Skip to main content
Erschienen in: Acta Neurologica Belgica 2/2020

28.02.2020 | Review article

Pathophysiology of hypoxic–ischemic encephalopathy: a review of the past and a view on the future

verfasst von: P. Greco, G. Nencini, I. Piva, M. Scioscia, C. A. Volta, S. Spadaro, M. Neri, G. Bonaccorsi, F. Greco, I. Cocco, F. Sorrentino, F. D’Antonio, L. Nappi

Erschienen in: Acta Neurologica Belgica | Ausgabe 2/2020

Einloggen, um Zugang zu erhalten

Abstract

Hypoxic–ischemic encephalopathy, also referred as HIE, is a type of brain injury or damage that is caused by a lack of oxygen to the brain during neonatal period. The incidence is approximately 1.5 cases per 1000 live births in developed countries. In low and middle-income countries, the incidence is much higher (10‒20 per 1000 live births). The treatment for neonatal HIE is hypothermia that is only partially effective (not more than 50% of the neonates treated achieve an improved outcome). HIE pathophysiology involves oxidative stress, mitochondrial energy production failure, glutaminergic excitotoxicity, and apoptosis. So, in the last years, many studies have focused on peptides that act somewhere in the pathway activated by severe anoxic injury leading to HIE. This review describes the pathophysiology of perinatal HIE and the mechanisms that could be the target of innovative HIE treatments.
Literatur
1.
Zurück zum Zitat Adstamongkonkul D, Hess DC (2017) Ischemic conditioning and neonatal hypoxic ischemic encephalopathy: a literature review. Cond Med 1(1):9–16PubMedPubMedCentral Adstamongkonkul D, Hess DC (2017) Ischemic conditioning and neonatal hypoxic ischemic encephalopathy: a literature review. Cond Med 1(1):9–16PubMedPubMedCentral
2.
Zurück zum Zitat Shah P, Perlman M (2009) Time courses of intrapartum asphyxia: neonatal characteristics and outcomes. Am J Perinatol 26(1):39–44PubMed Shah P, Perlman M (2009) Time courses of intrapartum asphyxia: neonatal characteristics and outcomes. Am J Perinatol 26(1):39–44PubMed
3.
Zurück zum Zitat Kurinczuk J, White-Koning M, Badawi N (2010) Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum Dev 86:329–338PubMed Kurinczuk J, White-Koning M, Badawi N (2010) Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum Dev 86:329–338PubMed
4.
Zurück zum Zitat Lawn J, Shibuya K, Stein C (2005) No cry at birth: global estimates of intrapartum stillbirths and intrapartum-related neonatal deaths. Bull World Health Organ 83(6):409–417PubMedPubMedCentral Lawn J, Shibuya K, Stein C (2005) No cry at birth: global estimates of intrapartum stillbirths and intrapartum-related neonatal deaths. Bull World Health Organ 83(6):409–417PubMedPubMedCentral
8.
Zurück zum Zitat Liu F, McCullough LD (2013) Inflammatory responses in hypoxic ischemic encephalopathy. Acta Pharmacol Sin 34:1121–1130PubMedPubMedCentral Liu F, McCullough LD (2013) Inflammatory responses in hypoxic ischemic encephalopathy. Acta Pharmacol Sin 34:1121–1130PubMedPubMedCentral
9.
Zurück zum Zitat Higgins RD, Raju T, Edwards AD et al (2011) Hypothermia and other treatment options for neonatal encephalopathy: an executive summary of the Eunice Kennedy Shriver NICHD workshop. J Pediatr 159:851–858PubMedPubMedCentral Higgins RD, Raju T, Edwards AD et al (2011) Hypothermia and other treatment options for neonatal encephalopathy: an executive summary of the Eunice Kennedy Shriver NICHD workshop. J Pediatr 159:851–858PubMedPubMedCentral
10.
Zurück zum Zitat Edwards AD, Brocklehurst P, Gunn AJ et al (2010) Neurological outcomes at 18 months of age after moderate hypothermia for perinatal hypoxic ischaemic encephalopathy: synthesis and meta-analysis of trial data. BMJ 340:c363PubMedPubMedCentral Edwards AD, Brocklehurst P, Gunn AJ et al (2010) Neurological outcomes at 18 months of age after moderate hypothermia for perinatal hypoxic ischaemic encephalopathy: synthesis and meta-analysis of trial data. BMJ 340:c363PubMedPubMedCentral
11.
