3 parts). N Engl J Med 1977; 297: 92–97.Google Scholar
76Kumar, P, Hanson, MA. Resetting of the hypoxic sensitivity of chemoreceptors in the newborn lamb. J Dev Physiol 1989; 11: 199–206.Google Scholar
77Herrington, RT, Harned, HS, Ferreiro, JI, Griffin, CA. The role of the central nervous system in perinatal respiration: studies of chemoregulatory mechanisms in the term lamb. Pediatrics 1971; 47: 857–64.Google Scholar
78Godfrey, S. Blood gases during asphyxia and resuscitation of fetal and newborn rabbits. Respir Physiol 1968; 4: 309–21.Google Scholar
79Guntheroth, WG, Kawabori, I. Hypoxic apnea and gasping. J Clin Invest 1975; 56: 1371–77.CrossRefGoogle ScholarPubMed
80St John, WM, Bledsoe, TA, Sokol, HW. Identification of medullary loci critical for neurogenesis of gasping. J Appl Physiol 1984; 56: 1008–19.CrossRefGoogle ScholarPubMed
81St John, WM, Knuth, KV. A characterization of the respiratory pattern of gasping. J Appl Physiol 1981; 50: 984–93.Google Scholar
82Egan, EA, Olver, RE, Strang, LB. Changes in non-electrolyte permeability of alveoli and the absorption of lung liquid at the start of breathing in the lamb. J Physiol(Lond) 1975; 244: 161–79.Google Scholar
83Harned, HS Jr, Ferreiro, J. Initiation of breathing by cold stimulation: effect of change in ambient temperature on respiratory activity of the full-term fetal lamb. J Pediatr 1973; 83: 663–69.CrossRefGoogle ScholarPubMed
84Kattwinkel, J, Nearman, HS, Fanaroff, AA, Katona, PG, Klaus, MH. Apnea of prematurity: comparative therapeutic effects of cutaneous stimulation and nasal continuous positive airway pressure. J Pediatr 1975; 86: 588–92.CrossRefGoogle ScholarPubMed
85Marchal, F, Bairam, A, Vert, P. Neontal apnea and apneic syndromes. Clin Perinatol 1987; 14:509–29.Google Scholar
86Condorelli, S, Scarpelli, EM. Fetal breathing: induction in utero and the effects of vagotomy and barbiturates. J Pediatr 1976; 88: 94–101.Google Scholar
87Ioffe, S, Jansen, AH, Russell, BJ, Chernick, V. Respiratory response to somatic stimulation in fetal lambs during sleep and wakefulness. Pfluegers Archiv 1980; 388: 143–48.CrossRefGoogle ScholarPubMed
88Desmond, MM, Franklin, RR, Vallbona, C et al. The clinical behavior of the newly born. I: The term baby. J Pediatr 1963; 62: 307–15.CrossRefGoogle Scholar
89Phillipson, EA, Bowes, G. Control of breathing during sleep. In: Fishman, AP ed. Handbook of physiology. The respiratory system, volume II, part 2. Bethesda, Maryland: American Physiological Society, 1986: 649–89.Google Scholar
90Ruckebusch, Y. Development of sleep and wakefulness in the foetal lamb. Electroencephalogr Clin Neurophysiol. 1972; 32: 119–28.Google Scholar
91Rigatto, H, Moore, M, Cates, D. Fetal breathing and behavior measured through a double-wall Plexiglas window in sheep. J Appl Physiol 1986; 61: 160–64.CrossRefGoogle ScholarPubMed
92Read, DJC, Henderson-Smart, DJ. Regulation of breathing in the newborn during different behavioral states. Ann Rev Physicol 1984; 46: 675–85.Google Scholar
93Walker, DW. Effects of increased core temperature on breathing movements and electrocortical activity in fetal sheep. J Develop Physicol 1988; 10: 513–23.Google Scholar
94Eliot, RJ, Klein, AH, Glatz, TH, Nathanielsz, PW, Fisher, DA. Plasma norepinephrine, epinephrine, and dopamine concentrations in maternal and fetal sheep during spontaneous parturition and in premature sheep during cortisol-induced parturition. Endocrinology 1981; 108: 1678–82.CrossRefGoogle ScholarPubMed
95Weiner, N. Norepinephrine, epinephrine, and the sympathomimetic amines. In: Gilman, AG, Goodman, LS, Rall, TW, Murad, F eds. The pharmacological basis of therapeutics. New York: Macmillan Publishing, 1985: 145–80.Google Scholar
96Fewell, JE, Baker, SB. Arousal from sleep during rapidly developing hypoxemia in lambs. Pediatr Res 1987; 22: 471–77.Google Scholar
