Why the term neonatal encephalopathy should be preferred over neonatal hypoxic-ischemic encephalopathy

American Journal of Obstetrics and Gynecology

Volumn 208, Issue 3, 2013, Pages 176-180

  Leviton, Alan ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

asphyxia; central nervous system diseases; diagnosis; diseases; infant; newborn

Indexed keywords

ACIDEMIA; APNEA; ARTICLE; BRAIN DAMAGE; CARDIOTOCOGRAPHY; CEREBRAL PALSY; COMPUTER ASSISTED TOMOGRAPHY; DELIVERY; FETUS MONITORING; GENE MUTATION; HEALTH CARE COST; HEALTH INSURANCE; HUMAN; HYPERCAPNIA; HYPOVENTILATION; HYPOXEMIA; HYPOXIC ISCHEMIC ENCEPHALOPATHY; INTRAUTERINE GROWTH RETARDATION; LABOR; MALPRACTICE; MEDICAL TERMINOLOGY; METABOLIC DISORDER; NEWBORN; NEWBORN ENCEPHALOPATHY; NEWBORN HYPOXIA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPIC VARIATION; PRADER WILLI SYNDROME; PRIORITY JOURNAL;

ASPHYXIA NEONATORUM; CENTRAL NERVOUS SYSTEM DISEASES; FEMALE; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; INFANT, NEWBORN; INTELLECTUAL DISABILITY; MALE; PREGNANCY; SEVERITY OF ILLNESS INDEX; SPASMS, INFANTILE; TERMINOLOGY AS TOPIC;

EID: 84874788214     PISSN: 00029378     EISSN: 10976868     Source Type: Journal    
DOI: 10.1016/j.ajog.2012.07.020     Document Type: Article

References (110)

