Endotoxin has acute and chronic effects on the cerebral circulation of fetal sheep

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 296, Issue 3, 2009, Pages

  Feng, Susan Y S ^a   Phillips, David J ^a   Stockx, Elaine M ^a   Yu, Victor Y H ^a,b   Walker, Adrian M ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b MONASH MEDICAL CENTRE   (Australia)

Author keywords

Cerebral blood flow; Fetus; Oxygen transport

Indexed keywords

BRADYKININ; ENDOTOXIN; LIPOPOLYSACCHARIDE; SODIUM CHLORIDE; CYTOKINE; ENDOTOXIN, ESCHERICHIA COLI; NITRATE; NITRITE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL OXYGEN SATURATION; ARTICLE; BRAIN BLOOD FLOW; BRAIN CIRCULATION; BRAIN HEMORRHAGE; BRAIN HYPOXIA; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN VASCULAR RESISTANCE; CONTROLLED STUDY; ENDOTOXEMIA; FETUS; HISTOLOGY; NONHUMAN; OXYGEN TRANSPORT; PRIORITY JOURNAL; SHEEP; SURVIVAL; VASOCONSTRICTION; VASODILATATION; ANIMAL; BIOSYNTHESIS; BLOOD; BLOOD PRESSURE; CEREBROSPINAL FLUID; DRUG EFFECT; ENDOTHELIUM CELL; FEMALE; FETUS DEATH; METABOLISM; OXYGEN CONSUMPTION; PHYSIOLOGY; PREGNANCY; STATISTICAL ANALYSIS; VASCULARIZATION;

ANIMALS; BLOOD PRESSURE; CEREBROSPINAL FLUID; CEREBROVASCULAR CIRCULATION; CYTOKINES; DATA INTERPRETATION, STATISTICAL; ENDOTHELIAL CELLS; ENDOTOXINS; FEMALE; FETAL DEATH; FETUS; LIPOPOLYSACCHARIDES; NITRATES; NITRITES; OXYGEN CONSUMPTION; PREGNANCY; SHEEP; TUMOR NECROSIS FACTOR-ALPHA; VASODILATION;

EID: 64149100404     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00087.2008     Document Type: Article

References (78)