Zurück zum Zitat Carloni S, Facchinetti F, Pelizzi N, Buonocore G, Balduini W (2018) Melatonin acts in synergy with hypothermia to reduce oxygen-glucose deprivation-Induced cell death in rat hippocampus organotypic slice cultures. Neonatology 114:364–371PubMed Carloni S, Facchinetti F, Pelizzi N, Buonocore G, Balduini W (2018) Melatonin acts in synergy with hypothermia to reduce oxygen-glucose deprivation-Induced cell death in rat hippocampus organotypic slice cultures. Neonatology 114:364–371PubMed
12.
Zurück zum Zitat Marcelino T, de Lemos RP, Miguel P, Netto C, Pereira Silva L, Matte C (2015) Effect of matermal exercise on biochemical parameters in rats submitted to neonatal hypoxia-ischemia. Brain Res 1622:91–101PubMed Marcelino T, de Lemos RP, Miguel P, Netto C, Pereira Silva L, Matte C (2015) Effect of matermal exercise on biochemical parameters in rats submitted to neonatal hypoxia-ischemia. Brain Res 1622:91–101PubMed
14.
Zurück zum Zitat Gunn A, Laptook A, Robertson N, Barks J, Thoresen M, Wassink GA (2017) Therapeutic hypothermia translates from ancient history in to practice. Pediatr Res 81:202–209PubMed Gunn A, Laptook A, Robertson N, Barks J, Thoresen M, Wassink GA (2017) Therapeutic hypothermia translates from ancient history in to practice. Pediatr Res 81:202–209PubMed
15.
Zurück zum Zitat Zubrow ABDPM, Ashraf Q, Fritz K, Mishra O (2002) Nitric oxide-mediated Ca2+/calmodulin-dependent protein kinase IV activity during hypoxia in neuronal nuclei from newborn piglets. Neurosci Lett 335:5–8PubMed Zubrow ABDPM, Ashraf Q, Fritz K, Mishra O (2002) Nitric oxide-mediated Ca2+/calmodulin-dependent protein kinase IV activity during hypoxia in neuronal nuclei from newborn piglets. Neurosci Lett 335:5–8PubMed
16.
Zurück zum Zitat Cao W, Carney J, Duchon A, Floyd R, Chevion M (1988) Oxygen free radical involvement in ischemia and reperfusion injury to brain. Neurosci Lett 88(2):233–238PubMed Cao W, Carney J, Duchon A, Floyd R, Chevion M (1988) Oxygen free radical involvement in ischemia and reperfusion injury to brain. Neurosci Lett 88(2):233–238PubMed
17.
Zurück zum Zitat Zubrow AB, Delivoria-Papadopoulosm M, Ashrafm QM et al (2002) Nitric oxide-mediated expression of Bax protein and DNA fragmentation during hypoxia in neuronal nuclei from newborn piglets. Brain Res 954(1):60–67PubMed Zubrow AB, Delivoria-Papadopoulosm M, Ashrafm QM et al (2002) Nitric oxide-mediated expression of Bax protein and DNA fragmentation during hypoxia in neuronal nuclei from newborn piglets. Brain Res 954(1):60–67PubMed
18.
Zurück zum Zitat Groenendaal F, Vles J, Lammers H, De Vente J, Smit D, Nikkels P (2008) Nitrotyrosine in human neonatal spinal cord after perinatal asphyxia. Neonatology 93(1):1–6PubMed Groenendaal F, Vles J, Lammers H, De Vente J, Smit D, Nikkels P (2008) Nitrotyrosine in human neonatal spinal cord after perinatal asphyxia. Neonatology 93(1):1–6PubMed
19.
Zurück zum Zitat Dorrepaal C, van Bel F, Moison R, Shadid M, van de Bor M, Steendijk P et al (1997) Oxidative stress during post-hypoxic-ischemic reperfusion in the newborn lamb: the effect of nitric oxide synthesis inhibition. Pediatr Res 41:321–326PubMed Dorrepaal C, van Bel F, Moison R, Shadid M, van de Bor M, Steendijk P et al (1997) Oxidative stress during post-hypoxic-ischemic reperfusion in the newborn lamb: the effect of nitric oxide synthesis inhibition. Pediatr Res 41:321–326PubMed
20.
Zurück zum Zitat Lu Y, Tucker D, Dong Y, Zhao N, Zhuo X, Zhang Q (2015) Role of mitochondria in neonatal hypoxic-ischemic brain injury. J Neurosci Rehabil 2(1):1–14PubMedPubMedCentral Lu Y, Tucker D, Dong Y, Zhao N, Zhuo X, Zhang Q (2015) Role of mitochondria in neonatal hypoxic-ischemic brain injury. J Neurosci Rehabil 2(1):1–14PubMedPubMedCentral
21.
