Regulation of cytochrome oxidase redox state during umbilical cord occlusion in preterm fetal sheep

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 292, Issue 4, 2007, Pages

  Bennet, Laura ^a   Roelfsema, Vincent ^a   Dean, Justin M ^a   Wassink, Guido ^a   Power, Gordon G ^b   Jensen, Ellen C ^a   Gunn, Alistair Jan ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Asphyxia; Preterm; Umbilical cord occlusion

Indexed keywords

CYTOCHROME C OXIDASE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN BLOOD FLOW; BRAIN METABOLISM; BRAIN PERFUSION; CAROTID ARTERY FLOW; CONTROLLED STUDY; CYTOTOXICITY; EDEMA; ELECTROENCEPHALOGRAM; ELECTRON TRANSPORT; FETUS; GESTATIONAL AGE; HYPOTENSION; MITOCHONDRION; NEAR INFRARED SPECTROSCOPY; NONHUMAN; OXIDATION REDUCTION STATE; PARIETAL LOBE; PREMATURITY; PRIORITY JOURNAL; SHEEP; THERMOGENESIS; TISSUE OXYGENATION; UMBILICAL CORD;

ANIMALS; BLOOD GLUCOSE; BRAIN; CARBON DIOXIDE; CAROTID ARTERIES; CEREBRAL CORTEX; EDEMA; ELECTRIC IMPEDANCE; ELECTROENCEPHALOGRAPHY; ELECTRON TRANSPORT COMPLEX IV; FEMALE; FETAL HYPOXIA; GESTATIONAL AGE; HYDROGEN-ION CONCENTRATION; LACTIC ACID; OXIDATION-REDUCTION; OXYGEN; PREGNANCY; SHEEP; THERMOGENESIS; TIME FACTORS; UMBILICAL CORD;

EID: 34147129619     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00743.2006     Document Type: Article

References (56)

