Neonatal encephalopathy: An inadequate term for hypoxic-ischemic encephalopathy

Annals of Neurology

Volumn 72, Issue 2, 2012, Pages 156-166

  Volpe, Joseph J ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; CLINICAL FEATURE; CRANIAL NERVE; HUMAN; HYPOXIC ISCHEMIC ENCEPHALOPATHY; NEUROIMAGING; NEUROPATHOLOGY; NEWBORN DISEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RESPIRATION DEPRESSION; REVIEW; SEIZURE;

ANIMALS; DIAGNOSTIC IMAGING; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; INFANT; INFANT, NEWBORN; INFANT, NEWBORN, DISEASES; MAGNETIC RESONANCE IMAGING; MALE; PREGNANCY; PREGNANCY COMPLICATIONS;

EID: 84865596546     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.23647     Document Type: Review

References (125)

1. Dammann O, Ferriero D, Gressens P,. Neonatal encephalopathy or hypoxic-ischemic encephalopathy? Appropriate terminology matters. Pediatr Res 2011; 70: 1-2.
2. Leviton A, Nelson KB,. Problems with definitions and classifications of newborn encephalopathy. Pediatr Neurol 1992; 8: 85-90.
3. Ferriero DM,. Medical progressâneonatal brain injury. N Eng J Med 2004; 351: 1985-1995.
4. Badawi N, Kurinczuk JJ, Keogh JM, et al. Antepartum risk factors for newborn encephalopathy: the Western Australian case-control study. Br Med J 1998; 317: 1549-1553. (Pubitemid 28550234)
5. Blume HK, Li CI, Loch CM, Koepsell TD,. Intrapartum fever and chorioamnionitis as risks for encephalopathy in term newborns: a case-control study. Dev Med Child Neurol 2008; 50: 19-24.
6. Badawi N, Kurinczuk JJ, Keogh JM, et al. Intrapartum risk factors for newborn encephalopathy: the Western Australian case-control study. Br Med J 1998; 317: 1554-1558. (Pubitemid 28550235)
7. Shah DK, Lavery S, Doyle LW, et al. Use of 2-channel bedside electroencephalogram monitoring in term-born encephalopathic infants related to cerebral injury defined by magnetic resonance imaging. Pediatrics 2006; 118: 47-55. (Pubitemid 46071146)
8. Cowan F, Rutherford M, Groenendaal F, et al. Origin and timing of brain lesions in term infants with neonatal encephalopathy. Lancet 2003; 361: 736-742. (Pubitemid 36293628)
9. Volpe JJ,. Neurology of the newborn. 5th ed. Philadelphia, PA: Elsevier, 2008.
10. Rice JE III, Vannucci RC, Brierley JB,. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 1981; 9: 131-141. (Pubitemid 11191192)
11. Liu Y, Silverstein FS, Skoff R, Barks JDE,. hypoxic-ischemic oligodendroglial injury in neonatal rat brain. Pediatr Res 2002; 51: 25-33. (Pubitemid 34008206)
12. Vannucci RC, Vannucci SJ,. Perinatal hypoxic-ischemic brain damage: evolution of an animal model. Dev Neurosci 2005; 27: 81-86. (Pubitemid 41096212)
13. Vannucci RC,. Experimental models of perinatal hypoxic-ischemic brain damage. APMIS Suppl 1993; 40: 89-95. (Pubitemid 24052964)
14. Welsh FA, Vannucci RC, Brierley JB,. Columnar alterations of NADH fluorescence during hypoxia-ischemia in immature rat brain. J Cereb Blood Flow Metab 1982; 2: 221-228. (Pubitemid 12065523)
15. Vannucci RC, Lyons DT, Vasta F,. Regional cerebral blood flow during hypoxia-ischemia in immature rats. Stroke 1988; 19: 245-250. (Pubitemid 18084400)
16. Yager JY, Brucklacher RM, Vannucci RC,. Cerebral oxidative metabolism and redox state during hypoxia-ischemia and early recovery in immature rats. Am J Physiol 1991; 261: H1102-H1108.
