Effect of Hypercarbia and Isoflurane on Brain Cell Death and Neurocognitive Dysfunction in 7-day-old Rats

Anesthesiology

Volumn 110, Issue 4, 2009, Pages 849-861

  Stratmann, Greg ^a,b   May, Laura D V ^a   Sall, Jeffrey W ^a   Alvi, Rehan S ^a   Bell, Joseph S ^a   Ormerod, Brandi K ^c   Rau, Vinuta ^a   Hilton, Joan F ^b   Dai, Ran ^a   Lee, Michael T ^a   Visrodia, Kavel H ^a   Ku, Ban ^a   Zusmer, Emanuel J ^a   Guggenheim, Jeremy ^a   Firouzian, Atoosa ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANESTHETIC AGENT; CARBON DIOXIDE; ISOFLURANE; INHALATION ANESTHETIC AGENT;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; BRAIN DYSFUNCTION; CELL DEATH; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; HYPERCAPNIA; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REFERENCE MEMORY; WORKING MEMORY; ANIMAL; BLOOD GAS ANALYSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHEMICALLY INDUCED DISORDER; CONDITIONING; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; FEAR; MEMORY DISORDER; NERVE CELL; SPRAGUE DAWLEY RAT; SURVIVAL RATE; TIME; TREATMENT OUTCOME;

ANESTHETICS, INHALATION; ANIMALS; BLOOD GAS ANALYSIS; CARBON DIOXIDE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONDITIONING (PSYCHOLOGY); DOSE-RESPONSE RELATIONSHIP, DRUG; FEAR; FEMALE; ISOFLURANE; MALE; MEMORY DISORDERS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SURVIVAL RATE; TIME FACTORS; TREATMENT OUTCOME;

EID: 65349116529     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e31819c7140     Document Type: Article

References (62)

