Erythropoietin protects newborn rat against sevoflurane-induced neurotoxicity

Paediatric Anaesthesia

Volumn 24, Issue 7, 2014, Pages 749-759

  Pellegrini, Lionel ^a,b   Bennis, Youssef ^b,c   Velly, Lionel ^a   Grandvuillemin, Isabelle ^b,d   Pisano, Pascale ^b,c   Bruder, Nicolas ^a   Guillet, Benjamin ^b,c,e  

^a TIMONE HOSPITAL   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE MARSEILLE   (France)

^d HÔPITAL DE LA CONCEPTION   (France)

^e Aix Marseille University   (France)

Author keywords

erythropoietin; neuroprotection; neurotoxicity; newborn; sevoflurane

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN EXTRACT; CASPASE 3; RECOMBINANT ERYTHROPOIETIN; SEVOFLURANE; ERYTHROPOIETIN; ETHER DERIVATIVE; INHALATION ANESTHETIC AGENT; RECOMBINANT PROTEIN;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; LEARNING; MORRIS WATER MAZE TEST; NEUROPROTECTION; NEUROTOXICITY; NEWBORN; NICK END LABELING; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SINGLE DRUG DOSE; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD GAS ANALYSIS; BRAIN; CHEMICALLY INDUCED; COGNITION DISORDERS; DRUG EFFECTS; MAZE TEST; MEMORY; NERVOUS SYSTEM DISEASES; PATHOLOGY; PSYCHOLOGY; RECOGNITION; SPRAGUE DAWLEY RAT; TOXICITY;

ANESTHETICS, INHALATION; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BLOOD GAS ANALYSIS; BRAIN; COGNITION DISORDERS; ERYTHROPOIETIN; MAZE LEARNING; MEMORY; METHYL ETHERS; NERVOUS SYSTEM DISEASES; RATS; RATS, SPRAGUE-DAWLEY; RECOGNITION (PSYCHOLOGY); RECOMBINANT PROTEINS;

EID: 84902385529     PISSN: 11555645     EISSN: 14609592     Source Type: Journal    
DOI: 10.1111/pan.12372     Document Type: Article

References (67)