1. Andrews T, Zhang P, Bhat NR. TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors. J Neurosci Res 54: 574-583, 1998. (Pubitemid 28546060)
2. Arias F, Tomich P. Etiology and outcome of low birth weight and preterm infants. Obstet Gynecol 60: 277-281, 1982. (Pubitemid 12048114)
3. Bowton DL, Bertels NH, Prough DS, Stump DA. Cerebral blood flow is reduced in patients with sepsis syndrome. Crit Care Med 17: 399-403, 1989.
4. Bustamante SA, Pang Y, Romero S, Pierce MR, Voelker CA, Thompson JH, Sandoval M, Liu X, Miller MJ. Inducible nitric oxide synthase and the regulation of central vessel caliber in the fetal rat. Circulation 94: 1948-1953, 1996. (Pubitemid 26349310)
5. Cheng YJ, Yang BC, Hsieh WC, Huang BM, Liu MY. Enhancement of TNF-alpha expression does not trigger apoptosis upon exposure of glial cells to lead and lipopolysaccharide. Toxicology 178: 183-191, 2002.
6. Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP, Pober JS, Wick TM, Konkle BA, Schwartz BS, Barnathan ES, McCrae KR, Hug BA, Schmidt AM, Stern DM. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 91: 3527-3561, 1998. (Pubitemid 28225719)
7. Coumans AB, Garnier Y, Supcun S, Jensen A, Berger R, Hasaart TH. Nitric oxide and fetal organ blood flow during normoxia and hypoxemia in endotoxin-treated fetal sheep. Obstet Gynecol 105: 145-155, 2005. (Pubitemid 40189925)
8. Dalitz P, Harding R, Rees SM, Cock ML. Prolonged reductions in placental blood flow and cerebral oxygen delivery in preterm fetal sheep exposed to endotoxin: possible factors in white matter injury after acute infection. J Soc Gynecol Investig 10: 283-290, 2003. (Pubitemid 36802329)
9. Dammann O, Leviton A. Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 42: 1-8, 1997. (Pubitemid 27276750)
10. Duncan JR, Cock ML, Scheerlinck JP, Westcott KT, McLean C, Harding R, Rees SM. White matter injury after repeated endotoxin exposure in the preterm ovine fetus. Pediatr Res 52: 941-949, 2002. (Pubitemid 35379477)
11. Duncan JR, Cock ML, Suzuki K, Scheerlinck JP, Harding R, Rees SM. Chronic endotoxin exposure causes brain injury in the ovine fetus in the absence of hypoxemia. J Soc Gynecol Investig 13: 87-96, 2006. (Pubitemid 43155839)
12. Dweik RA. Nitric oxide, hypoxia, and superoxide: the good, the bad, and the ugly! Thorax 60: 265-267, 2005.
13. Eklind S, Mallard C, Leverin AL, Gilland E, Blomgren K, Mattsby-Baltzer I, Hagberg H. Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 13: 1101-1106, 2001. (Pubitemid 32275747)
14. Ekstrom-Jodal B, Elfverson J, Larsson LE. Early effects of E. coli endotoxin on superior sagittal sinus blood flow. An experimental study in dogs. Acta Anaesthesiol Scand 26: 171-174, 1982. (Pubitemid 12086115)
15. Garnier Y, Coumans A, Berger R, Jensen A, Hasaart TH. Endotoxemia severely affects circulation during normoxia and asphyxia in immature fetal sheep. J Soc Gynecol Investig 8: 134-142, 2001. (Pubitemid 32493018)
16. Gilbert P, Tremblay J, Thorin E. Endothelium-derived endothelin-1 reduces cerebral artery sensitivity to nitric oxide by a protein kinase C-independent pathway. Stroke 32: 2351-2355, 2001. (Pubitemid 32954808)
17. Goncalves LF, Chaiworapongsa T, Romero R. Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev 8: 3-13, 2002. (Pubitemid 34754487)
18. Gorlach C, Wahl M. Bradykinin dilates rat middle cerebral artery and its large branches via endothelial B2 receptors and release of nitric oxide. Peptides 17: 1373-1378, 1996. (Pubitemid 27016350)
19. Graham EM, Holcroft CJ, Rai KK, Donohue PK, Allen MC. Neonatal cerebral white matter injury in preterm infants is associated with culture positive infections and only rarely with metabolic acidosis. Am J Obstet Gynecol 191: 1305-1310, 2004.
