Changes in cerebral blood flow, cerebral metabolites, and breathing movements in the sheep fetus following asphyxia produced by occlusion of the umbilical cord

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 1, 2009, Pages

  Yan, Edwin B ^a,c   Baburamani, Ana A ^b   Walker, Adrian M ^b   Walker, David W ^b  

^a ALFRED HOSPITAL   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Asphyxia; Cerebral blood flow; Cerebral metabolism; Fetal breathing movements; Microdialysis

Indexed keywords

GLYCEROL; PYRUVIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN CORTEX; BRAIN METABOLISM; BREATHING MECHANICS; CAPILLARY FLOW; CONTROLLED STUDY; FETUS; FETUS BREATHING; FETUS HYPOXIA; GLUCOSE UTILIZATION; LACTATE BLOOD LEVEL; NONHUMAN; PRIORITY JOURNAL; SHEEP; SUPERIOR SAGITTAL SINUS; UMBILICAL CORD;

ANIMALS; ASPHYXIA; BIOLOGICAL MARKERS; BLOOD FLOW VELOCITY; BLOOD PRESSURE; BRAIN; CARBON DIOXIDE; CEREBROVASCULAR CIRCULATION; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; ENERGY METABOLISM; FEMALE; FETAL BLOOD; FETAL HYPOXIA; GESTATIONAL AGE; GLUCOSE; GLYCEROL; HEART RATE; HYDROGEN-ION CONCENTRATION; LACTIC ACID; MICRODIALYSIS; OXYGEN; PREGNANCY; PYRUVIC ACID; RESPIRATORY MECHANICS; SHEEP; TIME FACTORS; UMBILICAL CORD;

EID: 67650065275     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00047.2009     Document Type: Article

References (45)