17. Yager JY, Brucklacher RM, Vannucci RC,. Cerebral energy metabolism during hypoxia-ischemia and early recovery in immature rats. Am J Physiol 1992; 262: H672-H677.
18. Yager JY, Brucklacher RM, Vannucci RC,. Paradoxical mitochondrial oxidation in perinatal hypoxic-ischemic brain damage. Brain Res 1996; 712: 230-238. (Pubitemid 26104808)
19. Vannucci RC, Yager JY,. Glucose, lactic acid, and perinatal hypoxic-ischemic brain damage. Pediatr Neurol 1992; 8: 3-12.
20. Gordon KE, Simpson J, Statman D, Silverstein FS,. Effects of perinatal stroke on striatal amino acid efflux in rats studied with in vivo microdialysis. Stroke 1991; 22: 928-932.
21. Vannucci RC, Brucklacher RM, Vannucci SJ,. Intracellular calcium accumulation during the evolution of hypoxic-ischemic brain damage in the immature rat. Brain Res Dev Brain Res 2001; 126: 117-120. (Pubitemid 32141241)
22. Vannucci RC, Christensen MA, Yager JY,. Nature, time-course, and extent of cerebral edema in perinatal hypoxic-ischemic brain damage. Pediatr Neurol 1993; 9: 29-34. (Pubitemid 23070093)
23. Yager JY, Ashwal S,. Animal models of perinatal hypoxic-ischemic brain damage. Pediatr Neurol 2009; 40: 156-167.
24. Richardson BS, Carmichael L, Homan J, et al. Fetal cerebral, circulatory, and metabolic responses during heart rate decelerations with umbilical cord compression. Am J Obstet Gynecol 1996; 175: 929-936. (Pubitemid 26357957)
25. Richardson BS, Bocking AD,. Metabolic and circulatory adaptations to chronic hypoxia in the fetus. Comp Biochem Physiol Mol Integr Physiol 1998; 119: 717-723. (Pubitemid 28219072)
26. Williams CE, Gunn AJ, Mallard C, Gluckman PD,. Outcome after ischemia in the developing sheep brain: an electroencephalographic and histological study. Ann Neurol 1992; 31: 14-21.
27. Gunn AJ, Parer JT, Mallard EC, et al. Cerebral histologic and electrocorticographic changes after asphyxia in fetal sheep. Pediatr Res 1992; 31: 486-491.
28. Mallard EC, Williams CE, Gunn AJ, et al. Frequent episodes of brief ischemia sensitize the fetal sheep brain to neuronal loss and induce striatal injury. Pediatr Res 1993; 33: 61-65. (Pubitemid 23094128)
29. 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 1997; 41: 96-104. (Pubitemid 27008642)
30. Petersson KH, Pinar H, Stopa EG, et al. White matter injury after cerebral ischemia in ovine fetuses. Pediatr Res 2002; 51: 768-776. (Pubitemid 34547344)
31. Reddy K, Mallard C, Guan J, et al. Maturational change in the cortical response to hypoperfusion injury in the fetal sheep. Pediatr Res 1998; 43: 674-682. (Pubitemid 28196461)
32. Myers RE,. Four patterns of perinatal brain damage and their conditions of occurrence in primates. Adv Neurol 1975; 10: 223-234.
33. Myers RE,. Two patterns of perinatal brain damage and their conditions of occurrence. Am J Obstet Gynecol 1972; 112: 246-276.
34. Brann AW Jr, Myers RE,. Central nervous system findings in the newborn monkey following severe in utero partial asphyxia. Neurology 1975; 25: 327-338.