1. Baker MA, Hayward JN. The influence of the nasal mucosa and the carotid rete upon hypothalamic temperature in sheep. J Physiol 198: 561-579, 1968.
2. Barlow RM. The foetal sheep: morphogenesis of the nervous system and histochemical aspects of myelination. J Comp Neurol 135: 249-262, 1969.
3. Bennet L, Roelfsema V, Pathipati P, Quaedackers J, Gunn AJ. Relationship between evolving epileptiform activity and delayed loss of mitochondrial activity after asphyxia measured by near-infrared spectroscopy in preterm fetal sheep. J Physiol 572: 141-154, 2006.
4. 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.
5. Bishai JM, Blood AB, Hunter CJ, Longo LD, Power GG. Fetal lamb cerebral blood flow (CBF) and oxygen tensions during hypoxia: a comparison of laser Doppler and microsphere measurements of CBF. J Physiol 546: 869-878, 2003.
6. Blood AB, Hunter CJ, Power GG. Adenosine mediates decreased cerebral metabolic rate and increased cerebral blood flow during acute moderate hypoxia in the near-term fetal sheep. J Physiol 553: 935-945, 2003.
7. Blood AB, Hunter CJ, Power GG. The role of adenosine in regulation of cerebral blood flow during hypoxia in the near-term fetal sheep. J Physiol 543: 1015-1023, 2002.
8. Boushel R, Piantadosi CA. Near-infrared spectroscopy for monitoring muscle oxygenation. Acta Physiol Scand 168: 615-622, 2000.
9. Boyle R. New pneumatical experiments about respiration. Philos Trans 5: 2011-2031, 1670.
10. Brun NC, Moen A, Borch K, Saugstad OD, Greisen G. Near-infrared monitoring of cerebral tissue oxygen saturation and blood volume in newborn piglets. Am J Physiol Heart Circ Physiol 273: H682-H686, 1997.
11. Clementi E, Brown GC, Feelisch M, Moncada S. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc Natl Acad Sci USA 95: 7631-7636, 1998.
12. Cooper CE, Springett R. Measurement of cytochrome oxidase and mitochondrial energetics by near-infrared spectroscopy. Philos Trans R Soc Lond B Biol Sci 352: 669-676, 1997.
13. Dean JM, George SA, Wassink G, Gunn AJ, Bennet L. Suppression of post hypoxic-ischemic EEG transients with dizocilpine is associated with partial striatal protection in the preterm fetal sheep. Neuropharmacology 50: 491-503, 2006.
14. 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.
15. Fraser M, Bennet L, Gunning M, Williams CE, Gluckman PD, George S, Gunn AJ. Cortical electroencephalogram suppression is associated with post-ischemic cortical injury in 0.65 gestation fetal sheep. Brain Res Dev Brain Res 154: 45-55, 2005.
16. Gagnon RE, Macnab AJ, Gagnon FA, Leblanc JG. Brain, spine, and muscle cytochrome Cu-A redox patterns of change during hypothermic circulatory arrest in swine. Comp Biochem Physiol A Mol Integr Physiol 141: 264-270, 2005.
17. George S, Gunn AJ, Westgate JA, Brabyn C, Guan J, Bennet L. Fetal heart rate variability and brainstem injury after asphyxia in preterm fetal sheep. Am J Physiol Regul Integr Comp Physiol 287: R925-R933, 2004.
18. Gilbert RD, Schroder H, Kawamura T, Dale PS, Power GG. Heat transfer pathways between fetal lamb and ewe. J Appl Physiol 59: 634-638, 1985.
19. Gonzalez H, Hunter CJ, Bennet L, Power GG, Gunn AJ. Cerebral oxygenation during post-asphyxial seizures in near-term fetal sheep. J Cereb Blood Flow Metab 25: 911-918, 2005.
20. Gratton R, Carmichael L, Homan J, Richardson B. Carotid arterial blood flow in the ovine fetus as a continuous measure of cerebral blood flow. J Soc Gynecol Investig 3: 60-65, 1996.
21. Gunn AJ, Gunn TR, de Haan HH, Williams CE, Gluckman PD. Dramatic neuronal rescue with prolonged selective head cooling after ischemia in fetal lambs. J Clin Invest 99: 248-256, 1997.
22. Gunn AJ, Quaedackers JS, Guan J, Heineman E, Bennet L. The premature fetus: not as defenseless as we thought, but still paradoxically vulnerable? Dev Neurosci 23: 175-179, 2001.
23. Hunter CJ, Bennet L, Power GG, Roelfsema V, Blood AB, Quaedackers JS, George S, Guan J, Gunn AJ. Key neuroprotective role for endogenous adenosine A1 receptor activation during asphyxia in the fetal sheep. Stroke 34: 2240-2245, 2003.
24. 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.
25. 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.
26. Jensen A, Hohmann M, Kunzel W. Dynamic changes in organ blood flow and oxygen consumption during acute asphyxia in fetal sheep. J Dev Physiol 9: 543-559, 1987.
27. Jensen EC, Bennet L, Hunter CJ, Power GG, 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.
28. Keunen H, Blanco CE, van Reempts JL, Hasaart TH. Absence of neuronal damage after umbilical cord occlusion of 10, 15, and 20 minutes in midgestation fetal sheep. Am J Obstet Gynecol 176: 515-520, 1997.
29. Keunen H, Deutz NE, van Reempts JL, Hasaart TH. Transient umbilical cord occlusion in late-gestation fetal sheep results in hippocampal damage but not in cerebral arteriovenous difference for nitrite, a stable end product of nitric oxide. J Soc Gynecol Investig 6: 120-126, 1999.