1. Schifilliti D, Grasso G, Conti A, et al,. Anaesthetic-related neuroprotection: intravenous or inhalational agents? CNS Drugs 2010; 24: 893-907.
2. Istaphanous GK, Ward CG, Loepke AW,. The impact of the perioperative period on neurocognitive development, with a focus on pharmacological concerns. Best Pract Res Clin Anaesthesiol 2010; 24: 433-449.
3. Loepke AW, McGowan FX Jr, Soriano SG,. The toxic effects of anesthetics in the developing brain: the clinical perspective. Anesth Analg 2008; 106: 1664-1669.
4. Jevtovic-Todorovic V, Olney JW,. PRO: Anesthesia-induced developmental neuroapoptosis: status of the evidence. Anesth Analg 2008; 106: 1659-1663.
5. Mellon RD, Simone AF, Rappaport BA,. Use of anesthetic agents in neonates and young children. Anesth Analg 2007; 104: 509-520.
6. Liang G, Ward C, Peng J, et al,. Isoflurane causes greater neurodegeneration than an equivalent exposure of Sevoflurane in the developing brain of neonatal mice. Anesthesiology 2010; 112: 1325-1334.
7. Satomoto M, Satoh Y, Terui K, et al,. Neonatal exposure to Sevoflurane induces abnormal social behaviors and deficits in fear conditioning in mice. Anesthesiology 2009; 110: 628-637.
8. Satomoto M,. Neonatal exposure to Sevoflurane induces abnormal social behaviors and deficits in fear conditioning in mice. Anesthesiology 2009; 110: 628-637.
9. Jevtovic-Todorovic V, Hartman RE, Izumi Y, et al,. Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J Neurosci 2003; 23: 876-882.
10. Fredriksson A, Archer T, Alm H, et al,. Neurofunctional deficits and potentiated apoptosis by neonatal NMDA antagonist administration. Behav Brain Res 2004; 153: 367-376.
11. Fredriksson A, Pontén E, Gordh T, et al,. Neonatal exposure to a combination of N-methyl-D-aspartate and gamma-aminobutyric acid type A receptor anesthetic agents potentiates apoptotic neurodegeneration and persistent behavioral deficits. Anesthesiology 2007; 107: 427-436.
12. Wilder RT, Flick RP, Sprung J, et al,. Early exposure to anesthesia and learning disabilities in a population-based birth cohort. Anesthesiology 2009; 110: 796-804.
13. DiMaggio B, DiMaggio C, Sun LS, et al,. A retrospective cohort study of the association of anesthesia and hernia repair surgery with behavioral and developmental disorders in young children. J Neurosurg Anesthesiol 2009; 21: 286-291.
14. Kalkman CJ, Peelen L, Moons KG, et al,. Behavior and development in children and age at the time of first anesthetic exposure. Anesthesiology 2009; 110: 805-812.
15. Sun LS, Li G, Dimaggio C, et al,. Anesthesia and neurodevelopment in children: time for an answer? Anesthesiology 2008; 109: 757-761.
16. Velly L, Pellegrini L, Guillet B, et al,. Erythropoietin 2nd cerebral protection after acute injuries: a double-edged sword? Pharmacol Ther 2010; 128: 445-459.
17. Studer L, Csete M, Lee SH, et al,. Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J Neurosci 2000; 20: 7377-7383.
18. Shingo T, Sorokan ST, Shimazaki T, et al,. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci 2001; 21: 9733-9743.
19. Yu X, Lin CS, Costantini F, et al,. The human erythropoietin receptor gene rescues erythropoiesis and developmental defects in the erythropoietin receptor null mouse. Blood 2001; 98: 475-477.
20. Yu X, Shacka JJ, Eells JB, et al,. Erythropoietin receptor signalling is required for normal brain development. Development 2002; 129: 505-516.
21. Ribatti D, Presta M, Vacca A, et al,. Human erythropoietin induces a pro-angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. Blood 1999; 93: 2627-2636.
22. Heeschen C, Aicher A, Lehmann R, et al,. Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 2003; 102: 1340-1346.
23. Zhang D, Zhang F, Zhang Y, et al,. Combining erythropoietin infusion with intramyocardial delivery of bone marrow cells is more effective for cardiac repair. Transpl Int 2007; 20: 174-183.
24. Oda S, Nagahama R, Nakano K, et al,. Nanoparticle-mediated endothelial cell-selective delivery of pitavastatin induces functional collateral arteries (therapeutic arteriogenesis) in a rabbit model of chronic hind limb ischemia. J Vasc Surg 2010; 52: 412-420.
25. Digicaylioglu M, Lipton SA,. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 2001; 412: 641-647.
26. Sirén AL, Ehrenreich H,. Erythropoietin-a novel concept for neuroprotection. Eur Arch Psychiatry Clin Neurosci 2001; 251: 179-184.
27. Keller M, Yang J, Griesmaier E, et al,. Erythropoietin is neuroprotective against NMDA-receptor-mediated excitotoxic brain injury in newborn mice. Neurobiol Dis 2006; 24: 357-366.
28. Zhu C, Kang W, Xu F, et al,. Erythropoietin improved neurologic outcomes in newborns with hypoxic-ischemic encephalopathy. Pediatrics 2009; 124: 218-226.
29. Elmahdy MF, Ghareeb Mahdy S, Baligh Ewiss E, et al,. Value of duplex scanning in differentiating embolic from thrombotic arterial occlusion in acute limb ischemia. Cardiovasc Revasc Med 2010; 11: 223-226.
30. Orliaguet G, Vivien B, Langeron O, et al,. Minimum alveolar concentration of volatile anesthetics in rats during postnatal maturation. Anesthesiology 2001; 95: 734-739.
31. Lu Y, Wu X, Dong Y, et al,. Anesthetic Sevoflurane causes neurotoxicity differently in neonatal naïve and Alzheimer disease transgenic mice. Anesthesiology 2010; 112: 1404-1416.
32. Bartolini L, Casamenti F, Pepeu G,. Aniracetam restores object recognition impaired by age, scopolamine, and nucleus basalis lesions. Pharmacol Biochem Behav 1996; 53: 277-283.
33. Antunes M, Biala G,. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 2012 May; 13: 93-110.
34. Li Y, Liang G, Wang S, et al,. Effects of fetal exposure to isoflurane on postnatal memory and learning in rats. Neuropharmacology 2007; 53: 942-950.