20. Grant DA, Franzini C, Wild J, Walker AM. Continuous measurement of blood flow in the superior sagittal sinus of the lamb. Am J Physiol Regul Integr Comp Physiol 269: R274-R279, 1995.
21. Green LR, Bennet L, Hanson MA. The role of nitric oxide synthesis in cardiovascular responses to acute hypoxia in the late gestation sheep fetus. J Physiol 497: 271-277, 1996. (Pubitemid 26397689)
22. Greisen G. Cerebral blood flow and energy metabolism in the newborn. Clin Perinatol 24: 531-546, 1997. (Pubitemid 27387983)
23. Grether JK, Cummins SK, Nelson KB. The California Cerebral Palsy Project. Paediatr Perinat Epidemiol 6: 339-351, 1992.
24. Grether JK, Nelson KB. Maternal infection and cerebral palsy in infants of normal birth weight. JAMA 278: 207-211, 1997.
25. 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. (Pubitemid 34701668)
26. Hagberg H, Peebles D, Mallard C. Models of white matter injury: comparison of infectious, hypoxic-ischemic, and excitotoxic insults. Ment Retard Dev Disabil Res Rev 8: 30-38, 2002. (Pubitemid 34754491)
27. Hallemeesch MM, Janssen BJ, de Jonge WJ, Soeters PB, Lamers WH, Deutz NE. NO production by cNOS and iNOS reflects blood pressure changes in LPS-challenged mice. Am J Physiol Endocrinol Metab 285: E871-E875, 2003.
28. Hamilton GS, Edwards B, Solin P, Walker AM. A model of coronary artery endothelial dysfunction in the sleeping lamb. Sleep Med 7: 573-579, 2006. (Pubitemid 44480747)
29. Harris WH, Pittman QJ, Veale WL, Cooper KE, Van Petten GR. Cardiovascular effects of fever in the ewe and fetal lamb. Am J Obstet Gynecol 128: 262-265, 1977.
30. Hernanz R, Alonso MJ, Briones AM, Vila E, Simonsen U, Salaices M. Mechanisms involved in the early increase of serotonin contraction evoked by endotoxin in rat middle cerebral arteries. Br J Pharmacol 140: 671-680, 2003. (Pubitemid 37386431)
31. Hutton LC, Castillo-Melendez M, Smythe GA, Walker DW. Microglial activation, macrophage infiltration, and evidence of cell death in the fetal brain after uteroplacental administration of lipopolysaccharide in sheep in late gestation. Am J Obstet Gynecol 198: 117.e1-117.e11, 2008. (Pubitemid 350309275)
32. Ikeda T, Murata Y, Quilligan EJ, Choi BH, Parer JT, Doi S, Park SD. Physiologic and histologic changes in near-term fetal lambs exposed to asphyxia by partial umbilical cord occlusion. Am J Obstet Gynecol 178: 24-32, 1998. (Pubitemid 28302789)
33. Jensen A, Garnier Y, Middelanis J, Berger R. Perinatal brain damage - from pathophysiology to prevention. Eur J Obstet Gynecol Reprod Biol 110, Suppl 1: S70-S79, 2003.
34. Johnson J, Sudheimer K, Davis K, Kernd G, Winn B. The Sheep Brain Atlas (Online). Michigan State University Brain Biodiversity Bank. https://www.msu.edu/brains/brains/sheep/index.html [2008].
35. Jones B, Peake K, Morris AJ, McCowan LM, Battin MR. Escherichia coli: a growing problem in early onset neonatal sepsis. Aust NZ J Obstet Gynaecol 44: 558-561, 2004. (Pubitemid 40073961)
36. Jones MD Jr, Traystman RJ. Cerebral oxygenation of the fetus, newborn, and adult. Semin Perinatol 8: 205-216, 1984.
37. Leclerc J, Pu Q, Corseaux D, Haddad E, Decoene C, Bordet R, Six I, Jude B, Vallet B. A single endotoxin injection in the rabbit causes prolonged blood vessel dysfunction and a procoagulant state. Crit Care Med 28: 3672-3678, 2000.
38. Levin ER. Endothelins as cardiovascular peptides. Am J Nephrol 16: 246-251, 1996.
39. Lin NT, Yang FL, Lee RP, Peng TC, Chen HI. Inducible nitric oxide synthase mediates cytokine release: the time course in conscious and septic rats. Life Sci 78: 1038-1043, 2006.
40. Lynch JK, Nelson KB. Epidemiology of perinatal stroke. Curr Opin Pediatr 13: 499-505, 2001.
