Bench to bedside strategies for optimizing neuroprotection following perinatal hypoxia-ischaemia in high and low resource settings

Early Human Development

Volumn 83, Issue 12, 2007, Pages 801-811

  Robertson, Nicola J ^a   Iwata, Osuke ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN; PHOSPHORUS;

ARTICLE; BODY TEMPERATURE; BODY WEIGHT; BRAIN CORTEX; BRAIN HYPOXIA; BRAIN ISCHEMIA; BRAIN OXYGEN CONSUMPTION; BRAIN OXYGEN TENSION; BRAIN SIZE; BRAIN TEMPERATURE; CELL SURVIVAL; COMMON CAROTID ARTERY; COOLING; DISEASE DURATION; DISEASE SEVERITY; GRAY MATTER; INDUCED HYPOTHERMIA; NEUROPROTECTION; NEWBORN HYPOXIA; NONHUMAN; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PIGLET; POINT OF CARE TESTING; VALIDATION STUDY;

ADULT; ANIMALS; ANIMALS, NEWBORN; HEALTH CARE RATIONING; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; NEUROPROTECTIVE AGENTS; SWINE;

EID: 35548984428     PISSN: 03783782     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.earlhumdev.2007.09.015     Document Type: Article

References (76)

1. Lawn J.E., et al., for the Lancet Neonatal Survival Steering Team. 4 million neonatal deaths: when? Where? Why?. Lancet 365 (2005) 891-900
2. Marlow N., and Budge H. Prevalence, causes, and outcome at 2 years of age of newborn encephalopathy. Arch Dis Child Fetal Neonatal Ed. 90 3 (2005) 193-194
3. Pierrat V., H.N., Liska A., Thomas D., Subtil D., and Truffert P. Groupe d'Etudes en Epidemiologie Perinatale. Prevalence, causes, and outcome at 2 years of age of newborn encephalopathy: population based study. Arch Dis Child Fetal Neonatal Ed 90 3 (2005) F257-F261
4. Ellis M., Manandhar N., Manandhar D., and Costello A. Risk factors for neonatal encephalopathy in Kathmandu, Nepal, a developing country: unmatched case-control study. BMJ 320 (2000) 1229-1236
5. Shankaran S., L.A., Ehrenkranz R.A., Tyson J.E., McDonald S.A., Donovan E.F., Fanaroff A.A., et al. National Institute of Child Health and Human Development Neonatal Research Network. Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N Engl J Med 353 15 (2005) 1574-1584
6. Gluckman P.D., Wyatt J.S., Azzopardi D., Ballard R., Edwards A.D., Ferriero D.M., et al. Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet 365 (2005) 663-670
7. Eicher D., Wagner C., Katikaneni L., Hulsey T., Bass W., Kaufman D., et al. Moderate hypothermia in neonatal encephalopathy: efficacy outcomes. Pediatr Neurol 32 1 (2005) 11-17
8. Dutta S., Pradeep G., and Narang A. Selective head cooling after neonatal encephalopathy. Lancet 365 9471 (2005) 1619
9. Azzopardi D., and Edwards A. Hypothermia. Semin Fetal Neonatal Med 12 4 (2007) 303-310
10. Edwards A., and Azzopardi D. Therapeutic hypothermia following perinatal asphyxia. Arch Dis Child Fetal Neonatal Ed. 91 2 (2006) F127-F131
11. Azzopardi D., Robertson N., Cowan F., Rutherford M., Rampling M., Edwards A., et al. Pilot study of treatment with whole body hypothermia for neonatal encephalopathy. Pediatrics 106 4 (2000) 684-694
12. Battin M., Penrice J., Gunn T., and Gunn A. Treatment of term infants with head cooling and mild systemic hypothermia (35.0 degrees C and 34.5 degrees C) after perinatal asphyxia. Pediatrics 111 2 (2003) 244-251
13. Eicher D., Wagner C., Katikaneni L., Hulsey T., Bass W., Kaufman D., et al. Moderate hypothermia in neonatal encephalopathy: safety outcomes. Pediatr Neurol 32 1 (2005) 18-24
14. Cheung K., Green R., and Magee K. Systematic review of randomized controlled trials of therapeutic hypothermia as a neuroprotectant in post cardiac arrest patients. CJEM 8 5 (2006) 329-337
15. Lang T., Hartman T., Hintz S., and Colby C. Hypothermia for the treatment of neonatal ischemic encephalopathy: is the genie out of the bottle?. Am J Perinatol 24 1 (2007) 27-31
16. Gunn A., and Gluckman P. Head cooling for neonatal encephalopathy: the state of the art. Clin Obstet Gynecol 50 3 (2007) 636-651