97Fewell, JE, Kondo, CS, Dascalu, V, Filyk, SC. Influence of carotid-denervation on the arousal and cardiopulmonary responses to alveolar hypercapnia in lambs. J Dev Physiol 1989; 12: 193–99.Google Scholar
98Natale, R, Clewlow, F, Dawes, GS. Measurement of fetal forelimb movements in the lamb in utero. Am J Obstet Gynecol 1981; 140: 545–51.Google Scholar
99Sippell, WG, Becker, H, Versmold, HT, Bidlingmaier, F, Knorr, D. Longitudinal studies of plasma aldosterone, corticosterone, deoxycorticosterone, progesterone, 17-hydroxyprogesterone, cortisol, and cortisone determined simultaneously in mother and child at birth and during the early neonatal period. I: Spontaneous delivery. J Clin Endocrinol Metab 1978; 46: 971–85.Google Scholar
100Challis, JRG, Dilley, SR, Robinson, JS, Thorburn, GD. Prostaglandins in the circulation of the fetal lamb. Prostaglandins 1976; 11: 1041–52.Google Scholar
101Olson, DM, Lye, SJ, Challis, JRG. Prostaglandin concentrations in ovine maternal and fetal tissues in late gestation. Pediatr Res 1986; 20: 83–86.Google Scholar
102Tulchinsky, D, Okada, DM. Hormones in human pregnancy. Am J Obstet Gynecol 1975; 121: 293–99.CrossRefGoogle ScholarPubMed
103Mitchell, MD, Brunt, J, Biddy, J, Flint, APF, Anderson, ABM, Turnbull, AC. Prostaglandins in the human umbilical circulation at birth. Br J Obstet Gynaecol 1978; 85: 114–18.Google Scholar
104Clyman, RI, Mauray, F, Heymann, MA, Roman, C. Effect of gestational age on pulmonary metabolism of prostaglandin E1 and E2. Prostaglandins 1981; 21: 505–13.Google Scholar
105Lagercrantz, H, Slotkin, TA. The “stress” of being born. Sci Am 1986; 254: 100–107.Google Scholar
106Kitterman, 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.Google ScholarPubMed
107Kitterman, JA, Liggins, GC, Fewell, JE, Tooley, WH. Inhibition of breathing movements in fetal sheep by prostaglandins. J Appl Physiol 1983; 54: 687–92.CrossRefGoogle ScholarPubMed
108Guerra, FA, Savich, RD, Wallen, LD et al. Prostaglandin E2 causes hypoventilation and apnea in newborn lambs. J Appl Physiol 1988; 64: 2160–66.Google Scholar
109Mitchell, MD, Lucas, A, Etches, PC, Brunt, JD, Turnbull, AC. Plasma prostaglandin levels during erly neonatal life following term and preterm delivery. Prostaglandins 1978; 16: 319–26.Google Scholar
110Wallen, LD, Murai, DT, Clyman, RI, Lee, CH, Mauray, FE, Kitterman, JA. Effects of meclofenamate on breathing movements in fetal sheep before delivery. J Appl Physiol. 1988; 64: 759–66.CrossRefGoogle ScholarPubMed
111Neutze, JB, Starling, MB, Eliot, RB, Baratt-Boyes, BG. Palliation of cyanotic congenital heart disease in infants with E-type prostaglandins. Circulation 1977; 55: 238–41.Google Scholar
112Patrick, J, Challis, JRG, Cross, J. Effects of maternal indomethacin administration on fetal breathing movements in sheep. J Dev Physiol 1987; 9: 295–300.Google ScholarPubMed
113Wallen, LD, Murai, DT, Clyman, RI, Lee, CH, Mauray, FE, Kitterman, JA. Regulation of breathing movements in fetal sheep by prostaglandin E2. J Appl Physiol 1986; 60: 526–31.CrossRefGoogle ScholarPubMed
114Patrick, J, Challis, JRG, Cross, J, Olson, DM, Lye, SJ, Turliuk, R. The relationship between fetal breathing movements and prostaglandin E2 during ACTH-induced labour in sheep. J Dev Physiol 1987; 9: 287–94.Google ScholarPubMed
115Rudolph, AM, Heymann, MA. Circulatory changes during growth in the fetal lamb. Circ Res 1970; 26: 289–99.Google Scholar
116Green, JF, Sheldon, MI. Ventilatory changes associated with changes in pulmonary blood flow in dogs. J Appl Physiol 1983; 54: 997–1002.Google Scholar
117Johnston, BM, Gunn, TR, Gluckman, PD. Surface cooling rapidly induces coordinated activity in the upper and lower airway muscles in the fetal lamb in utero. Pediatr Res 1988; 23: 257–61.Google Scholar