1. Loepke AW, Soriano SG: An assessment of the effects of general anesthetics on developing brain structure and neurocognitive function. Anesth Analg 2008; 106:1681-707
2. Anand KJ, Soriano SG: Anesthetic agents and the immature brain: Are these toxic or therapeutic? ANESTHESIOLOGY 2004; 101:527-30
3. Jevtovic-Todorovic V, Hartman RE, Izumi Y, Benshoff ND, Dikranian K, Zorumski CF, Olney JW, Wozniak DF: Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deícits. J Neurosci 2003; 23:876-82
4. Slikker W Jr, Zou X, Hotchkiss CE, Divine RL, Sadovova N, Twaddle NC, Doerge DR, Scallet AC, Patterson TA, Hanig JP, Paule MG, Wang C: Ketamine-induced neuronal cell death in the perinatal rhesus monkey. Toxicol Sci 2007; 98:145-58
5. Fredriksson A, Archer T, Alm H, Gordh T, Eriksson P: Neurofunctional deícits and potentiated apoptosis by neonatal NMDA antagonist administration. Behav Brain Res 2004; 153:367-76
6. Fredriksson A, Ponten E, Gordh T, Eriksson P: 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 deícits. ANESTHESIOLOGY 2007; 107:427-36
7. Mellon RD, Simone AF, Rappaport BA: Use of anesthetic agents in neonates and young children. Anesth Analg 2007; 104:509-20
8. Fendt M, Fanselow MS: The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev 1999; 23:743-60
9. Fanselow MS, Poulos AM: The neuroscience of mammalian associative learning. Annu Rev Psychol 2005; 56:207-34
10. Fanselow MS, LeDoux JE: Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 1999; 23:229-32
11. Maren S, Fanselow MS: The amygdala and fear conditioning: has the nut been cracked? Neuron 1996; 16:237-40
12. Kim JJ, Fanselow MS: Modality-speciíc retrograde amnesia of fear. Science 1992; 256:675-7
13. Phillips RG, LeDoux JE: Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992; 106:274-85
14. Sutherland RJ, Kolb B, Whishaw IQ: Spatial mapping: Deínitive disruption by hippocampal or medial frontal cortical damage in the rat. Neurosci Lett 1982; 31:271-6
15. Morris RG, Garrud P, Rawlins JN, OKeefe J: Place navigation impaired in rats with hippocampal lesions. Nature 1982; 297:681-3
16. Block AE, Dhanji H, Thompson-Tardif SF, Floresco SB: Thalamic-prefrontal cortical-ventral striatal circuitry mediates dissociable components of strategy set shifting. Cereb Cortex 2007; 17:1625-36
17. Duva CA, Floresco SB, Wunderlich GR, Lao TL, Pinel JP, Phillips AG: Disruption of spatial but not object-recognition memory by neurotoxic lesions of the dorsal hippocampus in rats. Behav Neurosci 1997; 111:1184-96
18. Floresco SB, Braaksma DN, Phillips AG: Thalamic-cortical-striatal circuitry subserves working memory during delayed responding on a radial arm maze. J Neurosci 1999; 19:11061-71
19. Floresco SB, Grace AA: Gating of hippocampal-evoked activity in prefrontal cortical neurons by inputs from the mediodorsal thalamus and ventral tegmental area. J Neurosci 2003; 23:3930-43
20. Stratmann G, Sall JW, May LDV, Bell JS, Magnusson KR, Rau V, Visrodia KH, Alvi RS, Ku B, Lee MT, Dai R: Isołurane differentially affects neurogenesis and long-term neurocognitive function in 60-day-old and 7-day old rats. ANESTHESIOLOGY 2009; 110:834-48
21. Pepelko WE, Dixon GA: Arterial blood gases in conscious rats exposed to hypoxia, hypercapnia, or both. J Appl Physiol 1975; 38:581-7
22. th edition. Sydney, Academic Press, 2005
23. Whishaw IQ: Cholinergic receptor blockade in the rat impairs locale but not taxon strategies for place navigation in a swimming pool. Behav Neurosci 1985; 99:979-1005
24. Whishaw IQ, Mittleman G, Bunch ST, Dunnett SB: Impairments in the acquisition, retention and selection of spatial navigation strategies after medial caudate-putamen lesions in rats. Behav Brain Res 1987; 24:125-38
25. Aggleton JP, Brown MW: Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci 1999; 22:425-44
26. Wang C, Sadovova N, Hotchkiss C, Fu X, Scallet AC, Patterson TA, Hanig J, Paule MG, Slikker W Jr: Blockade of N-methyl-D-aspartate receptors by ketamine produces loss of postnatal day 3 monkey frontal cortical neurons in culture. Toxicol Sci 2006;91: 192-201
27. Young C, Jevtovic-Todorovic V, Qin YQ, Tenkova T, Wang H, Labruyere J, Olney JW: Potential of ketamine and midazolam, individually or in combination, to induce apoptotic neurodegeneration in the infant mouse brain. Br J Pharmacol 2005; 146:189-97
28. Rizzi S, Carter LB, Jevtovic-Todorovic V: Clinically used general anesthetics induce neuroapoptosis in the developing piglet brain (abstract). Soc Neurosci Abst 2005; 251.7
29. Johnson SA, Young C, Olney JW: Isołurane-induced neuroapoptosis in the developing brain of nonhypoglycemic mice. J Neurosurg Anesthesiol 2008; 20:21-8
30. Stein V, Hermans-Borgmeyer I, Jentsch TJ, Hubner CA: Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 2004; 468:57-64
31. Oppenheim RW: Cell death during development of the nervous system. Annu Rev Neurosci 1991; 14:453-501
32. Oppenheim RW, Prevette D, Yin QW, Collins F, MacDonald J: Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science 1991; 251:1616-8
33. Kolb B, Sutherland RJ, Whishaw IQ: A comparison of the contributions of the frontal and parietal association cortex to spatial localization in rats. Behav Neurosci 1983; 97:13-27
34. Keith JR, Wu Y, Epp JR, Sutherland RJ: Fluoxetine and the dentate gyrus: Memory, recovery of function, and electrophysiology. Behav Pharmacol 2007; 18:521-31