41. Mackay MTGA. Stroke in children. Aust Fam Physician 36: 896-902, 2007.
42. Maekawa T, Fujii Y, Sadamitsu D, Yokota K, Soejima Y, Ishikawa T, Miyauchi Y, Takeshita H. Cerebral circulation and metabolism in patients with septic encephalopathy. Am J Emerg Med 9: 139-143, 1991.
43. Mallard C, Welin AK, Peebles D, Hagberg H, Kjellmer I. White matter injury following systemic endotoxemia or asphyxia in the fetal sheep. Neurochem Res 28: 215-223, 2003. (Pubitemid 36207346)
44. Mathewson AM, Wadsworth RM. Induction of iNOS restricts functional activity of both eNOS and nNOS in pig cerebral artery. Nitric Oxide 11: 331-339, 2004.
45. McClure L, O'Connor AE, Hayward S, Jenkin G, Walker DW, Phillips DJ. Effects of age and pregnancy on the circulatory activin response of sheep to acute inflammatory challenge by lipopolysaccharide. J Endocrinol 185: 139-149, 2005. (Pubitemid 40585075)
46. McCrabb GJ, Harding R. Role of nitric oxide in the regulation of cerebral blood flow in the ovine foetus. Clin Exp Pharmacol Physiol 23: 855-860, 1996. (Pubitemid 26361705)
47. Minc-Golomb D, Tsarfaty I, Schwartz JP. Expression of inducible nitric oxide synthase by neurones following exposure to endotoxin and cytokine. Br J Pharmacol 112: 720-722, 1994. (Pubitemid 24199072)
48. Moller K, Strauss GI, Qvist J, Fonsmark L, Knudsen GM, Larsen FS, Krabbe KS, Skinhoj P, Pedersen BK. Cerebral blood flow and oxidative metabolism during human endotoxemia. J Cereb Blood Flow Metab 22: 1262-1270, 2002.
49. Nelson KB, Dambrosia JM, Grether JK, Phillips TM. Neonatal cytokines and coagulation factors in children with cerebral palsy. Ann Neurol 44: 665-675, 1998.
50. Nelson KB, Willoughby RE. Infection, inflammation and the risk of cerebral palsy. Curr Opin Neurol 13: 133-139, 2000.
51. Northington FJ, Tobin JR, Harris AP, Traystman RJ, Koehler RC. Developmental and regional differences in nitric oxide synthase activity and blood flow in the sheep brain. J Cereb Blood Flow Metab 17: 109-115, 1997.
52. Okamoto H, Ito O, Roman RJ, Hudetz AG. Role of inducible nitric oxide synthase and cyclooxygenase-2 in endotoxin-induced cerebral hyperemia. Stroke 29: 1209-1218, 1998. (Pubitemid 28265479)
53. Palmer LA, Semenza GL, Stoler MH, Johns RA. Hypoxia induces type II NOS gene expression in pulmonary artery endothelial cells via HIF-1. Am J Physiol Lung Cell Mol Physiol 274: L212-L219, 1998.
54. Pearce W. Hypoxic regulation of the fetal cerebral circulation. J Appl Physiol 100: 731-738, 2006. (Pubitemid 43671632)
55. Peebles D. Intrauterine infection and periantal brain injury. In: Scientific Advisory Committee Opinion Paper 3, Royal College of Obstetricians and Gynaecologists, UK, 2007.
56. Peebles DM, Miller S, Newman JP, Scott R, Hanson MA. The effect of systemic administration of lipopolysaccharide on cerebral haemodynamics and oxygenation in the 0.65 gestation ovine fetus in utero. BJOG 110: 735-743, 2003. (Pubitemid 36936775)
57. Redline RW. Placental inflammation. Semin Neonatol 9: 265-274, 2004.
58. Rosengarten B, Hecht M, Auch D, Ghofrani HA, Schermuly RT, Grimminger F, Kaps M. Microcirculatory dysfunction in the brain precedes changes in evoked potentials in endotoxin-induced sepsis syndrome in rats. Cerebrovasc Dis 23: 140-147, 2007. (Pubitemid 46239154)
59. Seri I, Noori S. Diagnosis and treatment of neonatal hypotension outside the transitional period. Early Hum Dev 81: 405-411, 2005. (Pubitemid 40791130)
60. Sibson NR, Blamire AM, Perry VH, Gauldie J, Styles P, Anthony DC. TNF-alpha reduces cerebral blood volume and disrupts tissue homeostasis via an endothelin- and TNFR2-dependent pathway. Brain 125: 2446-2459, 2002. (Pubitemid 35303504)