1. Adamson SL, Kuipers IM, Olson DM. Umbilical cord occlusion stimulates breathing independent of blood gases and pH. J Appl Physiol 70: 1796 - 1809, 1991.
2. 2 and umbilical cord occlusion on fetal breathing and behavior Journal of Applied Physiology 1990 68 4 1597-1604 2. Baier 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 68: 1597-1604, 1990. (Pubitemid 20151887)
3. Barcroft J. Researches on Pre-Natal Life. Springfield, IL: Charles C Thomas, 1947.
4. Bennet L. Peebles D.M. Edwards A.D. Rios A. Hanson M.A. The cerebral hemodynamic response to asphyxia and hypoxia in the near- term fetal sheep as measured by near infrared spectroscopy Pediatric Research 1998 44 6 951-957 4. Bennet L, Peebles DM, Edwards AD, Rios A, Hanson MA. The cerebral hemodynamic response to asphyxia and hypoxia in the near-term fetal sheep as measured by near infrared spectroscopy. Pediatr Res 44: 951-957, 1998. (Pubitemid 28543986)
5. Bennet L. Rossenrode S. Gunning M.I. Gluckman P.D. Gunn A.J. The cardiovascular and cerebrovascular responses of the immature fetal sheep to acute umbilical cord occlusion Journal of Physiology 1999 517 1 247-257 DOI 10.1111/j.1469-7793.1999.0247z.x 5. Bennet L, Rossenrode S, Gunning MI, Gluckman PD, Gunn AJ. The cardiovascular and cerebrovascular responses of the immature fetal sheep to acute umbilical cord occlusion. J Physiol 517: 247-257, 1999. (Pubitemid 29243485)
6. Bergamini C.M. Gambetti S. Dondi A. Cervellati C. Oxygen, reactive oxygen species and tissue damage Current Pharmaceutical Design 2004 10 14 1611-1626 DOI 10.2174/1381612043384664 6. Bergamini CM, Gambetti S, Dondi A, Cervellati C. Oxygen, reactive oxygen species and tissue damage. Curr Pharm Des 10: 1611-1626, 2004. (Pubitemid 38559774)
7. Boddy K, Dawes GS, Fisher R, Pinter S, Robinson JS. Foetal respiratory movements, electrocortical and cardiovascular responses to hypoxaemia and hypercapnia in sheep. J Physiol 243: 599-618, 1974.
8. Breen S. Rees S. Walker D. Identification of brainstem neurons responding to hypoxia in fetal and newborn sheep Brain Research 1997 748 1 2 107-121 DOI 10.1016/S0006-8993(96)01273-5, PII S0006899396012735 8. Breen S, Rees S, Walker D. Identification of brainstem neurons responding to hypoxia in fetal and newborn sheep. Brain Res 748: 107-121, 1997. (Pubitemid 27094889)
9. Castillo-Melendez M. Chow J.A. Walker D.W. Lipid Peroxidation, Caspase-3 Immunoreactivity, and Pyknosis in Late-Gestation Fetal Sheep Brain after Umbilical Cord Occlusion Pediatric Research 2004 55 5 864-871 DOI 10.1203/01.PDR.0000115679.86566.C4 9. Castillo-Melendez M, Chow JA, Walker DW. Lipid peroxidation, caspase-3 immunoreactivity, and pyknosis in late-gestation fetal sheep brain after umbilical cord occlusion. Pediatr Res 55: 864-871, 2004. (Pubitemid 38520456)
10. Clewlow F, Dawes GS, Johnston BM, Walker DW. Changes in breathing, electrocortical and muscle activity in unanaesthetized fetal lambs with age. J Physiol 341: 463-476, 1983.
11. Dawes G.S. Gardner W.N. Johnston B.M. Walker D.W. Breathing in fetal lambs: The effect of brain stem section Journal of Physiology 1983 Vol. 335 535-553 11. Dawes GS, Gardner WN, Johnston BM, Walker DW. Breathing in fetal lambs: the effect of brain stem section. J Physiol 335: 535-553, 1983. (Pubitemid 13148386)
12. De Haan H.H. Gunn A.J. Williams C.E. Gluckman P.D. Brief repeated umbilical cord occlusions cause sustained cytotoxic cerebral edema and focal infarcts in near-term fetal lambs Pediatric Research 1997 41 1 96-104 12. de Haan HH, Gunn AJ, Williams CE, Gluckman PD. Brief repeated umbilical cord occlusions cause sustained cytotoxic cerebral edema and focal infarcts in near-term fetal lambs. Pediatr Res 41: 96-104, 1997. (Pubitemid 27008642)