35. Sanders RD, Xu J, Shu Y, et al,. Dexmedetomidine attenuates isoflurane-induced neurocognitive impairment in neonatal rats. Anesthesiology 2009; 110: 1077-1085.
36. Rozé JC, Denizot S, Carbajal R, et al,. Prolonged sedation and/or analgesia and 5-year neurodevelopment outcome in very preterm infants: results from the EPIPAGE cohort. Arch Pediatr Adolesc Med 2008; 162: 728-733.
37. Sprung J, Flick RP, Wilder RT, et al,. Anesthesia for cesarean delivery and learning disabilities in a population-based birth cohort. Anesthesiology 2009; 111: 302-310.
38. Tsuchimoto T, Ueki M, Miki T, et al,. Erythropoietin attenuates isoflurane-induced neurodegeneration and learning deficits in the developing mouse brain. Pediatr Anesth 2011; 21: 1209-1213.
39. Gulinello M, Gertner M, Mendoza G, et al,. Validation of a 2-day water maze protocol in mice. Behav Brain Res 2009; 23: 220-227.
40. Saab BJ, Saab AM, Roder JC,. Statistical and theoretical considerations for the platform re-location water maze. J Neurosci Methods 2011; 15: 44-52.
41. Sun Y, Calvert JW, Zhang JH,. Neonatal hypoxia/ischemia is associated with decreased inflammatory mediators after erythropoietin administration. Stroke 2005; 36: 1672-1678.
42. Spandou E, Papadopoulou Z, Soubasi V, et al,. Erythropoietin prevents long-term sensorimotor deficits and brain injury following neonatal hypoxia-ischemia in rats. Brain Res 2005; 1045: 22-30.
43. Demers EJ, McPherson RJ, Juul SE,. Erythropoietin protects dopaminergic neurons and improves neurobehavioral outcomes in juvenile rats after neonatal hypoxia-ischemia. Pediatr Res 2005; 58: 297-301.
44. Kumral A, Uysal N, Tugyan K, et al,. Erythropoietin improves long-term spatial memory deficits and brain injury following neonatal hypoxia-ischemia in rats. Behav Brain Res 2004; 153: 77-86.
45. Sanders RD, Sun P, Patel S, et al,. Dexmedetomidine provides cortical neuroprotection: impact on anaesthetic-induced neuroapoptosis in the rat developing brain. Acta Anaesthesiol Scand 2010; 54: 710-716.
46. Loepke AW, Soriano SG,. An assessment of the effects of general anesthetics on developing brain structure and neurocognitive function. Anesth Analg 2008; 106: 1681-1707.
47. Istaphanous GK, Loepke AW,. General anesthetics and the developing brain. Curr Opin Anaesthesiol 2009; 22: 368-373.
48. Yon JH, Daniel-Johnson J, Carter LB, et al,. Anesthesia induces neuronal cell death in the developing rat brain via the intrinsic and extrinsic apoptotic pathways. Neuroscience 2005; 135: 815-827.
49. Yon JH, Carter LB, Reiter RJ, et al,. Melatonin reduces the severity of anesthesia-induced apoptotic neurodegeneration in the developing brain. Neurobiol Dis 2006; 21: 522-530.
50. Zhou X, Song FH, He W, et al,. Neonatal exposure to sevoflurane causes apoptosis and reduces nNOS protein expression in rat hippocampus. Mol Med Rep 2012; 6: 543-546.
51. Fang F, Xue Z, Cang J,. Sevoflurane exposure in 7-day-old rats affects neurogenesis, neurodegeneration and neurocognitive function. Neurosci Bull 2012; 28: 499-508.
52. Wei L, Han BH, Li Y, et al,. Cell death mechanism and protective effect of erythropoietin after focal ischemia in the whisker-barrel cortex of neonatal rats. J Pharmacol Exp Ther 2006; 317: 109-116.
53. Kaindl AM, Sifringer M, Koppelstaetter A, et al,. Erythropoietin protects the developing brain from hyperoxia-induced cell death and proteome changes. Ann Neurol 2008; 64: 523-534.
54. Dzietko M, Felderhoff-Mueser U, Sifringer M, et al,. Erythropoietin protects the developing brain against N-methyl-D-aspartate receptor antagonist neurotoxicity. Neurobiol Dis 2004 Mar; 15: 177-187.
55. Viviani B, Bartesaghi S, Corsini E, et al,. Erythropoietin protects primary hippocampal neurons increasing the expression of brain-derived neurotrophic factor. J Neurochem 2005; 93: 412-421.
56. Bibel M, Barde YA,. Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev 2000; 14: 2919-2937.
57. Almeida RD, Manadas BJ, Melo CV, et al,. Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ 2005; 12: 1329-1343.
58. Husson I, Rangon CM, Lelièvre V, et al,. BDNF-induced white matter neuroprotection and stage-dependent neuronal survival following a neonatal excitotoxic challenge. Cereb Cortex 2005; 15: 250-261.
59. Nguyen TL, Kim CK, Cho JH, et al. Neuroprotection signaling pathway of nerve growth factor and brain-derived neurotrophic factor against staurosporine induced apoptosis in hippocampal H19-7/IGF-IR. Exp Mol Med 2010; 42: 583-595. Erratum in: Exp Mol Med 2010; 42:798
60. Fauchère JC, Dame C, Vonthein R, et al. An approach to using recombinant erythropoietin for neuroprotection in very preterm infants. Pediatrics 2008; 122: 375-382.
61. Juul SE, McPherson RJ, Bauer LA, et al. A phase I/II trial of high-dose erythropoietin in extremely low birth weight infants: pharmacokinetics and safety. Pediatrics 2008; 122: 383-391.
62. McAdams RM, McPherson RJ, Mayock DE, et al. Outcomes of extremely low birth weight infants given early high-dose erythropoietin. J Perinatol 2012; 33: 226-230.
63. Elmahdy H, El-Mashad AR, El-Bahrawy H, et al. Human recombinant erythropoietin in asphyxia neonatorum: pilot trial. Pediatrics 2010; 125: e1135-e1142.
64. McPherson RJ, Demers EJ, Juul SE,. Safety of high-dose recombinant erythropoietin in a neonatal rat model. Neonatology 2007; 91: 36-43.
65. Ohlsson A, Aher SM,. Early erythropoietin for preventing red blood cell transfusion in preterm and/or low birth weight infants. Cochrane Database Syst Rev 2006; 19: CD004863.
66. Cameron CB, Robinson S, Gregory GA,. The minimum anesthetic concentration of isoflurane in children. Anesth Analg 1984; 63: 418-420.
67. Taylor RH, Lerman J,. Minimum alveolar concentration of desflurane and hemodynamic responses in neonates, infants, and children. Anesthesiology 1991; 75: 975-979.