35. Leung AS, Leung EK, Paul RH,. Uterine rupture after previous cesarean delivery: maternal and fetal consequences. Am J Obstet Gynecol 1993; 169: 945-950. (Pubitemid 23317533)
36. Larroche JC,. Developmental pathology of the neonate. New York, NY: Excerpta Medica, 1977.
37. Norman MG,. Perinatal brain damage. In:, Rosenberg HS, Boilande RP, eds. Perspectives in pediatric pathology. Vol 4. Chicago, IL: Mosby, 1978: 41-92.
38. Rorke LB,. Pathology of perinatal brain injury. New York, NY: Raven Press, 1982.
39. Friede RL,. Developmental neuropathology. 2nd ed. New York, NY: Springer-Verlag, 1989.
40. Rorke LB,. Anatomical features of the developing brain implicated in pathogenesis of hypoxic-ischemic injury. Brain Pathol 1992; 2: 211-221.
41. Folkerth RD, Kinney HC,. Disorders of the perinatal period. In:, Love S, Louis DN, Ellison D, eds. Greenfield's neuropathology. Vol 1. 8th ed. London, UK: Hodder Arnold, 2008: 241-334.
42. Edwards AD, Yue X, Cox P, et al. Apoptosis in the brains of infants suffering intrauterine cerebral injury. Pediatr Res 1997; 42: 684-689. (Pubitemid 27459479)
43. Becher JC, Bell JE, Keeling JW, et al. The Scottish perinatal neuropathology study: clinicopathological correlation in early neonatal deaths. Arch Dis Child Fetal Neonatal Ed 2004; 89: F399-F407. (Pubitemid 39178815)
44. Leech RW, Alvord EC Jr,. Anoxic-ischemic encephalopathy in the human neonatal period. The significance of brain stem involvement. Arch Neurol 1977; 34: 109-113. (Pubitemid 8024972)
45. Eken P, Jansen GH, Groenendaal F, et al. Intracranial lesions in the fullterm infant with hypoxic ischaemic encephalopathy: ultrasound and autopsy correlation. Neuropediatrics 1995; 25: 301-307.
46. Leech RW, Brumback RA,. Massive brain stem necrosis in the human neonate: presentation of three cases with review of the literature. J Child Neurol 1988; 3: 258-262. (Pubitemid 18267369)
47. Roelants-Van Rijn AM, Nikkels PGJ, Groenendaal F, et al. Neonatal diffusion-weighted MR imaging: relation with histopathology or follow-up MR examination. Neuropediatrics 2001; 32: 286-294. (Pubitemid 34165672)
48. Gilles FH,. Hypotensive brain stem necrosis. Selective symmetrical necrosis of tegmental neuronal aggregates following cardiac arrest. Arch Pathol 1969; 88: 32-41.
49. Janzer RC, Friede RL,. Hypotensive brain stem necrosis or cardiac arrest encephalopathy? Acta Neuropathol 1980; 50: 53-56. (Pubitemid 10148213)
50. Volpe JJ, Kinney HC, Jensen FE, Rosenberg PA,. The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int J Dev Neurosci 2011; 29: 423-440.
51. Haynes RL, Folkerth RD, Keefe R, et al. Nitrosative and oxidative injury to premyelinating oligodendrocytes is accompanied by microglial activation in periventricular leukomalacia in the human premature infant. J Neuropathol Exp Neurol 2003; 62: 441-450. (Pubitemid 36560186)
52. Back SA, Luo NL, Borenstein NS, et al. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 2001; 21: 1302-1312. (Pubitemid 32128775)
53. Buser JR, Maire J, Riddle A, et al. Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann Neurol 2012; 71: 93-109.
54. Edwards AD, Mehmet H,. Apoptosis in perinatal hypoxic-ischaemic cerebral damage. Neuropathol Appl Neurobiol 1996; 22: 482-503.
55. Barkovich AJ, Westmark K, Partridge C, et al. Perinatal asphyxia: MR findings in the first 10 days. AJNR Am J Neuroradiol 1995; 16: 427-438.