30. Kubonoya K, Yoneyama Y, Sawa R, Araki T, Power GG. Brain temperature and metabolic responses during umbilical cord occlusion in fetal sheep. Pflügers Arch 436: 667-672, 1998.
31. Lawler FH, Brace RA. Fetal and maternal arterial pressures and heart rates: histograms, correlations, and rhythms. Am J Physiol Regul Integr Comp Physiol 243: R433-R444, 1982.
32. Ley D, Oskarsson G, Bellander M, Hernandez-Andrade E, Lingman G, Marsal K, Olsson T, Pesonen E, Thorngren-Jerneck K, Werner O, Hellstrom-Westas L. Different responses of myocardial and cerebral blood flow to cord occlusion in exteriorized fetal sheep. Pediatr Res 55: 568-575, 2004.
33. Lotgering FK, Bishai JM, Struijk PC, Blood AB, Hunter CJ, Power GG, Longo LD. Ten-minute umbilical cord occlusion markedly reduces cerebral blood flow and heat production in fetal sheep. Am J Obstet Gynecol 189: 233-238, 2003.
34. Lutz PL, Milton SL. Negotiating brain anoxia survival in the turtle. J Exp Biol 207: 3141-3147, 2004.
35. 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.
36. Marks KA, Mallard EC, Roberts I, Williams CE, Sirimanne ES, Johnston B, Gluckman PD, Edwards AD. Delayed vasodilation and altered oxygenation after cerebral ischemia in fetal sheep. Pediatr Res 39: 48-54, 1996.
37. 31P nuclear magnetic resonance spectroscopy. Anesth Analg 83: 513-518, 1996.
38. Mortola JP. Implications of hypoxic hypometabolism during mammalian ontogenesis. Respir Physiol Neurobiol 141: 345-356, 2004.
39. Nakajima W, Ishida A, Takada G. Effect of anoxia on striatal monoamine metabolism in immature rat brain compared with that of hypoxia: an in vivo microdialysis study. Brain Res 740: 316-322, 1996.
40. Newman JP, Peebles DM, Hanson MA. Adenosine produces changes in cerebral hemodynamics and metabolism as assessed by near-infrared spectroscopy in late-gestation fetal sheep in utero. Pediatr Res 50: 217-221, 2001.
41. Newman JP, Peebles DM, Harding SR, Springett R, Hanson MA. Hemodynamic and metabolic responses to moderate asphyxia in brain and skeletal muscle of late-gestation fetal sheep. J Appl Physiol 88: 82-90, 2000.
42. Nguyen P, Yan EB, Castillo-Melendez M, Walker DW, Hirst JJ. Increased allopregnanolone levels in the fetal sheep brain following umbilical cord occlusion. J Physiol 560: 593-602, 2004.
43. Quaedackers JS, Roelfsema V, Heineman E, Gunn AJ, Bennet L. The role of the sympathetic nervous system in post-asphyxial intestinal hypoperfusion in the preterm sheep fetus. J Physiol 557: 1033-1044, 2004.
44. 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.
45. Reynolds EO, Wyatt JS, Azzopardi D, Delpy DT, Cady EB, Cope M, Wray S. New non-invasive methods for assessing brain oxygenation and haemodynamics. Br Med Bull 44: 1052-1075, 1988.
46. Soul JS, Taylor GA, Wypij D, Duplessis AJ, Volpe JJ. Noninvasive detection of changes in cerebral blood flow by near-infrared spectroscopy in a piglet model of hydrocephalus. Pediatr Res 48: 445-449, 2000.
47. 31P NMRS and NIRS. Adv Exp Med Biol 530: 555-563, 2003.
48. Sylvia AL, Seidler FJ, Slotkin TA. Effect of transient hypoxia on oxygenation of the developing rat brain: relationships among haemoglobin saturation, autoregulation of blood flow and mitochondrial redox state. J Dev Physiol 12: 287-292, 1989.
49. Tan WK, Williams CE, During MJ, Mallard CE, Gunning MI, Gunn AJ, Gluckman PD. Accumulation of cytotoxins during the development of seizures and edema after hypoxic-ischemic injury in late gestation fetal sheep. Pediatr Res 39: 791-797, 1996.
50. Tsuji M, duPlessis A, Taylor G, Crocker R, Volpe JJ. Near infrared spectroscopy detects cerebral ischemia during hypotension in piglets. Pediatr Res 44: 591-595, 1998.
51. Van Bel F, Dorrepaal CA, Benders MJ, Zeeuwe PE, van de Bor M, Berger HM. Changes in cerebral hemodynamics and oxygenation in the first 24 hours after birth asphyxia. Pediatrics 92: 365-372, 1993.
52. Van Bel F, Roman C, Klautz RJ, Teitel DF, Rudolph AM. Relationship between brain blood flow and carotid arterial flow in the sheep fetus. Pediatr Res 35: 329-333, 1994.
53. Williams CE, Gunn A, Gluckman PD. Time course of intracellular edema and epileptiform activity following prenatal cerebral ischemia in sheep. Stroke 22: 516-521, 1991.
54. Wong-Riley MT. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12: 94-101, 1989.
55. Wray S, Cope M, Delpy DT, Wyatt JS, Reynolds EO. Characterization of the near infrared absorption spectra of cytochrome aa3 and haemoglobin for the non-invasive monitoring of cerebral oxygenation. Biochim Biophys Acta 933: 184-192, 1988.
56. Wyatt JS, Cope M, Delpy DT, Richardson CE, Edwards AD, Wray S, Reynolds EO. Quantitation of cerebral blood volume in human infants by near-infrared spectroscopy. J Appl Physiol 68: 1086-1091, 1990.