Zurück zum Zitat Erecinska M, Silver I (1994) Ions and energy in mammalian brain. Prog Neurobiol 43(1):37–71PubMed Erecinska M, Silver I (1994) Ions and energy in mammalian brain. Prog Neurobiol 43(1):37–71PubMed
22.
Zurück zum Zitat Gilland E, Puka-Sundvall M, Hillered L, Hagberg H (1998) Mitochondrial function and energy metabolism after hypoxia-ischemia in the immature brain: involvement of NMDA receptors. J Cereb Blood Flow Metab 18(3):297–304PubMed Gilland E, Puka-Sundvall M, Hillered L, Hagberg H (1998) Mitochondrial function and energy metabolism after hypoxia-ischemia in the immature brain: involvement of NMDA receptors. J Cereb Blood Flow Metab 18(3):297–304PubMed
23.
Zurück zum Zitat Wang K (2000) Calpain and caspase: can you tell the difference? Trends Neurosci 23(1):20–6PubMed Wang K (2000) Calpain and caspase: can you tell the difference? Trends Neurosci 23(1):20–6PubMed
24.
Zurück zum Zitat Wang H, Pathan N, Ethell I, Krajewski S, Yamaguchi Y, Shibasaki F et al (1999) Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 229:339–343 Wang H, Pathan N, Ethell I, Krajewski S, Yamaguchi Y, Shibasaki F et al (1999) Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 229:339–343
25.
Zurück zum Zitat McDonald J, Johnston M (1990) Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res Rev 15:41–70PubMed McDonald J, Johnston M (1990) Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res Rev 15:41–70PubMed
26.
Zurück zum Zitat Johnston MV, Trescher WH, Ishida A, Nakajima W, Zipursky A (2001) Neurobiology of hypoxic-ischemic injury in the developing brain. Pediatr Res 49(6):735–741PubMed Johnston MV, Trescher WH, Ishida A, Nakajima W, Zipursky A (2001) Neurobiology of hypoxic-ischemic injury in the developing brain. Pediatr Res 49(6):735–741PubMed
27.
Zurück zum Zitat Cassina A, Radi R (1996) Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 328(2):309–316PubMed Cassina A, Radi R (1996) Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 328(2):309–316PubMed
28.
Zurück zum Zitat Thornton C, Rousset CI, Kichev A, Miyakuni Y, Vontell R, Baburamani AA et al (2012) Molecular mechanisms of neonatal brain injury. Neurol Res Int 2012:e506320 Thornton C, Rousset CI, Kichev A, Miyakuni Y, Vontell R, Baburamani AA et al (2012) Molecular mechanisms of neonatal brain injury. Neurol Res Int 2012:e506320
29.
Zurück zum Zitat Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LGD, Neumann D et al (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13(22):2004–2008PubMed Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LGD, Neumann D et al (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13(22):2004–2008PubMed
31.
Zurück zum Zitat Uchino H, Minamikawa-Tachino R, Kristián T, Perkins G, Narazaki M, Siesjö B et al (2002) Differential neuroprotection by cyclosporin A and FK506 following ischemia corresponds with differing abilities to inhibit calcineurin and the mitochodrial permeability transition. Neurobiol Dis 10(3):219–233PubMed Uchino H, Minamikawa-Tachino R, Kristián T, Perkins G, Narazaki M, Siesjö B et al (2002) Differential neuroprotection by cyclosporin A and FK506 following ischemia corresponds with differing abilities to inhibit calcineurin and the mitochodrial permeability transition. Neurobiol Dis 10(3):219–233PubMed
32.
Zurück zum Zitat Alessandri B, Rice A, Levasseur J, DeFord M, Hamm R, Bullock M (2002) Cyclosporin A improves brain tissue oxygen consumption and learning/memory performance after lateral fluid percussion injury in rats. J Neurotrauma 19(7):829–841PubMed Alessandri B, Rice A, Levasseur J, DeFord M, Hamm R, Bullock M (2002) Cyclosporin A improves brain tissue oxygen consumption and learning/memory performance after lateral fluid percussion injury in rats. J Neurotrauma 19(7):829–841PubMed
33.
Zurück zum Zitat Perier C, Tieu KGC, Caspersen C, Jackson-Lewis V, Carelli V, Martinuzzi A et al (2005) Complex I deficiency primes bax dependent neuronal apoptosis through mitochondrial oxidative damage. Proc Natl Acad Sci USA 102(52):19126–21913PubMedPubMedCentral Perier C, Tieu KGC, Caspersen C, Jackson-Lewis V, Carelli V, Martinuzzi A et al (2005) Complex I deficiency primes bax dependent neuronal apoptosis through mitochondrial oxidative damage. Proc Natl Acad Sci USA 102(52):19126–21913PubMedPubMedCentral
34.