1. K.B. Nelson, A. Leviton How much of neonatal encephalopathy is due to birth asphyxia? Am J Dis Child 145 1991 1325 1331
2. O. Dammann, D. Ferriero, P. Gressens Neonatal encephalopathy or hypoxic-ischemic encephalopathy? Appropriate terminology matters Pediatr Res 70 2011 1 2
3. J.J. Volpe Neonatal encephalopathy - an inadequate term for hypoxic-ischemic encephalopathy Ann Neurol 72 2012 156 166
4. L. Bennet, L. Booth, A.J. Gunn Potential biomarkers for hypoxic-ischemic encephalopathy Semin Fetal Neonatal Med 15 2010 253 260
5. J.L. Wayenberg Threshold of metabolic acidosis associated with neonatal encephalopathy in the term newborn J Matern Fetal Neonatal Med 18 2005 381 385
6. E.J. Quilligan, R.H. Paul Fetal monitoring: is it worth it? Obstet Gynecol 45 1975 96 100
7. M.G. Ross Labor and fetal heart rate decelerations: relation to fetal metabolic acidosis Clin Obstet Gynecol 54 2011 74 82
8. B.S. Schifrin, S. Ater Fetal hypoxic and ischemic injuries Curr Opin Obstet Gynecol 18 2006 112 122
9. J.D. Larma, A.M. Silva, C.J. Holcroft, R.E. Thompson, P.K. Donohue, E.M. Graham Intrapartum electronic fetal heart rate monitoring and the identification of metabolic acidosis and hypoxic-ischemic encephalopathy Am J Obstet Gynecol 197 2007 301.e1 301.e8
10. J.P. Neilson Fetal electrocardiogram (ECG) for fetal monitoring during labour Cochrane Database Syst Rev 4 2012 CD000116
11. S. Potti, V. Berghella ST waveform analysis versus cardiotocography alone for intrapartum fetal monitoring: a meta-analysis of randomized trials Am J Perinatol 29 2012 657 664
12. J.H. Becker, L. Bax, I. Amer-Wahlin ST analysis of the fetal electrocardiogram in intrapartum fetal monitoring: a meta-analysis Obstet Gynecol 119 2012 145 154
13. C.E. East, L.R. Leader, P. Sheehan, N.E. Henshall, P.B. Colditz Intrapartum fetal scalp lactate sampling for fetal assessment in the presence of a non-reassuring fetal heart rate trace Cochrane Database Syst Rev 2010 CD006174
14. A. Locatelli, M. Incerti, A. Ghidini, M. Greco, E. Villa, G. Paterlini Factors associated with umbilical artery acidemia in term infants with low Apgar scores at 5 min Eur J Obstet Gynecol Reprod Biol 139 2008 146 150
15. M. Susser What is a cause and how do we know one? A grammar for pragmatic epidemiology Am J Epidemiol 133 1991 635 648
16. M. Parascandola, D.L. Weed Causation in epidemiology J Epidemiol Community Health 55 2001 905 912
17. R. Campaner Mechanistic causality and counterfactual-manipulative causality: recent insights from philosophy of science J Epidemiol Community Health 65 2011 1070 1074
18. K. Hoffmann, C. Heidemann, C. Weikert, M.B. Schulze, H. Boeing Estimating the proportion of disease due to classes of sufficient causes Am J Epidemiol 163 2006 76 83
19. A. Leviton Single-cause attribution Dev Med Child Neurol 29 1987 805 807
20. G. Bunin What causes childhood brain tumors? Limited knowledge, many clues Pediatr Neurosurg 32 2000 321 326
21. R.L. Brown Epidemiology of injury and the impact of health disparities Curr Opin Pediatr 22 2010 321 325
22. D. Cederberg, P. Siesjo What has inflammation to do with traumatic brain injury? Childs Nerv Syst 26 2010 221 226
23. C. Thornton, C.I. Rousset, A. Kichev Molecular mechanisms of neonatal brain injury Neurol Res Int 2012 2012 506320
24. C. Limperopoulos, C.B. Benson, H. Bassan Cerebellar hemorrhage in the preterm infant: ultrasonographic findings and risk factors Pediatrics 116 2005 717 724
25. E. Mayr Cause and effect in biology Science 134 1961 1501 1506
26. K.N. Laland, K. Sterelny, J. Odling-Smee, W. Hoppitt, T. Uller Cause and effect in biology revisited: is Mayr's proximate-ultimate dichotomy still useful? Science 334 2011 1512 1516
27. O. Dammann, A. Leviton Perinatal brain damage causation Dev Neurosci 29 2007 280 288
28. K.J. Rothman Causes Am J Epidemiol 104 1976 587 592
29. A. Morabia On the origin of Hill's causal criteria Epidemiology 2 1991 367 369
30. D.L. Weed Epidemiologic evidence and causal inference Hematol Oncol Clin North Am 14 2000 797 807 viii
31. A.C. Ward The role of causal criteria in causal inferences: Bradford Hill's "aspects of association" Epidemiol Perspect Innov 6 2009 2
32. American College of Obstetricians and Gynecologists Fetal and neonatal neurologic injury 1992 American College of Obstetricians and Gynecologists Washington, DC
33. A. MacLennan A template for defining a causal relation between acute intrapartum events and cerebral palsy: international consensus statement BMJ 319 1999 1054 1059