17. Lin Z., Yu H., Lin J., Chen S., Liang Z., and Zhang Z. Mild hypothermia via selective head cooling as neuroprotective therapy in term neonates with perinatal asphyxia: an experience from a single neonatal intensive care unit. J Perinatol 26 3 (2006) 180-184
18. Henderson W., Dhingra V., Chittock D., Fenwick J., and Ronco J. Hypothermia in the management of traumatic brain injury. A systematic review and meta-analysis. Intensive Care Med 29 10 (2003) 1637-1644
19. Couzin J. Medicine. The big chill. Science 317 5839 (2007) 743-745
20. Hayashi S., Takayasu M., Inao S., Yoshida J., and Group N.T.H.S. Balance of risk of therapeutic hypothermia. Acta Neurochir Suppl 95 (2005) 269-272
21. Wyatt J., Gluckman P., Liu P., Azzopardi D., Ballard R., Edwards A., et al. Determinants of outcomes after head cooling for neonatal encephalopathy. Pediatrics 119 5 (2007) 912-921
22. Biggar W., Barker C., Bohn D., and Kent G. Partial recovery of neutrophil functions during prolonged hypothermia in pigs. J Appl Physiol 60 4 (1986) 1186-1189
23. Bohn D., Biggar W., Smith C., Conn A., and Barker G. Influence of hypothermia, barbiturate therapy, and intracranial pressure monitoring on morbidity and mortality after near-drowning. Crit Care Med 14 6 (1986) 529-534
24. Schubert A. Side effects of mild hypothermia. J Neurosurg Anesthesiol 7 2 (1995) 139-147
25. Lorek A., Takei Y., Cady E., Wyatt J., Penrice J., Edwards A., et al. Delayed ("secondary") cerebral energy failure after acute hypoxia-ischemia in the newborn piglet: continuous 48-hour studies by phosphorus magnetic resonance spectroscopy. Pediatr Res 36 (1994) 699-706
26. Thoresen M., Penrice J., Lorek A., Cady E., Wylezinska M., Kirkbride V., et al. Mild hypothermia after severe transient hypoxia-ischemia ameliorates delayed cerebral energy failure in the newborn piglet. Pediatr Res 37 5 (1995) 667-670
27. Azzopardi D., Wyatt J., Cady E., Delpy D., Baudin J., Stewart A., et al. Prognosis of newborn infants with hypoxic-ischemic brain injury assessed by phosphorus magnetic resonance spectroscopy. Pediatr Res 25 5 (1989) 445-451
28. Martin E., Buchli R., Ritter S., Schmid R., Largo R., Boltshauser E., et al. Diagnostic and prognostic value of cerebral 31P magnetic resonance spectroscopy in neonates with perinatal asphyxia. Pediatr Res 40 5 (1996) 749-758
29. Robertson N., Cox I., Cowan F., Counsell S., Azzopardi D., and Edwards A. Cerebral intracellular lactic alkalosis persisting months after neonatal encephalopathy measured by magnetic resonance spectroscopy. Pediatr Res 46 3 (1999) 287-296
30. Robertson N., Cowan F., Cox I., and Edwards A. Brain alkaline intracellular pH after neonatal encephalopathy. Ann Neurol 52 6 (2002) 732-742
31. Northington F., Ferriero D., Graham E., Traystman R., and Martin L. Early neurodegeneration after hypoxia-ischemia in neonatal rat is necrosis while delayed neuronal death is apoptosis. Neurobiol Dis 8 2 (2001) 207-219
32. Taylor D., Edwards A., and Mehmet H. Oxidative metabolism, apoptosis and perinatal brain injury. Brain Pathol 9 1 (1999) 93-117
33. Johnston M., Trescher W., Ishida A., and Nakajima W. Neurobiology of hypoxic-ischemic injury in the developing brain. Pediatr Res 49 6 (2001) 735-741
34. Orrenius S., Zhivotovsky B., and Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol. 4 7 (2003) 552-565
35. Brown G., and Bal-Price A. Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria. Mol Neurobiol 27 3 (2003) 325-355
36. Iwata O., Iwata S., JST, De Vita E., Bainbridge A., Herbertd L., et al. "Therapeutic time window" duration decreases with increasing severity of cerebral hypoxia-ischaemia under normothermia and delayed hypothermia in newborn piglets. Brain Res 1154 (2007) 173-180
37. Cady E., Amess P., Penrice J., Wylezinska M., Sams V., and Wyatt J. Early cerebral-metabolite quantification in perinatal hypoxic-ischaemic encephalopathy by proton and phosphorus magnetic resonance spectroscopy. Magn Reson Imaging 15 5 (1997) 605-611