Zurück zum Zitat Thornton C, Hagberg H (2015) Role of mitochondria in apoptotic and necroptotic cell death in the developing brain. Clin Chim Acta 451:35–38PubMedPubMedCentral Thornton C, Hagberg H (2015) Role of mitochondria in apoptotic and necroptotic cell death in the developing brain. Clin Chim Acta 451:35–38PubMedPubMedCentral
35.
Zurück zum Zitat Nakajima W, Ishida ALM, Gabrielson K, Wilson M, Martin L, Blue M et al (2000) Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. J Neurosci 20(21):7994–8004PubMedPubMedCentral Nakajima W, Ishida ALM, Gabrielson K, Wilson M, Martin L, Blue M et al (2000) Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. J Neurosci 20(21):7994–8004PubMedPubMedCentral
36.
Zurück zum Zitat Montaldo P, Kaforou M, Pollara G et al (2019) Whole blood gene expression reveals specific transcriptome changes in neonatal encephalopathy. Neonatology 115(1):68–76PubMed Montaldo P, Kaforou M, Pollara G et al (2019) Whole blood gene expression reveals specific transcriptome changes in neonatal encephalopathy. Neonatology 115(1):68–76PubMed
37.
Zurück zum Zitat Northington FJ, Chavez-Valdez R, Martin LJ (2011) Neuronal cell death in neonatal hypoxia-ischemia. Ann Neurol 69(5):743–758PubMedPubMedCentral Northington FJ, Chavez-Valdez R, Martin LJ (2011) Neuronal cell death in neonatal hypoxia-ischemia. Ann Neurol 69(5):743–758PubMedPubMedCentral
38.
Zurück zum Zitat Ginet V, Puyal J, Clarke PG, Truttmann AC (2009) Enhancement of autophagic flux after neonatal cerebral hypoxia-ischemia and its region-specific relationship to apoptotic mechanisms. Am J Pathol 175(5):1962–1974PubMedPubMedCentral Ginet V, Puyal J, Clarke PG, Truttmann AC (2009) Enhancement of autophagic flux after neonatal cerebral hypoxia-ischemia and its region-specific relationship to apoptotic mechanisms. Am J Pathol 175(5):1962–1974PubMedPubMedCentral
39.
Zurück zum Zitat Koike M, Shibata M, Tadakoshi M et al (2008) Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 172(2):454–469PubMedPubMedCentral Koike M, Shibata M, Tadakoshi M et al (2008) Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 172(2):454–469PubMedPubMedCentral
40.
Zurück zum Zitat Xu Y, Tian Y, Tian Y, Li X, Zhao P (2016) Autophagy activation involved in hypoxic-ischemic brain injury induces cognitive and memory impairment in neonatal rats. J Neurochem 139(5):795–805PubMed Xu Y, Tian Y, Tian Y, Li X, Zhao P (2016) Autophagy activation involved in hypoxic-ischemic brain injury induces cognitive and memory impairment in neonatal rats. J Neurochem 139(5):795–805PubMed
41.
Zurück zum Zitat Choi D, Rothman SM (1990) The role of glutamate neurotoxicity in hypoxicischemic neuronal death. Ann Rev Neurosci 13:171–182PubMed Choi D, Rothman SM (1990) The role of glutamate neurotoxicity in hypoxicischemic neuronal death. Ann Rev Neurosci 13:171–182PubMed
42.
43.
Zurück zum Zitat Del Bigio M, Becker L (1994) Microglial aggregation in the dentate gyrus: a marker of mild hypoxic-ischaemic brain insult in human infants. Neuropathol Appl Neurobiol 20:144–151PubMed Del Bigio M, Becker L (1994) Microglial aggregation in the dentate gyrus: a marker of mild hypoxic-ischaemic brain insult in human infants. Neuropathol Appl Neurobiol 20:144–151PubMed
44.
Zurück zum Zitat Hagberg H, Mallard C, Ferriero DM, Vannucci SJ, Levison SW, Vexler ZS et al (2015) The role of inflammation in perinatal brain injury. Nat Rev Neurol 11:192–208PubMedPubMedCentral Hagberg H, Mallard C, Ferriero DM, Vannucci SJ, Levison SW, Vexler ZS et al (2015) The role of inflammation in perinatal brain injury. Nat Rev Neurol 11:192–208PubMedPubMedCentral
45.
Zurück zum Zitat Faustino J, Wang X, Johnson C, Klibanov A, Derugin N, Wendland M et al (2011) Microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke. J Neurosci 31:12992–13001PubMedPubMedCentral Faustino J, Wang X, Johnson C, Klibanov A, Derugin N, Wendland M et al (2011) Microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke. J Neurosci 31:12992–13001PubMedPubMedCentral
46.