13. Ebensperger G. Ebensperger R. Herrera E.A. Riquelme R.A. Sanhueza E.M. Lesage F. Marengo J.J. Tejo R.I. Llanos A.J. Reyes R.V. Fetal brain hypometabolism during prolonged hypoxaemia in the Ilama Journal of Physiology 2005 567 3 963-975 DOI 10.1113/jphysiol.2005.094524 13. Ebensperger G, Ebensperger R, Herrera EA, Riquelme RA, Sanhueza EM, Lesage F, Marengo JJ, Tejo RI, Llanos AJ, Reyes RV. Fetal brain hypometabolism during prolonged hypoxaemia in the llama. J Physiol 567: 963-975, 2005. (Pubitemid 41387837)
14. George S, Scotter J, Dean JM, Bennet L, Waldvogel HJ, Guan J, Faull RL, Gunn AJ. Induced cerebral hypothermia reduces post-hypoxic loss of phenotypic striatal neurons in preterm fetal sheep. Exp Neurol 203: 137-147, 2006.
15. Gluckman P.D. Johnston B.M. Lesions in the upper lateral pons abolish the hypoxic depression of breathing in unanaesthetized fetal lambs in utero Journal of Physiology 1987 Vol. 382 373-383 15. Gluckman PD, Johnston BM. Lesions in the upper lateral pons abolish the hypoxic depression of breathing in unanaesthetized fetal lambs in utero. J Physiol 382: 373-383, 1987. (Pubitemid 17226152)
16. Gunn AJ, Parer JT, Mallard EC, Williams CE, Gluckman PD. Cerebral histologic and electrocorticographic changes after asphyxia in fetal sheep. Pediatr Res 31: 486-491, 1992.
17. Hillered L. Valtysson J. Enblad P. Persson L. Interstitial glycerol as a marker for membrane phospholipid degradation in the acutely injured human brain Journal of Neurology Neurosurgery and Psychiatry 1998 64 4 486-491 17. Hillered L, Valtysson J, Enblad P, Persson L. Interstitial glycerol as a marker for membrane phospholipid degradation in the acutely injured human brain. J Neurol Neurosurg Psych 64: 486-491, 1998. (Pubitemid 28195950)
18. Hunter C.J. Blood A.B. Power G.G. Cerebral metabolism during cord occlusion and hypoxia in the fetal sheep: A novel method of continuous measurement based on heat production Journal of Physiology 2003 552 1 241-251 DOI 10.1113/jphysiol.2003.048082 18. Hunter CJ, Blood AB, Power GG. Cerebral metabolism during cord occlusion and hypoxia in the fetal sheep: a novel method of continuous measurement based on heat production. J Physiol 552: 241-251, 2003. (Pubitemid 37265482)
19. Hunter C.J. Blood A.B. White C.R. Pearce W.J. Power G.G. Role of nitric oxide in hypoxic cerebral vasodilatation in the ovine fetus Journal of Physiology 2003 549 2 625-633 19. Hunter CJ, Blood AB, White CR, Pearce WJ, Power GG. Role of nitric oxide in hypoxic cerebral vasodilatation in the ovine fetus. J Physiol 549: 625-633, 2003. (Pubitemid 36701772)
20. Jensen EC, Bennet L, Hunter CJ, Power GC, Gunn AJ. Post-hypoxic hypoperfusion is associated with suppression of cerebral metabolism and increased tissue oxygenation in near-term fetal sheep. J Physiol 572: 131-139, 2006.
21. Jones C.T. Ritchie J.W.K. The metabolic and endocrine effects of circulating catecholamines in fetal sheep Journal of Physiology 1978 VOL. 285 395-408 21. Jones CT, Ritchie JW. The metabolic and endocrine effects of circulating catecholamines in fetal sheep. J Physiol 285: 395-408, 1978. (Pubitemid 9083852)
22. Kaneko M. White S. Homan J. Richardson B.S. Cerebral blood flow and metabolism in relation to electrocortical activity with severe umbilical cord occlusion in the near-term ovine fetus American Journal of Obstetrics and Gynecology 2003 188 4 961-972 DOI 10.1067/mob.2003.219 22. Kaneko M, White S, Homan J, Richardson B. Cerebral blood flow and metabolism in relation to electrocortical activity with severe umbilical cord occlusion in the near-term ovine fetus. Am J Obstet Gynecol 188: 961-972, 2003. (Pubitemid 36530046)
23. Kawagoe Y. Green L. White S. Richardson B.S. Intermittent umbilical cord occlusion in the ovine fetus near term: Effects on behavioral state activity American Journal of Obstetrics and Gynecology 1999 181 6 1520-1529 23. Kawagoe Y, Green L, White S, Richardson B. Intermittent umbilical cord occlusion in the ovine fetus near term: effects on behavioral state activity. Am J Obstet Gynecol 181: 1520-1529, 1999. (Pubitemid 30021902)