34. American College of Obstetricians and Gynecologists Task Force on Neonatal Encephalopathy and Cerebral Palsy; American Academy of Pediatrics Neonatal encephalopathy and cerebral palsy: defining the pathogenesis and pathophysiology 2003 Washington, DC
35. L.M. Korst, J.P. Phelan, Y.M. Wang, G.I. Martin, M.O. Ahn Acute fetal asphyxia and permanent brain injury: a retrospective analysis of current indicators J Matern Fetal Med 8 1999 101 106
36. E.M. Strijbis, I. Oudman, P. van Essen, A.H. MacLennan Cerebral palsy and the application of the international criteria for acute intrapartum hypoxia Obstet Gynecol 107 2006 1357 1365
37. American College of Obstetricians and Gynecologists Practice bulletin no. 116: Management of intrapartum fetal heart rate tracings Obstet Gynecol 116 2010 1232 1240
38. R.K. Freeman, M.P. Nageotte Comments on American College of Obstetricians and Gynecologists Practice Bulletin no. 106 Am J Obstet Gynecol 202 2010 411 412
39. C. Elliott, P.A. Warrick, E. Graham, E.F. Hamilton Graded classification of fetal heart rate tracings: association with neonatal metabolic acidosis and neurologic morbidity Am J Obstet Gynecol 202 2010 258.e1 258.e8
40. A. Leviton, K.B. Nelson Problems with definitions and classifications of newborn encephalopathy Pediatr Neurol 8 1992 85 90
41. R.D. Higgins, T. Raju, A.D. Edwards Hypothermia and other treatment options for neonatal encephalopathy: an executive summary of the Eunice Kennedy Shriver NICHD workshop J Pediatr 159 2011 851 858.e1
42. D.J. Ashley The two "hit" and multiple "hit" theories of carcinogenesis Br J Cancer 23 1969 313 328
43. A.G. Knudson Jr Mutation and cancer: statistical study of retinoblastoma Proc Natl Acad Sci U S A 68 1971 820 823
44. R.K. Freeman Medical and legal implications for necessary requirements to diagnose damaging hypoxic-ischemic encephalopathy leading to later cerebral palsy Am J Obstet Gynecol 199 2008 585 586
45. S. Eklind, C. Mallard, A.L. Leverin Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury Eur J Neurosci 13 2001 1101 1106
46. S. Eklind, C. Mallard, P. Arvidsson, H. Hagberg Lipopolysaccharide induces both a primary and a secondary phase of sensitization in the developing rat brain Pediatr Res 58 2005 112 116
47. Y. Kim, R. Busto, W.D. Dietrich, S. Kraydieh, M.D. Ginsberg Delayed postischemic hyperthermia in awake rats worsens the histopathological outcome of transient focal cerebral ischemia Stroke 27 1996 2274 2280 discussion 81
48. U. Aden, G. Favrais, F. Plaisant Systemic inflammation sensitizes the neonatal brain to excitotoxicity through a pro-/anti-inflammatory imbalance: key role of TNFalpha pathway and protection by etanercept Brain Behav Immun 24 2010 747 758
49. X. Wang, L. Stridh, W. Li Lipopolysaccharide sensitizes neonatal hypoxic-ischemic brain injury in a MyD88-dependent manner J Immunol 183 2009 7471 7477
50. T. Markus, T. Cronberg, C. Cilio, C. Pronk, T. Wieloch, D. Ley Tumor necrosis factor receptor-1 is essential for LPS-induced sensitization and tolerance to oxygen-glucose deprivation in murine neonatal organotypic hippocampal slices J Cereb Blood Flow Metab 29 2009 73 86
51. B.W. McColl, S.M. Allan, N.J. Rothwell Systemic infection, inflammation and acute ischemic stroke Neuroscience 158 2009 1049 1061
52. G.S. Kendall, M. Hirstova, S. Horn TNF gene cluster deletion abolishes lipopolysaccharide-mediated sensitization of the neonatal brain to hypoxic ischemic insult Lab Invest 91 2011 328 341
53. T. Tomimatsu, H. Fukuda, T. Kanagawa, J. Mu, T. Kanzaki, Y. Murata Effects of hyperthermia on hypoxic-ischemic brain damage in the immature rat: its influence on caspase-3-like protease Am J Obstet Gynecol 188 2003 768 773
54. L.W. Impey, C.E. Greenwood, R.S. Black, P.S. Yeh, O. Sheil, P. Doyle The relationship between intrapartum maternal fever and neonatal acidosis as risk factors for neonatal encephalopathy Am J Obstet Gynecol 198 2008 49.e1 49.e6
55. S.J. Adamson, L.M. Alessandri, N. Badawi, P.R. Burton, P.J. Pemberton, F. Stanley Predictors of neonatal encephalopathy in full-term infants BMJ 311 1995 598 602
56. N. Badawi, J.J. Kurinczuk, J.M. Keogh Intrapartum risk factors for newborn encephalopathy: the Western Australian case-control study BMJ 317 1998 1554 1558
57. O. Dammann, M.J. Brinkhaus, D.B. Bartels Immaturity, perinatal inflammation, and retinopathy of prematurity: a multi-hit hypothesis Early Hum Dev 85 2009 325 329