56. Kaufman SA, Miller SP, Ferriero DM, et al. Encephalopathy as a predictor of magnetic resonance imaging abnormalities in asphyxiated newborns. Pediatr Neurol 2003; 28: 342-346. (Pubitemid 36876132)
57. Rutherford M, Counsell S, Allsop J, et al. Diffusion-weighted magnetic resonance imaging in term perinatal brain injury: a comparison with site of lesion and time from birth. Pediatrics 2004; 114: 1004-1014. (Pubitemid 41529766)
58. Miller SP, Ramaswamy V, Michelson D, et al. Patterns of brain injury in term neonatal encephalopathy. J Pediatr 2005; 146: 453-460. (Pubitemid 40469706)
59. Okereafor A, Allsop J, Counsell SJ, et al. Patterns of brain injury in neonates exposed to perinatal sentinel events. Pediatrics 2008; 101: 906-914.
60. Li AM, Chau V, Poskitt KJ, et al. White matter injury in term newborns with neonatal encephalopathy. Pediatr Res 2009; 65: 85-89.
61. Chau V, Poskitt KJ, Sargent MA, et al. Comparison of computer tomography and magnetic resonance imaging scans on the third day of life in term newborns with neonatal encephalopathy. Pediatrics 2009; 123: 319-326.
62. Steinman KJ, Gorno-Tempini ML, Glidden DV, et al. Neonatal watershed brain injury on magnetic resonance imaging correlates with verbal IQ at 4 years. Pediatrics 2009; 123: 1025-1030.
63. Martinez-Biarge M, Diez-Sebastian J, Kapellou O, et al. Predicting motor outcome and death in term hypoxic-ischemic encephalopathy. Neurology 2011; 76: 2055-2061.
64. Martinez-Biarge M, Diez-Sebastian J, Rutherford MA, Cowan FM,. Outcomes after central grey matter injury in term perinatal hypoxic-ischaemic encephalopathy. Early Hum Dev 2010; 86: 675-682.
65. de Vries LS, Cowan FM,. Evolving understanding of hypoxic-ischemic encephalopathy in the term infant. Semin Pediatr Neurol 2009; 16: 216-225.
66. American College of Obstetricians and Gynecologists and American Academy of Pediatrics. Neonatal encephalopathy and cerebral palsy: defining the pathogenesis and pathophysiology. Washington, DC: American College of Obstetricians and Gynecologists and American Academy of Pediatrics, 2003.
67. Schifrin BS,. The CTG and the timing and mechanism of fetal neurological injuries. Best Pract Res Clin Obstet Gynaecol 2004; 18: 437-456. (Pubitemid 38950050)
68. Schifrin BS, Ater S,. Fetal hypoxic and ischemic injuries. Curr Opin Obstet Gynecol 2006; 18: 112-122.
69. Marin-Padilla M,. The human brain: prenatal development and structure. Berlin, Germany: Springer-Verlag, 2011.
70. Logitharajah P, Rutherford MA, Cowan FM,. hypoxic-ischemic encephalopathy in preterm infants: antecedent factors, brain imaging, and outcome. Pediatr Res 2009; 66: 222-229.
71. Rutherford MA, Pennock JM, Counsell SJ, et al. Abnormal magnetic resonance signal in the internal capsule predicts poor neurodevelopmental outcome in infants with hypoxic-ischemic encephalopathy. Pediatrics 1998; 102: 323-328. (Pubitemid 28354996)
72. Hunt RW, Neil JJ, Coleman LT, et al. Apparent diffusion coefficient in the posterior limb of the internal capsule predicts outcome after perinatal asphyxia. Pediatrics 2004; 114: 999-1003. (Pubitemid 41529765)
73. Alderliesten T, de Vries LS, Benders MJ, et al. MR imaging and outcome of term neonates with perinatal asphyxia: value of diffusion-weighted MR imaging and (1)H MR spectroscopy. Radiology 2011; 261: 235-242.