38. Vannucci R., Towfighi J., and Vannucci S. Secondary energy failure after cerebral hypoxia-ischemia in the immature rat. J Cereb Blood Flow Metab 24 10 (2003) 1090-1097
39. Graulich J., Hoffmann U., Maier R., Ruscher K., Pomper J., Ko H., et al. Acute neuronal injury after hypoxia is influenced by the reoxygenation mode in juvenile hippocampal slice cultures. Brain Res Dev Brain Res 137 1 (2002) 35-42
40. Meng S., Qiao M., Foniok T., and Tuor U. White matter damage precedes that in gray matter despite similar magnetic resonance imaging changes following cerebral hypoxia-ischemia in neonatal rats. Exp Brain Res 166 1 (2005) 56-60
41. Baiden-Amissah K., Joashi U., Blumberg R., Mehmet H., Edwards A., and Cox P. Expression of amyloid precursor protein (beta-APP) in the neonatal brain following hypoxic ischaemic injury. Neuropathol Appl Neurobiol 24 5 (1998) 346-352
42. Puka-Sundvall M., Gajkowska B., Cholewinski M., Blomgren K., Lazarewicz J., and Hagberg H. Subcellular distribution of calcium and ultrastructural changes after cerebral hypoxia-ischemia in immature rats. Brain Res Dev Brain Res 125 1-2 (2000) 31-41
43. Cady E, Bainbridge A, Iwata O, Wyatt J, Robertson N. Very early phosphorus (31P) MRS markers of outcome after transient perinatal cerebral hypoxia-ischaemia. (http://www.pas-meeting.org). 2006;59:3726.5.
44. Agnew D., Koehler R., Guerguerian A., Shaffner D., Traystman R., Martin L., et al. Hypothermia for 24 hours after asphyxic cardiac arrest in piglets provides striatal neuroprotection that is sustained 10 days after rewarming. Pediatr Res 54 2 (2003) 253-262
45. Tooley J., Satas S., Porter H., Silver I., and Thoresen M. Head cooling with mild systemic hypothermia in anesthetized piglets is neuroprotective. Ann Neurol 53 1 (2003) 65-72
46. Gunn A., Gunn T., Gunning M., Williams C., and Gluckman P. Neuroprotection with prolonged head cooling started before postischemic seizures in fetal sheep. Pediatrics 102 5 (1998) 1098-1106
47. Colbourne F., and Corbett D. Delayed and prolonged post-ischemic hypothermia is neuroprotective in the gerbil. Brain Res 654 2 (1994) 265-272
48. Colbourne F., and Corbett D. Delayed postischemic hypothermia: a six month survival study using behavioral and histological assessments of neuroprotection. J Neurosci 15 11 (1995) 7250-7260
49. Gunn A.J.B.L., Gunning M.I., Gluckman P.D., and Gunn T.R. Hypothermia is not neuroprotective when started after postischemic seizures in fetal sheep. Pediatr Res 46 3 (1999) 274-280
50. Thoresen M., Satas S., Løberg E., Whitelaw A., Acolet D., Lindgren C., et al. Twenty-four hours of mild hypothermia in unsedated newborn pigs starting after a severe global hypoxic-ischemic insult is not neuroprotective. Pediatr Res 50 3 (2001) 405-411
51. McCullough J., Zhang N., Reich D., Juvonen T., Klein J., Spielvogel D., et al. Cerebral metabolic suppression during hypothermic circulatory arrest in humans. Ann Thorac Surg 67 6 (1999) 1895-1899
52. Busto R., Globus M., Dietrich W., Martinez E., Valdés I., and Ginsberg M. Effect of mild hypothermia on ischemia-induced release of neurotransmitters and free fatty acids in rat brain. Stroke 20 7 (1989) 904-910
53. Zeevalk G., and Nicklas W. Hypothermia, metabolic stress, and NMDA-mediated excitotoxicity. J Neurochem 61 4 (1993) 1445-1453
54. Kil H., Zhang J., and Piantadosi C. Brain temperature alters hydroxyl radical production during cerebral ischemia/reperfusion in rats. J Cereb Blood Flow Metab 16 1 (1996) 100-106
55. O'Brien F., Iwata O., Thornton J., De Vita E., Sellwood M., Iwata S., et al. Delayed whole-body cooling to 33 or 35 degrees C and the development of impaired energy generation consequential to transient cerebral hypoxia-ischemia in the newborn piglet. Pediatrics 117 5 (2006) 1549-1559
56. Ma D., Hossain M., Chow A., Arshad M., Battson R., Sanders R., et al. Xenon and hypothermia combine to provide neuroprotection from neonatal asphyxia. Ann Neurol 58 2 (2005) 182-193
57. Liu Y., Barks J., Xu G., and Silverstein F. Topiramate extends the therapeutic window for hypothermia-mediated neuroprotection after stroke in neonatal rats. Stroke 35 6 (2004) 1460-1465