58. A. Leviton, K. Kuban, E.N. Allred, R. Fichorova, T.M. O'Shea, N. Paneth Elevated concentrations of circulating indicators of inflammation in infants born before the 28th post-menstrual week predict a small head circumference two years later Early Hum Dev 87 2011 325 330
59. A. Leviton, K. Kuban, T.M. O'Shea The relationship between early concentrations of 25 blood proteins and cerebral white matter injury in preterm newborns: the ELGAN study J Pediatr 158 2011 897 903.e5
60. T.M. O'Shea, E.N. Allred, K. Kuban Elevated concentrations of inflammation-related proteins in postnatal blood predict severe developmental delay at two years in extremely premature infants J Pediatr 160 2012 395 401.e4
61. S.D. Bilbo, J.C. Biedenkapp, A. Der-Avakian, L.R. Watkins, J.W. Rudy, S.F. Maier Neonatal infection-induced memory impairment after lipopolysaccharide in adulthood is prevented via caspase-1 inhibition J Neurosci 25 2005 8000 8009
62. A.M. Kaindl, G. Favrais, P. Gressens Molecular mechanisms involved in injury to the preterm brain J Child Neurol 24 2009 1112 1118
63. A.A. Kroon, J. Wang, Z. Huang, L. Cao, M. Kuliszewski, M. Post Inflammatory response to oxygen and endotoxin in newborn rat lung ventilated with low tidal volume Pediatr Res 68 2010 63 69
64. M.A. Orman, M.G. Ierapetritou, F. Berthiaume, I.P. Androulakis The dynamics of the early inflammatory response in double-hit burn and sepsis animal models Cytokine 56 2011 494 502
65. L.L. Williamson, P.W. Sholar, R.S. Mistry, S.H. Smith, S.D. Bilbo Microglia and memory: modulation by early-life infection J Neurosci 31 2011 15511 15521
66. K.B. Nelson, T. Chang Is cerebral palsy preventable? Curr Opin Neurol 21 2008 129 135
67. K.B. Nelson Causative factors in cerebral palsy Clin Obstet Gynecol 51 2008 749 762
68. N.N. Finer, C.M. Robertson, R.T. Richards, L.E. Pinnell, K.L. Peters Hypoxic-ischemic encephalopathy in term neonates: perinatal factors and outcome J Pediatr 98 1981 112 117
69. M.L. Levene, J. Kornberg, T.H. Williams The incidence and severity of post-asphyxial encephalopathy in full-term infants Early Hum Dev 11 1985 21 26
70. A.I. Airede Birth asphyxia and hypoxic-ischaemic encephalopathy: incidence and severity Ann Trop Paediatr 11 1991 331 335
71. N. Badawi, J.J. Kurinczuk, J.M. Keogh Antepartum risk factors for newborn encephalopathy: the Western Australian case-control study BMJ 317 1998 1549 1553
72. A.T. Berg Indices of fetal growth-retardation, perinatal hypoxia-related factors and childhood neurological morbidity Early Hum Dev 19 1989 271 283
73. M. Ellis, N. Manandhar, D.S. Manandhar, A.M. Costello Risk factors for neonatal encephalopathy in Kathmandu, Nepal, a developing country: unmatched case-control study BMJ 320 2000 1229 1236
74. P. Wintermark, T. Boyd, M.C. Gregas, M. Labrecque, A. Hansen Placental pathology in asphyxiated newborns meeting the criteria for therapeutic hypothermia Am J Obstet Gynecol 203 2010 579.e1 579.e9
75. R.H. Wharton, M.J. Bresnan Neonatal respiratory depression and delay in diagnosis in Prader-Willi syndrome Dev Med Child Neurol 31 1989 231 236
76. E. Nsegbe, A. Wallen-Mackenzie, S. Dauger Congenital hypoventilation and impaired hypoxic response in Nurr1 mutant mice J Physiol 556 2004 43 59
77. J. Berner, Y. Shvarev, H. Lagercrantz, A. Bilkei-Gorzo, T. Hokfelt, R. Wickstrom Altered respiratory pattern and hypoxic response in transgenic newborn mice lacking the tachykinin-1 gene J Appl Physiol 103 2007 552 559
78. N.D. Tomycz, R.L. Haynes, E.F. Schmidt, K. Ackerson, H.C. Kinney Novel neuropathologic findings in the Haddad syndrome Acta Neuropathol 119 2010 261 269
79. T. Armangue, A. Macaya, E. Vazquez, M.J. Jurado, M. Roig-Quilis Central hypoventilation and brainstem dysgenesis Pediatr Neurol 46 2012 257 259
80. L.J. Jennings, M. Yu, C.M. Rand Variable human phenotype associated with novel deletions of the PHOX2B gene Pediatr Pulmonol 47 2012 153 161
81. B. Schule, D.D. Armstrong, H. Vogel, A. Oviedo, U. Francke Severe congenital encephalopathy caused by MECP2 null mutations in males: central hypoxia and reduced neuronal dendritic structure Clin Genet 74 2008 116 126
82. E.M. Graham, K.A. Ruis, A.L. Hartman, F.J. Northington, H.E. Fox A systematic review of the role of intrapartum hypoxia-ischemia in the causation of neonatal encephalopathy Am J Obstet Gynecol 199 2008 587 595