74. Vermeulen RJ, van Schie PE, Hendrikx L, et al. Diffusion-weighted and conventional MR imaging in neonatal hypoxic ischemia: two-year follow-up study. Radiology 2008; 249: 631-639.
75. Rutherford M, Malamateniou C, McGuinness A, et al. Magnetic resonance imaging in hypoxic-ischaemic encephalopathy. Early Hum Dev 2010; 86: 351-360.
76. Gonzalez FF, Miller SP,. Does perinatal asphyxia impair cognitive function without cerebral palsy? Arch Dis Child Fetal Neonatal Ed 2006; 91: F454-F459. (Pubitemid 44701860)
77. Al-Macki N, Miller SP, Hall N, Shevell M,. The spectrum of abnormal neurologic outcomes subsequent to term intrapartum asphyxia. Pediatr Neurol 2009; 41: 399-405.
78. Pasternak JF, Gorey MT,. The syndrome of acute near-total intrauterine asphyxia in the term infant. Pediatr Neurol 1998; 18: 391-398. (Pubitemid 28308704)
79. Roland EH, Poskitt K, Rodriguez E, et al. Perinatal hypoxic-ischemic thalamic injury: clinical features and neuroimaging. Ann Neurol 1998; 44: 161-166. (Pubitemid 28374103)
80. Korst LM, Phelan JP, Wang YM, et al. Acute fetal asphyxia and permanent brain injury: a retrospective analysis of current indicators. J Matern Fetal Med 1999; 8: 101-106. (Pubitemid 29218466)
81. Martinez-Biarge M, Madero R, Gonzalez A, et al. Perinatal morbidity and risk of hypoxic-ischemic encephalopathy associated with intrapartum sentinel events. Am J Obstet Gynecol 2012; 206: 148.e1-7.
82. Kinney HC, Panigrahy A, Newburger JW, et al. Hypoxic-ischemic brain injury in infants with congenital heart disease dying after cardiac surgery. Acta Neuropathol 2005; 110: 563-578. (Pubitemid 41763986)
83. Barkovich AJ, Raybaud C,. Pediatric neuroimaging. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins, 2012.
84. McKinstry RC, Miller JH, Snyder AZ, et al. A prospective, longitudinal diffusion tensor imaging study of brain injury in newborns. Neurology 2002; 59: 824-833.
85. Soul JS, Robertson RL, Tzika AA, et al. Time course of changes in diffusion-weighted magnetic resonance imaging in a case of neonatal encephalopathy with defined onset and duration of hypoxic-ischemic insult. Pediatrics 2001; 108: 1211-1214. (Pubitemid 33021200)
86. Barkovich AJ, Miller SP, Bartha A, et al. MR imaging, MR spectroscopy, and diffusion tensor imaging of sequential studies in neonates with encephalopathy. AJNR Am J Neuroradiol 2006; 27: 533-547. (Pubitemid 44897772)
87. Barkovich AJ, Westmark KD, Bedi HS, et al. Proton spectroscopy and diffusion imaging on the first day of life after perinatal asphyxia: preliminary report. AJNR Am J Neuroradiol 2001; 22: 1786-1794. (Pubitemid 32999596)
88. Hanrahan JD, Cox IJ, Edwards AD, et al. Persistent increases in cerebral lactate concentration after birth asphyxia. Pediatr Res 1998; 44: 304-311. (Pubitemid 28389983)
89. Amess PN, Penrice J, Wylezinska M, et al. Early brain proton magnetic resonance spectroscopy and neonatal neurology related to neurodevelopmental outcome at 1 year in term infants after presumed hypoxic-ischaemic brain injury. Dev Med Child Neurol 1999; 41: 436-445. (Pubitemid 29322483)
90. Miller SP, Weiss J, Barnwell A, et al. Seizure-associated brain injury in term newborns with perinatal asphyxia. Neurology 2002; 58: 542-548. (Pubitemid 34164934)
91. Thayyil S, Chandrasekaran M, Taylor A, et al. Cerebral magnetic resonance biomarkers in neonatal encephalopathy: a meta-analysis. Pediatrics 2010; 125: e382-e395.