61. Siesjo B, Katsura K, Pahlmark K, Smith ML. The multiple causes of ischemic brain damage: a speculative synthesis. In: Pharmacology of Cerebral Ischemia, edited by Krieglstein J and Oberpichler-Schwenk H. Stuttgart, Germany: Medpharm Scientific, 1992, p. 511-525.
62. Skopal J, Turbucz P, Vastag M, Bori Z, Pek M, deChatel R, Nagy Z, Toth M, Karadi I. Regulation of endothelin release from human brain microvessel endothelial cells. J Cardiovasc Pharmacol 31, Suppl 1: S370-S372, 1998.
63. Soul JS, Hammer PE, Tsuji M, Saul JP, Bassan H, Limperopoulos C, Disalvo DN, Moore M, Akins P, Ringer S, Volpe JJ, Trachtenberg F, du Plessis AJ. Fluctuating pressure-passivity is common in the cerebral circulation of sick premature infants. Pediatr Res 61: 467-473, 2007. (Pubitemid 46569302)
64. Stoll BJ, Hansen NI, Adams-Chapman I, Fanaroff AA, Hintz SR, Vohr B, Higgins RD. Neurodevelopmental and growth impairment among extremely low-birth-weight infants with neonatal infection. JAMA 292: 2357-2365, 2004. (Pubitemid 39491920)
65. Stuehr DJ. Mammalian nitric oxide synthases. Biochim Biophys Acta 1411: 217-230, 1999.
66. Svedin P, Kjellmer I, Welin AK, Blad S, Mallard C. Maturational effects of lipopolysaccharide on white-matter injury in fetal sheep. J Child Neurol 20: 960-964, 2005. (Pubitemid 43299326)
67. Ueno M, Lee TJ. Endotoxin decreases the contractile responses of the porcine basilar artery to vasoactive substances. J Cereb Blood Flow Metab 13: 712-719, 1993. (Pubitemid 23187515)
68. Wang X, Hagberg H, Nie C, Zhu C, Ikeda T, Mallard C. Dual role of intrauterine immune challenge on neonatal and adult brain vulnerability to hypoxia-ischemia. J Neuropathol Exp Neurol 66: 552-561, 2007. (Pubitemid 46869697)
69. Wang X, Rousset CI, Hagberg H, Mallard C. Lipopolysaccharide-induced inflammation and perinatal brain injury. Semin Fetal Neonatal Med 11: 343-353, 2006. (Pubitemid 44038704)
70. Whyte RI, Warren HS, Greene E, Glennon ML, Robinson DR, Zapol WM. Tolerance to low-dose endotoxin in awake sheep. J Appl Physiol 66: 2546-2552, 1989. (Pubitemid 19164948)
71. Wu YW, Colford JM Jr. Chorioamnionitis as a risk factor for cerebral palsy: a meta-analysis. JAMA 284: 1417-1424, 2000.
72. Wu YW, Escobar GJ, Grether JK, Croen LA, Greene JD, Newman TB. Chorioamnionitis and cerebral palsy in term and near-term infants. JAMA 290: 2677-2684, 2003.
73. Yan E, Castillo-Melendez M, Nicholls T, Hirst J, Walker D. Cerebrovascular responses in the fetal sheep brain to low-dose endotoxin. Pediatr Res 55: 855-863, 2004. (Pubitemid 38520455)
74. Yanowitz TD, Jordan JA, Gilmour CH, Towbin R, Bowen A, Roberts JM, Brozanski BS. Hemodynamic disturbances in premature infants born after chorioamnionitis: association with cord blood cytokine concentrations. Pediatr Res 51: 310-316, 2002. (Pubitemid 34174966)
75. Yoon BH, Jun JK, Romero R, Park KH, Gomez R, Choi JH, Kim IO. Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1beta, and tumor necrosis factor-alpha), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol 177: 19-26, 1997. (Pubitemid 27327305)
76. Yoon BH, Park CW, Chaiworapongsa T. Intrauterine infection and the development of cerebral palsy. BJOG 110, Suppl 20: 124-127, 2003. (Pubitemid 36577401)
77. Yoon BH, Romero R, Kim CJ, Koo JN, Choe G, Syn HC, Chi JG. High expression of tumor necrosis factor-alpha and interleukin-6 in periventricular leukomalacia. Am J Obstet Gynecol 177: 406-411, 1997. (Pubitemid 27385721)
78. Yoon BH, Romero R, Moon JB, Shim SS, Kim M, Kim G, Jun JK. Clinical significance of intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Obstet Gynecol 185: 1130-1136, 2001. (Pubitemid 33097376)