Zurück zum Zitat Varnum M, Ikezu T (2012) The classification of microglial activation phenotypes on neurodegeneration and regeneration in Alzheimer’s disease brain. Arch Immunol Ther Exp 60:251–266 Varnum M, Ikezu T (2012) The classification of microglial activation phenotypes on neurodegeneration and regeneration in Alzheimer’s disease brain. Arch Immunol Ther Exp 60:251–266
47.
Zurück zum Zitat Swanson R, Ying W, Kauppinen T (2004) Astrocyte influences on ischemic neuronal death. Curr Mol Med 4:193–205PubMed Swanson R, Ying W, Kauppinen T (2004) Astrocyte influences on ischemic neuronal death. Curr Mol Med 4:193–205PubMed
48.
Zurück zum Zitat Anderson C, Swanson R (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1–14PubMed Anderson C, Swanson R (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1–14PubMed
49.
Zurück zum Zitat Jiang N, Chopp M, Chahwala S (1998) Neutrophil inhibitory factor treatment of focal cerebral ischemia in the rat. Brain Res 788:25–34PubMed Jiang N, Chopp M, Chahwala S (1998) Neutrophil inhibitory factor treatment of focal cerebral ischemia in the rat. Brain Res 788:25–34PubMed
50.
Zurück zum Zitat Bona E, Andersson A, Blomgren K, Gilland E, Puka-Sundvall M, Gustafson K et al (1999) Chemokine and inflammatory cell response to hypoxia-ischemia in immature rats. Pediatr Res 45(4 Pt 1):500–509PubMed Bona E, Andersson A, Blomgren K, Gilland E, Puka-Sundvall M, Gustafson K et al (1999) Chemokine and inflammatory cell response to hypoxia-ischemia in immature rats. Pediatr Res 45(4 Pt 1):500–509PubMed
51.
Zurück zum Zitat Yıldız E, Ekici B, Tatlı B (2017) Neonatal hypoxic ischemic encephalopathy: an update on disease pathogenesis and treatment. Expert Rev Neurother 17(5):449–459PubMed Yıldız E, Ekici B, Tatlı B (2017) Neonatal hypoxic ischemic encephalopathy: an update on disease pathogenesis and treatment. Expert Rev Neurother 17(5):449–459PubMed
52.
Zurück zum Zitat Liu J, Feng ZC (2010) Increased umbilical cord plasma interleukin-1 beta levels was correlated with adverse outcomes of neonatal hypoxicischemic encephalopathy. J Trop Pediatr 56:178–182PubMed Liu J, Feng ZC (2010) Increased umbilical cord plasma interleukin-1 beta levels was correlated with adverse outcomes of neonatal hypoxicischemic encephalopathy. J Trop Pediatr 56:178–182PubMed
53.
Zurück zum Zitat Green H, Treacy E, Keohane A, Sullivan A, O’Keeffe G, Nolan Y (2012) A role for interleukin-1beta in determining the lineage fate of embryonic rat hippocampal neural precursor cells. Mol Cell Neurosci 49:311–312PubMed Green H, Treacy E, Keohane A, Sullivan A, O’Keeffe G, Nolan Y (2012) A role for interleukin-1beta in determining the lineage fate of embryonic rat hippocampal neural precursor cells. Mol Cell Neurosci 49:311–312PubMed
54.
Zurück zum Zitat Martin D, Chinookoswong N, Miller G (1994) The interleukin-1 receptor antagonist (rhIL-1ra) protects against cerebral infarction in a rat model of hypoxia-ischemia. Exp Neurol 130:362–367PubMed Martin D, Chinookoswong N, Miller G (1994) The interleukin-1 receptor antagonist (rhIL-1ra) protects against cerebral infarction in a rat model of hypoxia-ischemia. Exp Neurol 130:362–367PubMed
55.
Zurück zum Zitat Baggiolini M (2001) Chemokines in pathology and medicine. J Intern Med 250:91–104PubMed Baggiolini M (2001) Chemokines in pathology and medicine. J Intern Med 250:91–104PubMed
56.
Zurück zum Zitat Wu Q, Chen W, Sinha B et al (2015) Neuroprotective agents for neonatal hypoxic-ischemic brain injury. Drug Discov Today 20(11):1372–1381PubMed Wu Q, Chen W, Sinha B et al (2015) Neuroprotective agents for neonatal hypoxic-ischemic brain injury. Drug Discov Today 20(11):1372–1381PubMed
58.