92. Roth SC, Edwards AD, Cady EB, et al. Relation between cerebral oxidative metabolism following birth asphyxia, and neurodevelopmental outcome and brain growth at one year. Dev Med Child Neurol 1992; 34: 285-295.
93. Azzopardi D, Wyatt JS, Cady EB, et al. Prognosis of newborn infants with hypoxic-ischemic brain injury assessed by phosphorus magnetic resonance spectroscopy. Pediatr Res 1989; 25: 445-451. (Pubitemid 19128271)
94. Martin E, Buchli R, Ritter S, et al. Diagnostic and prognostic value of cerebral 31P magnetic resonance spectroscopy in neonates with perinatal asphyxia. Pediatr Res 1996; 40: 749-758. (Pubitemid 26376570)
95. Rosen MG, Scibetta J, Chik L, Borgstedt AD,. An approach to the study of brain damage. The principles of fetal electroencephalography. Am J Obstet Gynecol 1973; 115: 37-47.
96. Chik L, Sokol RJ, Rosen MG, Borgstedt AD,. Computer interpreted fetal electroencephalogram. II. Patterns in infants who were neurologically abnormal at 1 year of age. Am J Obstet Gynecol 1976; 125: 541-544.
97. Chik L, Sokol RJ, Rosen MG, et al. Computer interpreted fetal monitoring data. Discriminant analysis or perinatal data as a model for prediction of neurologic status at one year of age. J Pediatr 1977; 90: 985-989.
98. Sokol RJ, Rosen MG, Chik L,. Fetal electroencephalographic monitoring related to infant outcome. Am J Obstet Gynecol 1977; 127: 329-330.
99. Maynard DE, Cohen RJ, Viniker DA,. Intrapartum fetal monitoring with the cerebral function monitor. Br J Obstet Gynaecol 1979; 86: 941-947. (Pubitemid 10209342)
100. Weller C, Dyson RJ, McFadyen IR,. Fetal electroencephalography using a new, flexible electrode. Am J Obstet Gynceol 1981; 88: 983.
101. Thaler I, Boldes R, Timor-Tritsch I,. Real-time spectral analysis of the fetal EEG: a new approach to monitoring sleep states and fetal condition during labor. Pediatr Res 2000; 48: 340-345. (Pubitemid 30637334)
102. Peebles DM, Edwards AD, Wyatt JS, et al. Changes in human fetal cerebral hemoglobin concentration and oxygenation during labor measured by near-infrared spectroscopy. Am J Obstet Gynecol 1992; 166: 1369-1373.
103. Peebles DM, Spencer JA, Edwards AD, et al. Relation between frequency of uterine contractions and human fetal cerebral oxygen saturation studied during labour by near infrared spectroscopy. Br J Obstet Gynaecol 1994; 101: 44-48. (Pubitemid 24204773)
104. Aldrich CJ, Wyatt JS, Spencer JAD, et al. The effect of maternal oxygen administration on human fetal cerebral oxygenation measured during labour by near infrared spectroscopy. Br J Obstet Gynaecol 1994; 101: 509-513. (Pubitemid 24210153)
105. Aldrich CJ, D'Antona D, Spencer JAD, et al. The effect of maternal posture on fetal cerebral oxygenation during labour. Br J Obstet Gynaecol 1995; 102: 14-19.
106. Aldrich CJ, Dantona D, Spencer J, et al. Late fetal heart decelerations and changes in cerebral oxygenation during the first stage of labour. Br J Obstet Gynaecol 1995; 102: 9-13.