83. L. Shalak, S. Johnson-Welch, J.M. Perlman Chorioamnionitis and neonatal encephalopathy in term infants with fetal acidemia: histopathologic correlations Pediatr Neurol 33 2005 162 165
84. R. Depp Perinatal asphyxia: assessing its causal role and timing Semin Pediatr Neurol 2 1995 3 36
85. R.L. Naeye, A.R. Localio Determining the time before birth when ischemia and hypoxemia initiated cerebral palsy Obstet Gynecol 86 1995 713 719
86. E.S. Draper, J.J. Kurinczuk, C.R. Lamming, M. Clarke, D. James, D. Field A confidential enquiry into cases of neonatal encephalopathy Arch Dis Child Fetal Neonatal Ed 87 2002 F176 F180
87. F. Cowan, M. Rutherford, F. Groenendaal Origin and timing of brain lesions in term infants with neonatal encephalopathy Lancet 361 2003 736 742
88. J.C. Becher, J.E. Bell, J.W. Keeling, N. McIntosh, B. Wyatt The Scottish perinatal neuropathology study: clinicopathological correlation in early neonatal deaths Arch Dis Child Fetal Neonatal Ed 89 2004 F399 F407
89. C.S. Ennen, T.A. Huisman, W.J. Savage Glial fibrillary acidic protein as a biomarker for neonatal hypoxic-ischemic encephalopathy treated with whole-body cooling Am J Obstet Gynecol 205 2011 251.e1 251.e7
90. V.J. Lynch Use with caution: developmental systems divergence and potential pitfalls of animal models Yale J Biol Med 82 2009 53 66
91. H.B. van der Worp, D.W. Howells, E.S. Sena Can animal models of disease reliably inform human studies? PLoS Med 7 2010 e1000245
92. A. Regenberg, D.J. Mathews, D.M. Blass The role of animal models in evaluating reasonable safety and efficacy for human trials of cell-based interventions for neurologic conditions J Cereb Blood Flow Metab 29 2009 1 9
93. J.M. Perlman Intrapartum hypoxic-ischemic cerebral injury and subsequent cerebral palsy: medicolegal issues Pediatrics 99 1997 851 859
94. F.H. Gilles, I.G. Gomez Developmental neuropathology of the second half of gestation Early Hum Dev 81 2005 245 253
95. M.M. Shroff, J.P. Soares-Fernandes, H. Whyte, C. Raybaud MR imaging for diagnostic evaluation of encephalopathy in the newborn Radiographics 30 2010 763 780
96. A. Okereafor, J. Allsop, S.J. Counsell Patterns of brain injury in neonates exposed to perinatal sentinel events Pediatrics 121 2008 906 914
97. K.A. Ruis, C.U. Lehmann, F.J. Northington, D.D. Lin, E.M. Graham Neonatal brain imaging and the identification of metabolic acidemia and hypoxic-ischemic encephalopathy J Matern Fetal Neonatal Med 22 2009 823 828
98. N. Ankrum Readings 2008 Austin Chronicle Austin, TX
99. S.A. Gyekye Occupational safety management: the role of causal attribution Int J Psychol 45 2010 405 416
100. A. Tversky, D. Kahneman Availability: a heuristic for judging frequency and probability Cogn Psychol 5 1973 207 232
101. B.A. Spellman, A. Kincannon, S. Stose The relation between counterfactual and causal reasoning D.R. Mandel, D.J. Hilton, P. Catellani, The psychology of counterfactual thinking 2005 Routledge London
102. O. Wegwarth, W. Gaissmaier, G. Gigerenzer Smart strategies for doctors and doctors-in-training: heuristics in medicine Med Educ 43 2009 721 728
103. T. Gerstenberg, D.A. Lagnado Spreading the blame: the allocation of responsibility amongst multiple agents Cognition 115 2010 166 171
104. T. Gerstenberg, D.A. Lagnado When contributions make a difference: explaining order effects in responsibility attribution Psychon Bull Rev 19 2012 729 736
105. A.J. Lee, V.A. Lambermont, J.J. Pillow Fetal responses to lipopolysaccharide-induced chorioamnionitis alter immune and airway responses in 7-week-old sheep Am J Obstet Gynecol 204 2011 364.e17 364.e24
106. A.D. Freeman, J.M. Freeman No-fault cerebral palsy insurance: an alternative to the obstetrical malpractice lottery J Health Polit Policy Law 14 1989 707 718
107. American College of Obstetricians and Gynecologists Committee opinion no. 497: Coping with the stress of medical professional liability litigation Obstet Gynecol 118 2011 389 391
108. Virginia Joint Legislative Audit and Review Committee Review of the Virginia birth-related neurological injury Compensation Program 2002 vol 2012 2002
109. S. Spigel Virginia and Florida child brain injury compensation funds. Report to the Connecticut Office of Legislative Research Sept. 11, 2003 2003-R-0620 2003 (vol 2012)
110. S.L. Clark, M.A. Belfort, S.L. Byrum, J.A. Meyers, J.B. Perlin Improved outcomes, fewer cesarean deliveries, and reduced litigation: results of a new paradigm in patient safety Am J Obstet Gynecol 199 2008 105.e1 105.e7