Zurück zum Zitat Faulkner S, Bainbridge A, Kato T, Chandrasekaran M, Kapetanakis AB, Hristova M, Liu M, Evans S, De Vita E, Kelen D et al (2011) Xenon augmented hypothermia reduces early lactate/N-acetylaspartate and cell death in perinatal asphyxia. Ann Neurol 70:133–150PubMed Faulkner S, Bainbridge A, Kato T, Chandrasekaran M, Kapetanakis AB, Hristova M, Liu M, Evans S, De Vita E, Kelen D et al (2011) Xenon augmented hypothermia reduces early lactate/N-acetylaspartate and cell death in perinatal asphyxia. Ann Neurol 70:133–150PubMed
59.
Zurück zum Zitat Chakkarapani E, Dingley J, Liu X, Hoque N, Aquilina K, Porter H, Thoresen M (2010) Xenon enhances hypothermic neuroprotection in asphyxiated newborn pigs. Ann Neurol 68:330–341PubMed Chakkarapani E, Dingley J, Liu X, Hoque N, Aquilina K, Porter H, Thoresen M (2010) Xenon enhances hypothermic neuroprotection in asphyxiated newborn pigs. Ann Neurol 68:330–341PubMed
60.
Zurück zum Zitat Azzopardi D, Robertson NJ, Bainbridge A, Cady E, Charles-Edwards G, Deierl A, Fagiolo G, Franks NP, Griffiths J, Hajnal J et al (2016) Moderate hypothermia within 6 h of birth plus inhaled xenon versus moderate hypothermia alone after birth asphyxia (TOBY-Xe): a proof-of-concept, open-label, randomised controlled trial. Lancet Neurol 15:145–153PubMedPubMedCentral Azzopardi D, Robertson NJ, Bainbridge A, Cady E, Charles-Edwards G, Deierl A, Fagiolo G, Franks NP, Griffiths J, Hajnal J et al (2016) Moderate hypothermia within 6 h of birth plus inhaled xenon versus moderate hypothermia alone after birth asphyxia (TOBY-Xe): a proof-of-concept, open-label, randomised controlled trial. Lancet Neurol 15:145–153PubMedPubMedCentral
61.
Zurück zum Zitat Faulkner SD, Downie NA, Mercer CJ, Kerr SA, Sanders RD, Robertson NJ (2012) A xenon recirculating ventilator for the newborn piglet: developing clinical applications of xenon for neonates. Eur J Anaesthesiol 29:577–585PubMed Faulkner SD, Downie NA, Mercer CJ, Kerr SA, Sanders RD, Robertson NJ (2012) A xenon recirculating ventilator for the newborn piglet: developing clinical applications of xenon for neonates. Eur J Anaesthesiol 29:577–585PubMed
62.
Zurück zum Zitat Broad KD, Fierens I, Fleiss B, Rocha-Ferreira E, Ezzati M, Hassell J, Alonso-Alconada D, Bainbridge A, Kawano G, Ma D et al (2016) Inhaled 45–50% argon augments hypothermic brain protection in a piglet model of perinatal asphyxia. Neurobiol Dis 87:29–38PubMedPubMedCentral Broad KD, Fierens I, Fleiss B, Rocha-Ferreira E, Ezzati M, Hassell J, Alonso-Alconada D, Bainbridge A, Kawano G, Ma D et al (2016) Inhaled 45–50% argon augments hypothermic brain protection in a piglet model of perinatal asphyxia. Neurobiol Dis 87:29–38PubMedPubMedCentral
63.
Zurück zum Zitat Aly H, Elmahdy H, El-Dib M, Rowisha M, Awny M, El-Gohary T, Elbatch M, Hamisa M, El-Mashad AR (2015) Melatonin use for neuroprotection in perinatal asphyxia: a randomized controlled pilot study. J Perinatol 35:186–191PubMed Aly H, Elmahdy H, El-Dib M, Rowisha M, Awny M, El-Gohary T, Elbatch M, Hamisa M, El-Mashad AR (2015) Melatonin use for neuroprotection in perinatal asphyxia: a randomized controlled pilot study. J Perinatol 35:186–191PubMed
64.
Zurück zum Zitat Wu YW, Mathur AM, Chang T, McKinstry RC, Mulkey SB, Mayock DE, Van Meurs KP, Rogers EE, Gonzalez FF, Comstock BA et al (2016) High-dose erythropoietin and hypothermia for hypoxic-ischemic encephalopathy: a phase ii trial. Pediatrics 137:e20160190 Wu YW, Mathur AM, Chang T, McKinstry RC, Mulkey SB, Mayock DE, Van Meurs KP, Rogers EE, Gonzalez FF, Comstock BA et al (2016) High-dose erythropoietin and hypothermia for hypoxic-ischemic encephalopathy: a phase ii trial. Pediatrics 137:e20160190
65.