107. Salhab WA, Wyckoff MH, Laptook AR, Perlman JM,. Initial hypoglycemia and neonatal brain injury in term infants with severe fetal acidemia. Pediatrics 2004; 114: 361-366. (Pubitemid 39006662)
108. Basu P, Som S, Choudhuri N, Das H,. Contribution of the blood glucose level in perinatal asphyxia. Eur J Pediatr 2009; 168: 833-838.
109. Nadeem M, Murray DM, Boylan GB, et al. Early blood glucose profile and neurodevelopmental outcome at two years in neonatal hypoxic-ischaemic encephalopathy. BMC Pediatr 2011; 11: 10.
110. Girard S, Kadhim H, Roy M, et al. Role of perinatal inflammation in cerebral palsy. Pediatr Neurol 2009; 40: 168-174.
111. Mallard C, Wang X,. Infection-induced vulnerability of perinatal brain injury. Neurol Res Int 2012: 1-6.
112. Brochu ME, Girard S, Lavoie K, Sebire G,. Developmental regulation of the neuroinflammatory responses to LPS and/or hypoxia-ischemia between preterm and term neonates: an experimental study. J Neuroinflammation 2011; 8: 55.
113. Nelson KB, Grether JK,. Potentially asphyxiating conditions and spastic cerebral palsy in infants of normal birth weight. Am J Obstet Gynecol 1998; 179: 507-513. (Pubitemid 28413392)
114. Wang X, Rousset CI, Hagberg H, Mallard C,. Lipopolysaccharide-induced inflammation and perinatal brain injury. Semin Fetal Neonatal Med 2006; 11: 343-353. (Pubitemid 44038704)
115. Eklind S, Mallard C, Leverin A-L, et al. Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 2001; 13: 1101-1106. (Pubitemid 32275747)
116. Yang L, Sameshima H, Ikeda T, Ikenoue T,. Lipopolysaccharide administration enhances hypoxic-ischemic brain damage in newborn rats. J Obstet Gynaecol Res 2004; 30: 142-147. (Pubitemid 38508630)
117. Yang L, Sameshima H, Yamaguchi M, Ikenoue T,. Expression of inducible nitric oxide synthase and cyclooxygenase-2 mRNA in brain damage induced by lipopolysaccharide and intermittent hypoxia-ischemia in neonatal rats. J Obstet Gynaecol Res 2005; 31: 185-191. (Pubitemid 40563044)
118. Nijboer CH, Groenendaal F, Kavelaars A, et al. Gender-specific neuroprotection by 2-iminobiotin after hypoxia-ischemia in the neonatal rat via a nitric oxide independent pathway. J Cereb Blood Flow Metab 2007; 27: 282-292. (Pubitemid 46148455)
119. Harish G, Venkateshappa C, Mahadevan A, et al. Glutathione metabolism is modulated by postmortem interval, gender difference and agonal state in postmortem human brains. Neurochem Int 2011; 59: 1029-1042.
120. Wu YW, Croen LA, Vanderwerf A, et al. Candidate genes and risk for CP: a population-based study. Pediatr Res 2011; 70: 642-646.
121. Alkayed NJ, Harukuni I, Kimes AS, et al. Gender-linked brain injury in experimental stroke. Stroke 1998; 29: 159-165; discussion 166.
122. Hurn PD, Vannucci SJ, Hagberg H,. Adult or perinatal brain injury: does sex matter? Stroke 2005; 36: 193-195. (Pubitemid 40170780)
123. Du L, Bayir H, Lai Y, et al. Innate gender-based proclivity in response to cytotoxicity and programmed cell death pathway. J Biol Chem 2004; 279: 38563-38570. (Pubitemid 39296010)
124. Zhu C, Xu F, Wang X, et al. Different apoptotic mechanisms are activated in male and female brains after neonatal hypoxia-ischaemia. J Neurochem 2006; 96: 1016-1027.
125. Goldsmith JP,. Programs offer alternative to malpractice suits when newborns suffer neurologic injury. AAP News 2012: 10-11.