24. Kitterman J.A. Liggins G.C. Clements J.A. Tooley W.H. Stimulation of breathing movements in fetal sheep by inhibitors of prostaglandin synthesis Journal of Developmental Physiology 1979 1 6 453-466 24. Kitterman JA, Liggins GC, Clements JA, Tooley WH. Stimulation of breathing movements in fetal sheep by inhibitors of prostaglandin synthesis. J Dev Physiol 1: 453-466, 1979. (Pubitemid 10008625)
25. Koos B.J. Central stimulation of breathing movements in fetal lambs by prostaglandin synthetase inhibitors Journal of Physiology 1985 VOL. 362 455-466 25. Koos BJ. Central stimulation of breathing movements in fetal lambs by prostaglandin synthetase inhibitors. J Physiol 362: 455-466, 1985. (Pubitemid 15122259)
26. Koos B.J. Chau A. Matsuura M. Punla O. Kruger L. Thalamic locus mediates hypoxic inhibition of breathing in fetal sheep Journal of Neurophysiology 1998 79 5 2383-2393 26. Koos BJ, Chau A, Matsuura M, Punla O, Kruger L. Thalamic locus mediates hypoxic inhibition of breathing in fetal sheep. J Neurophysiol 79: 2383-2393, 1998. (Pubitemid 28261627)
27. Kumar A, Mittal R, Khanna HD, Basu S. Free radical injury and blood-brain barrier permeability in hypoxic-ischemic encephalopathy. Pediatrics 122: e722-e727, 2008.
28. Leviton A. Dammann O. O'Shea T.M. Paneth N. Adult stroke and perinatal brain damage: Like grandparent, like grandchild? Neuropediatrics 2002 33 6 281-287 DOI 10.1055/s-2002-37089 28. Leviton A, Dammann O, O'Shea TM, Paneth N. Adult stroke and perinatal brain damage: like grandparent, like grandchild? Neuropediatrics 33: 281-287, 2002. (Pubitemid 36222138)
29. Lingwood B.E. Dunster K.R. Healy G.N. Ward L.C. Colditz P.B. Cerebral impedance and neurological outcome following a mild or severe hypoxic/ischemic episode in neonatal piglets Brain Research 2003 969 1 2 160-167 DOI 10.1016/S0006-8993(03)02295-9 29. Lingwood BE, Dunster KR, Healy GN, Ward LC, Colditz PB. Cerebral impedance and neurological outcome following a mild or severe hypoxic/ ischemic episode in neonatal piglets. Brain Res 969: 160-167, 2003. (Pubitemid 36369623)
30. Mallard EC, Gunn AJ, Williams CE, Johnston BM, Gluckman PD. Transient umbilical cord occlusion causes hippocampal damage in the fetal sheep. Am J Obstet Gynecol 167: 1423-1430, 1992.
31. Mallard E.C. Williams C.E. Johnston B.M. Gluckman P.D. Increased vulnerability to neuronal damage after umbilical cord occlusion in fetal sheep with advancing gestation American Journal of Obstetrics and Gynecology 1994 170 1 I 206-214 31. Mallard EC, Williams CE, Johnston BM, Gluckman PD. Increased vulnerability to neuronal damage after umbilical cord occlusion in fetal sheep with advancing gestation. Am J Obstet Gynecol 170: 206-214, 1994. (Pubitemid 24084056)
32. Merenda A. Gugliotta M. Holloway R. Levasseur J.E. Alessandri B. Sun D. Bullock M.R. Validation of brain extracellular glycerol as an indicator of cellular membrane damage due to free radical activity after traumatic brain injury Journal of Neurotrauma 2008 25 5 527-537 DOI 10.1089/neu.2007.0359 32. Merenda A, Gugliotta M, Holloway R, Levasseur JE, Alessandri B, Sun D, Bullock MR. Validation of brain extracellular glycerol as an indicator of cellular membrane damage due to free radical activity after traumatic brain injury. J Neurotrauma 25: 527-537, 2008. (Pubitemid 351685484)
33. Miller S.L. Yan E.B. Castillo-Melendez M. Jenkin G. Walker D.W. Melatonin provides neuroprotection in the late-gestation fetal sheep brain in response to umbilical cord occlusion Developmental Neuroscience 2005 27 2 4 200-210 DOI 10.1159/000085993 33. Miller SL, Yan EB, Castillo-Melendez M, Jenkin G, Walker DW. Melatonin provides neuroprotection in the late-gestation fetal sheep brain in response to umbilical cord occlusion. Dev Neurosci 27: 200-210, 2005. (Pubitemid 41096227)