Zurück zum Zitat Baserga MC, Beachy JC, Roberts JK, Ward RM, DiGeronimo RJ, Walsh WF, Ohls RK, Anderson J, Mayock DE, Juul SE et al (2015) Darbepoetin administration to neonates undergoing cooling for encephalopathy: a safety and pharmacokinetic trial. Pediatr Res 78:315–322PubMedPubMedCentral Baserga MC, Beachy JC, Roberts JK, Ward RM, DiGeronimo RJ, Walsh WF, Ohls RK, Anderson J, Mayock DE, Juul SE et al (2015) Darbepoetin administration to neonates undergoing cooling for encephalopathy: a safety and pharmacokinetic trial. Pediatr Res 78:315–322PubMedPubMedCentral
67.
Zurück zum Zitat Maiwald CA, Annink KV, Rüdiger M et al (2019) Effect of allopurinol in addition to hypothermia treatment in neonates for hypoxic-ischemic brain injury on neurocognitive outcome (ALBINO): study protocol of a blinded randomized placebo-controlled parallel group multicenter trial for superiority (phase III). BMC Pediatr 19(1):210PubMedPubMedCentral Maiwald CA, Annink KV, Rüdiger M et al (2019) Effect of allopurinol in addition to hypothermia treatment in neonates for hypoxic-ischemic brain injury on neurocognitive outcome (ALBINO): study protocol of a blinded randomized placebo-controlled parallel group multicenter trial for superiority (phase III). BMC Pediatr 19(1):210PubMedPubMedCentral
68.
Zurück zum Zitat Bhat MA, Charoo BA, Bhat JI, Ahmad SM, Ali SW, Mufti MU (2009) Magnesium sulfate in severe perinatal asphyxia: a randomized, placebo-controlled trial. Pediatrics 123:e764–e769PubMed Bhat MA, Charoo BA, Bhat JI, Ahmad SM, Ali SW, Mufti MU (2009) Magnesium sulfate in severe perinatal asphyxia: a randomized, placebo-controlled trial. Pediatrics 123:e764–e769PubMed
69.
Zurück zum Zitat Galinsky R, Bennet L, Groenendaal F, Lear CA, Tan S, van Bel F, Juul SE, Robertson NJ, Mallard C, Gunn AJ (2014) Magnesium is not consistently neuroprotective for perinatal hypoxia-ischemia in term-equivalent models in preclinical studies: a systematic review. Dev Neurosci 36:73–82PubMed Galinsky R, Bennet L, Groenendaal F, Lear CA, Tan S, van Bel F, Juul SE, Robertson NJ, Mallard C, Gunn AJ (2014) Magnesium is not consistently neuroprotective for perinatal hypoxia-ischemia in term-equivalent models in preclinical studies: a systematic review. Dev Neurosci 36:73–82PubMed
70.
Zurück zum Zitat Tagin M, Shah PS, Lee KS (2013) Magnesium for newborns with hypoxic-ischemic encephalopathy: a systematic review and meta-analysis. J Perinatol 33:663–669PubMed Tagin M, Shah PS, Lee KS (2013) Magnesium for newborns with hypoxic-ischemic encephalopathy: a systematic review and meta-analysis. J Perinatol 33:663–669PubMed
71.
Zurück zum Zitat Felling RJ, Snyder MJ, Romanko MJ, Rothstein RP, Ziegler AN, Yang Z et al (2006) Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia. J Neurosci 26(16):4359–4369PubMedPubMedCentral Felling RJ, Snyder MJ, Romanko MJ, Rothstein RP, Ziegler AN, Yang Z et al (2006) Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia. J Neurosci 26(16):4359–4369PubMedPubMedCentral
73.
Zurück zum Zitat Daadi MM, Davis AS, Arac A et al (2010) Human neural stem cell grafts modify microglial response and enhance axonal sprouting in neonatal hypoxic–ischemic brain injury. Stroke 41(3):516–523PubMedPubMedCentral Daadi MM, Davis AS, Arac A et al (2010) Human neural stem cell grafts modify microglial response and enhance axonal sprouting in neonatal hypoxic–ischemic brain injury. Stroke 41(3):516–523PubMedPubMedCentral
74.