35. Zhang CL, Zou Y, He W, Gage FH, Evans RM: A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 2008; 451:1004-7
36. Dupret D, Revest JM, Koehl M, Ichas F, De Giorgi F, Costet P, Abrous DN, Piazza PV: Spatial relational memory requires hippocampal adult neurogenesis. PLoS ONE 2008; 3:e1959
37. Sonner JM, Antognini JF, Dutton RC, Flood P, Gray AT, Harris RA, Homanics GE, Kendig J, Orser B, Raines DE, Rampil IJ, Trudell J, Vissel B, Eger EI 2nd: Inhaled anesthetics and immobility: mechanisms, mysteries, and minimum alveolar anesthetic concentration. Anesth Analg 2003;97: 718-40
38. Ieraci A, Herrera DG: Single alcohol exposure in early life damages hippocampal stem/progenitor cells and reduces adult neurogenesis. Neurobiol Dis 2007; 26:597-605
39. Klintsova AY, Helfer JL, Calizo LH, Dong WK, Goodlett CR, Greenough WT: Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure. Alcohol Clin Exp Res 2007; 31: 2073-82
40. Vutskits L, Gascon E, Potter G, Tassonyi E, Kiss JZ: Low concentrations of ketamine initiate dendritic atrophy of differentiated GABAergic neurons in culture. Toxicology 2007; 234:216-26
41. Vutskits L, Gascon E, Tassonyi E, Kiss JZ: Clinically relevant concentrations of propofol but not midazolam alter in vitro dendritic development of isolated gamma-aminobutyric acid-positive interneurons. ANESTHESIOLOGY 2005; 102:970-6
42. Vutskits L, Gascon E, Tassonyi E, Kiss JZ: Effect of ketamine on dendritic arbor development and survival of immature GABAergic neurons in vitro. Toxicol Sci 2006; 91:540-9
43. Patel P, Head B, Patel H, Drummond J, Roth D: Tpa reduces isołurane induced neuronal apoptosis and dendritic spines loss in rat neonatal neurons (abstract). ANESTHESIOLOGY 2008; 109:A1413
44. Vutskits L, De Roo M, Klauser P, Briner A, Muller D: Anesthetics impair dendritic spine development in the postnatal mouse somatosensory cortex (abstract). ANESTHESIOLOGY 2008; 109:A325
45. Scallet AC, Schmued LC, Slikker W Jr, Grunberg N, Faustino PJ, Davis H, Lester D, Pine PS, Sistare F, Hanig JP: Developmental neurotoxicity of ketamine: Morphometric conírmation, exposure parameters, and multiple łuorescent labeling of apoptotic neurons. Toxicol Sci 2004; 81:364-70
46. Schmued LC, Albertson C, Slikker W Jr: Fluoro-Jade: A novel łuorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res 1997;751: 37-46
47. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vockler J, Dikranian K, Tenkova TI, Stefovska V, Turski L, Olney JW: Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 1999; 283:70-4
48. Ikonomidou C, Bittigau P, Ishimaru MJ, Wozniak DF, Koch C, Genz K, Price MT, Stefovska V, Horster F, Tenkova T, Dikranian K, Olney JW: Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 2000; 287:1056-60
49. Wang C, Sadovova N, Fu X, Schmued L, Scallet A, Hanig J, Slikker W: The role of the N-methyl-D-aspartate receptor in ketamine-induced apoptosis in rat forebrain culture. Neuroscience 2005; 132:967-77
50. Wise-Faberowski L, Zhang H, Ing R, Pearlstein RD, Warner DS: Isołurane-induced neuronal degeneration: an evaluation in organotypic hippocampal slice cultures. Anesth Analg 2005; 101:651-7
51. Wozniak DF, Hartman RE, Boyle MP, Vogt SK, Brooks AR, Tenkova T, Young C, Olney JW, Muglia LJ: Apoptotic neurodegeneration induced by ethanol in neonatal mice is associated with profound learning/memory deícits in juveniles followed by progressive functional recovery in adults. Neurobiol Dis 2004;17:403-14
52. Yon JH, Carter LB, Reiter RJ, Jevtovic-Todorovic V: Melatonin reduces the severity of anesthesia-induced apoptotic neurodegeneration in the developing rat brain. Neurobiol Dis 2006; 21:522-30
53. Yon JH, Daniel-Johnson J, Carter LB, Jevtovic-Todorovic V: Anesthesia induces neuronal cell death in the developing rat brain via the intrinsic and extrinsic apoptotic pathways. Neuroscience 2005; 135:815-27
54. Young C, Olney JW: Neuroapoptosis in the infant mouse brain triggered by a transient small increase in blood alcohol concentration. Neurobiol Dis 2006; 22:548-54
55. Webb SJ, Monk CS, Nelson CA: Mechanisms of postnatal neurobiological development: Implications for human development. Dev Neuropsychol 2001; 19:147-71
56. Dobbing J, Sands J: Comparative aspects of the brain growth spurt. Early Hum Dev 1979; 3:79-83
57. DeFelipe J, Marco P, Fairen A, Jones EG: Inhibitory synaptogenesis in mouse somatosensory cortex. Cereb Cortex 1997; 7:619-34
58. Crain B, Cotman C, Taylor D, Lynch G: A quantitative electron microscopic study of synaptogenesis in the dentate gyrus of the rat. Brain Res 1973; 63:195-204
59. Clancy B, Kersh B, Hyde J, Darlington RB, Anand KJ, Finlay BL: Web-based method for translating neurodevelopment from laboratory species to humans. Neuroinformatics 2007; 5:79-94
60. Overstreet-Wadiche LS, Bensen AL, Westbrook GL: Delayed development of adult-generated granule cells in dentate gyrus. J Neurosci 2006; 26:2326-34
61. Draguhn A, Heinemann U: Different mechanisms regulate IPSC kinetics in early postnatal and juvenile hippocampal granule cells. J Neurophysiol 1996; 76:3983-93
62. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R: GABA: A pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 2007; 87:1215-84