34. Quilligan E.J. Clewlow F. Johnston B.M. Walker D.W. Effect of 5-hydroxytryptophan on electrocortical activity and breathing movements of fetal sheep American Journal of Obstetrics and Gynecology 1981 141 3 271-275 34. Quilligan EJ, Clewlow F, Johnston BM, Walker DW. Effect of 5-hydroxytryptophan on electrocortical activity and breathing movements of fetal sheep. Am J Obstet Gynecol 141: 271-275, 1981. (Pubitemid 11026956)
35. st Meeting of the Fetal and Neonatal Physiological Society, Abstract # 106, 2004 (http://www.fnps-society.org).
36. Reddy K. Mallard C. Guan J. Marks K. Bennet L. Gunning M. Gunn A. Gluckman P. Williams C.E. Maturational change in the cortical response to hypoperfusion injury in the fetal sheep Pediatric Research 1998 43 5 674-682 36. Reddy K, Mallard C, Guan J, Marks K, Bennet L, Gunning M, Gunn A, Gluckman P, Williams C. Maturational change in the cortical response to hypoperfusion injury in the fetal sheep. Pediatr Res 43: 674-682, 1998. (Pubitemid 28196461)
37. Siesjo BK, Katsura K. Ischemic brain damage: focus on lipids and lipid mediators. Adv Exp Med Biol 318: 41-56, 1992.
38. Sperling M.A. Christensen R.A. Ganguli S. Anand R. Adrenergic modulation of pancreatic hormone secretion in utero: Studies in fetal sheep Pediatric Research 1980 14 3 203-208 38. Sperling MA, Christensen RA, Ganguli S, Anand R. Adrenergic modulation of pancreatic hormone secretion in utero: studies in fetal sheep. Ped Res 14: 203-208, 1980. (Pubitemid 10133513)
39. Sunshine P. Perinatal asphyxia: an overview. In: Fetal and Neonatal Brain Injury, edited by Stevenson DK, Benitz WE and Sunshine P. Cambridge, UK: Cambridge University Press, 2003, p. 3-29.
40. Thariat J, Collin F, Marchetti C, Ahmed-Adrar NS, Vitrac H, Jore D, Gardes-Albert M. Marked difference in cytochrome c oxidation mediated by HO(*) and/or O(2)(*-) free radicals in vitro. Biochimie 90: 1442-1451, 2008.
41. Vannucci S.J. Seaman L.B. Vannucci R.C. Effects of hypoxia-ischemia on GLUT1 and GLUT3 glucose transporters in immature rat brain Journal of Cerebral Blood Flow and Metabolism 1996 16 1 77-81 41. Vannucci SJ, Seaman LB, Vannucci RC. Effects of hypoxia-ischemia on GLUT1 and GLUT3 glucose transporters in immature rat brain. J Cereb Blood Flow Metab 16: 77-81, 1996. (Pubitemid 26007952)
42. Watson C.S. Schaefer R. White S.E. Homan J.H. Fraher L. Harding R. Bocking A.D. Effect of intermittent umbilical cord occlusion on fetal respiratory activity and brain adenosine in late-gestation sheep Reproduction, Fertility and Development 2002 14 1 2 35-42 DOI 10.1071/RD01013 42. Watson CS, Schaefer R, White SE, Homan JH, Fraher L, Harding R, Bocking AD. Effect of intermittent umbilical cord occlusion on fetal respiratory activity and brain adenosine in late-gestation sheep. Reprod Fert Dev 14: 35-42, 2002. (Pubitemid 34506263)
43. Williams CE, Gunn AJ, Mallard C, Gluckman PD. Outcome after ischemia in the developing sheep brain: an electroencephalographic and histological study. Ann Neurol 31: 14-21, 1992.
44. Yan E.B. Unthank J.K. Castillo-Melendez M. Miller S.L. Langford S.J. Walker D.W. Novel method for in vivo hydroxyl radical measurement by microdialysis in fetal sheep brain in utero Journal of Applied Physiology 2005 98 6 2304-2310 DOI 10.1152/japplphysiol.00617.2004 44. Yan EB, Unthank JK, Castillo-Melendez M, Miller SL, Langford SJ, Walker DW. Novel method for in vivo hydroxyl radical measurement by microdialysis in fetal sheep brain in utero. J Appl Physiol 98: 2304-2310, 2005. (Pubitemid 40726929)
45. Yokoyama H, Kuroiwa H, Yano R, Araki T. Targeting reactive oxygen species, reactive nitrogen species, and inflammation in MPTP neurotoxicity and Parkinson's disease. Neurol Sci 29: 293-301, 2008.