Zurück zum Zitat Shinoyama M, Ideguchi M, Kida H et al (2013) Cortical region-specific engraftment of embryonic stem cell derived neural progenitor cell restores axonal sprouting to a subcortical target and achieves motor functional recovery in a mouse model of neonatal hypoxic ischemic brain injury. Front Cell Neurosci 7:128PubMedPubMedCentral Shinoyama M, Ideguchi M, Kida H et al (2013) Cortical region-specific engraftment of embryonic stem cell derived neural progenitor cell restores axonal sprouting to a subcortical target and achieves motor functional recovery in a mouse model of neonatal hypoxic ischemic brain injury. Front Cell Neurosci 7:128PubMedPubMedCentral
75.
Zurück zum Zitat Ji G, Liu M, Zhao XF et al (2015) NF-kB signaling is involved in the effects of intranasally engrafted human neural stem cells on neurofunctional improvements in neonatal rat hypoxic–ischemic encephalopathy. CNS Neurosci Ther 21(12):926–935PubMedPubMedCentral Ji G, Liu M, Zhao XF et al (2015) NF-kB signaling is involved in the effects of intranasally engrafted human neural stem cells on neurofunctional improvements in neonatal rat hypoxic–ischemic encephalopathy. CNS Neurosci Ther 21(12):926–935PubMedPubMedCentral
76.
Zurück zum Zitat Luan Z, Yin GC, Hu XH et al (2005) Treatment of an infant with severe neonatal hypoxic–ischemic encephalopathy sequelae with transplantation of human neural stem cell into cerebral ventricle. Zhonghua Er Ke Za Zhi 43(8):580–583 (discussion 580) PubMed Luan Z, Yin GC, Hu XH et al (2005) Treatment of an infant with severe neonatal hypoxic–ischemic encephalopathy sequelae with transplantation of human neural stem cell into cerebral ventricle. Zhonghua Er Ke Za Zhi 43(8):580–583 (discussion 580) PubMed
77.
Zurück zum Zitat Luan Z, Liu WP, Qu SQ et al (2011) Treatment of newborns with severe injured brain with transplantation of human neural precursor cell. Zhonghua Er Ke Za Zhi 49(6):445–449PubMed Luan Z, Liu WP, Qu SQ et al (2011) Treatment of newborns with severe injured brain with transplantation of human neural precursor cell. Zhonghua Er Ke Za Zhi 49(6):445–449PubMed
78.
Zurück zum Zitat Pimentel-coelho PM, Magalhaes ES, Lopes LM et al (2010) Human cord blood transplantation in a neonatal rat model of hypoxic–ischemic brain damage: functional outcome related to neuroprotection in the striatum. Stem Cells Dev 19(3):351–358PubMed Pimentel-coelho PM, Magalhaes ES, Lopes LM et al (2010) Human cord blood transplantation in a neonatal rat model of hypoxic–ischemic brain damage: functional outcome related to neuroprotection in the striatum. Stem Cells Dev 19(3):351–358PubMed
79.
Zurück zum Zitat Huang HZ, Wen XH, Liu H et al (2013) Human umbilical cord blood mononuclear cell transplantation promotes long-term neurobehavioral functional development of newborn SD rats with hypoxic ischemic brain injury. Zhonghua Er Ke Za Zhi 51(6):460–466PubMed Huang HZ, Wen XH, Liu H et al (2013) Human umbilical cord blood mononuclear cell transplantation promotes long-term neurobehavioral functional development of newborn SD rats with hypoxic ischemic brain injury. Zhonghua Er Ke Za Zhi 51(6):460–466PubMed
80.
Zurück zum Zitat Yasuhara T, Hara K, Maki M et al (2010) Mannitol facilitates neurotrophic factor up-regulation and behavioural recovery in neonatal hypoxic–ischaemic rats with human umbilical cord blood grafts. J Cell Mol Med 14(4):914–921PubMedPubMedCentral Yasuhara T, Hara K, Maki M et al (2010) Mannitol facilitates neurotrophic factor up-regulation and behavioural recovery in neonatal hypoxic–ischaemic rats with human umbilical cord blood grafts. J Cell Mol Med 14(4):914–921PubMedPubMedCentral
81.
Metadaten
Titel
Pathophysiology of hypoxic–ischemic encephalopathy: a review of the past and a view on the future
verfasst von
P. Greco
G. Nencini
I. Piva
M. Scioscia
C. A. Volta
S. Spadaro
M. Neri
G. Bonaccorsi
F. Greco
I. Cocco
F. Sorrentino
F. D’Antonio
L. Nappi
Publikationsdatum
28.02.2020
Verlag
Springer International Publishing
Erschienen in
Acta Neurologica Belgica / Ausgabe 2/2020
Print ISSN: 0300-9009
Elektronische ISSN: 2240-2993
DOI
https://doi.org/10.1007/s13760-020-01308-3

Weitere Artikel der Ausgabe 2/2020

Acta Neurologica Belgica 2/2020 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.