58. Beilharz E., Williams C., Dragunow M., Sirimanne E., and Gluckman P. Mechanisms of delayed cell death following hypoxic-ischemic injury in the immature rat: evidence for apoptosis during selective neuronal loss. Brain Res Mol Brain Res 29 1 (1995) 1-14
59. Geddes R., Vannucci R., and Vannucci S. Delayed cerebral atrophy following moderate hypoxia-ischemia in the immature rat. Dev Neurosci 23 3 (2001) 180-185
60. Iwata S., Iwata O., Thornton J., Shanmugalingam S., Bainbridge A., Peebles D., et al. Superficial brain is cooler in small piglets: neonatal hypothermia implications. Ann Neurol 60 5 (2006) 578-585
61. Laptook A., Shalak L., and Corbett R. Differences in brain temperature and cerebral blood flow during selective head versus whole-body cooling. Pediatrics 108 5 (2001) 1103-1110
62. Baena R., Busto R., Dietrich W., Globus M., and Ginsberg M. Hyperthermia delayed by 24 hours aggravates neuronal damage in rat hippocampus following global ischemia. Neurology 48 3 (1997) 768-773
63. Shum-Tim D., Nagashima M., Shinoka T., Bucerius J., Nollert G., Lidov H., et al. Postischemic hyperthermia exacerbates neurologic injury after deep hypothermic circulatory arrest. J Thorac Cardiovasc Surg 116 5 (1998) 780-792
64. Minamisawa H., Smith M., and Siesjö B. The effect of mild hyperthermia and hypothermia on brain damage following 5, 10, and 15 minutes of forebrain ischemia. Ann Neurol 28 1 (1990) 26-33
65. Iwata O., Thornton J., Sellwood M., Iwata S., Sakata Y., Noone M., et al. Depth of delayed cooling alters neuroprotection pattern after hypoxia-ischemia. Ann Neurol 58 1 (2005) 75-87
66. Gupta A., Al-Rawi P., Hutchinson P., and Kirkpatrick P. Effect of hypothermia on brain tissue oxygenation in patients with severe head injury. Br J Anaesth 88 2 (2002) 188-192
67. Cady E., D'Souza P., Penrice J., and Lorek A. The estimation of local brain temperature by in vivo 1H magnetic resonance spectroscopy. Magn Reson Med 33 6 (1995) 862-867
68. Corbett R., Laptook A., and Weatherall P. Noninvasive measurements of human brain temperature using volume-localized proton magnetic resonance spectroscopy. J Cereb Blood Flow Metab 17 4 (1997) 363-369
69. Karaszewski B., Wardlaw J., Marshall I., Cvoro V., Wartolowska K., Haga K., et al. Measurement of brain temperature with magnetic resonance spectroscopy in acute ischemic stroke. Ann Neurol 60 4 (2006) 438-446
70. Childs C., Hiltunen Y., Vidyasagar R., and Kauppinen R. Determination of regional brain temperature using proton magnetic resonance spectroscopy to assess brain-body temperature differences in healthy human subjects. Magn Reson Med 57 1 (2007) 59-66
71. Corbett R., Laptook A., Tollefsbol G., and Kim B. Validation of a noninvasive method to measure brain temperature in vivo using 1H NMR spectroscopy. J Neurochem 64 3 (1995) 1224-1230
72. Corbett R., Purdy P., Laptook A., Chaney C., and Garcia D. Noninvasive measurement of brain temperature after stroke. AJNR Am J Neuroradiol 20 10 (1999) 1851-1857
73. Zarifi M., Astrakas L., Poussaint T., Plessis A.A., Zurakowski D., and Tzika A. Prediction of adverse outcome with cerebral lactate level and apparent diffusion coefficient in infants with perinatal asphyxia. Radiology 225 3 (2002) 859-870
74. Cheong J., Cady E., Penrice J., Wyatt J., Cox I., and Robertson N. Proton MR spectroscopy in neonates with perinatal cerebral hypoxic-ischemic injury: metabolite peak-area ratios, relaxation times, and absolute concentrations. AJNR Am J Neuroradiol 27 7 (2006) 1546-1554
75. Lawn J., Shibuya K., and Stein C. No cry at birth: global estimates of intrapartum stillbirths and intrapartum-related neonatal deaths. Bull World Health Organ 83 6 (2005) 409-417
76. Horn A., Woods D., Thompson C., Eis I., and Kroon M. Selective cerebral hypothermia for post-hypoxic neuroprotection in neonates using a solid ice cap. S Afr Med J 96 9 Pt 2 (2006) 976-981