Propofol exposure in pregnant rats induces neurotoxicity and persistent learning deficit in the offspring

Brain Sciences

Volumn 4, Issue 2, 2014, Pages 356-375

  Xiong, Ming ^a   Li, Jing ^a   Alhashem, Hussain M ^a   Tilak, Vasanti ^a   Patel, Anuradha ^a   Pisklakov, Sergey ^a   Siegel, Allan ^a   Ye, Jiang Hong ^a   Bekker, Alex ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Learning deficit; Neurotoxicity; Offspring; Prenatal exposure; Propofol

Indexed keywords

CASPASE 3; NEURON SPECIFIC NUCLEAR PROTEIN; PROPOFOL; PROTEIN P28; SYNAPTOPHYSIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; DRUG EXPOSURE; FEMALE; GESTATIONAL AGE; HABITUATION; HIPPOCAMPUS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LEARNING DISORDER; NEUROTOXICITY; NONHUMAN; OPEN FIELD TEST; OXYGEN SATURATION; PREGNANT WOMAN; PROGENY; PULSE OXIMETER; RAT; SPATIAL LEARNING; VAGINAL DELIVERY; WESTERN BLOTTING;

EID: 84919866811     PISSN: None     EISSN: 20763425     Source Type: Journal    
DOI: 10.3390/brainsci4020356     Document Type: Article

References (37)

1. Kotani, Y.; Shimazawa, M.; Yoshimura, S.; Iwama, T.; Hara, H. The experimental and clinical pharmacology of propofol, an anesthetic agent with neuroprotective properties. CNS Neurosci. Ther. 2008, 14, 95-106
2. Olsen, E.A.; Brambrink, A.M. Anesthetic neurotoxicity in the newborn and infant. Curr. Opin. Anaesthesiol. 2013, doi:10.1097/01.aco.0000433061.59939.b7
3. Creeley, C.E.; Dikranian, K.T.; Dissen, G.A.; Back, S.A.; Olney, J.W.; Brambrink, A.M. Isoflurane-induced Apoptosis of Neurons and Oligodendrocytes in the Fetal Rhesus Macaque Brain. Anesthesiology 2013, doi:10.1097/ALN.0000000000000037
4. Jevtovic-Todorovic, V. Pediatric anesthesia neurotoxicity: An overview of the 2011 SmartTots panel. Anesth. Analg. 2011, 113, 965-968
5. Van de Velde, M.; de Buck, F. Anesthesia for non-obstetric surgery in the pregnant patient. Minerva Anestesiol. 2007, 73, 235-240
6. Palanisamy, A.; Baxter, M.G.; Keel, P.K.; Xie, Z.; Crosby, G.; Culley, D.J. Rats exposed to isoflurane in utero during early gestation are behaviorally abnormal as adults. Anesthesiology 2011, 114, 521-528
7. Kong, F.J.; Xu, L.; He, D.; Zhang, X.; Lu, H. Effects of gestational isoflurane exposure on postnatal memory and learning in rats. Eur. J. Pharmacol. 2011, 670, 168-174
8. Dupret, D.; O'Neill, J.; Csicsvari, J. Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning. Neuron 2013, 78, 166-180
9. Dupret, D.; Fabre, A.; Döbrössy, M.D.; Panatier, A.; Rodríguez, J.J.; Lamarque, S.; Lemaire, V.; Oliet, S.H.; Piazza, P.V.; Abrous, D.N. Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol. 2007, 5, e214
10. Edelmann, L.; Hanson, P.I.; Chapman, E.R.; Jahn, R. Synaptobrevin binding to synaptophysin: A potential mechanism for controlling the exocytotic fusion machine. EMBO J. 1995, 14, 224-231
11. Grosse, G.; Tapp, R.; Wartenberg, M.; Sauer, H.; Fox, P.A.; Grosse, J.; Gratzl, M.; Bergmann, M. Prenatal hippocampal granule cells in primary cell culture form mossy fiber boutons at pyramidal cell dendrites. J. Neurosci. Res. 1998, 51, 602-611
12. Voigt, T.; de Lima, A.D.; Beckmann, M. Synaptophysin immunohistochemistry reveals inside-out pattern of early synaptogenesis in ferret cerebral cortex. J. Comp. Neurol. 1993, 330, 48-64
13. Lavezzi, A.M.; Corna, M.F.; Matturri, L. Neuronal nuclear antigen (NeuN): A useful marker of neuronal immaturity in sudden unexplained perinatal death. J. Neurol. Sci. 2013, 329, 45-50
14. Mullen, R.J.; Buck, C.R.; Smith, A.M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992, 116, 201-211
15. Yang, G.; Chang, P.C.; Bekker, A.; Blanck, T.J.; Gan, W.B. Transient effects of anesthetics on dendritic spines and filopodia in the living mouse cortex. Anesthesiology 2011, 115, 718-726
16. Li, Y.; Liang, G.; Wang, S.; Meng, Q.; Wang, Q.; Weia, H. Effects of fetal exposure to isoflurane on postnatal memory and learning in rats. Neuropharmacology 2007, 53, 942-950
17. Cattano, D.; Young, C.; Straiko, M.M.; Olney, J.W. Subanesthetic doses of propofol induce neuroapoptosis in the infant mouse brain. Anesth. Analg. 2008, 106, 1712-1714
18. Yu, D.; Jiang, Y.; Gao, J.; Liu, B.; Chen, P. Repeated exposure to propofol potentiates neuroapoptosis and long-term behavioral deficits in neonatal rats. Neurosci. Lett. 2013, 534, 41-46
19. Pearn, M.L.; Hu, Y.; Niesman, I.R.; Patel, H.H.; Drummond, J.C.; Roth, D.M.; Akassoglou, K.; Patel, P.M.; Head, B.P. Propofol neurotoxicity is mediated by p75 neurotrophin receptor activation. Anesthesiology 2012, 116, 352-361
20. Creeley, C.; Dikranian, K.; Dissen, G.; Martin, L.; Olney, L.; Brambrink, A. Propofol-induced apoptosis of neurones and oligodendrocytes in fetal and neonatal rhesus macaque brain. Br. J. Anaesth. 2013, 110 (Suppl. 1), i29-i38
21. Vutskits, L.; Gascon, E.; Tassonyi, E.; Kiss, J.Z. Clinically relevant concentrations of propofol but not midazolam alter in vitro dendritic development of isolated γ-aminobutyric acid-positive interneurons. Anesthesiology 2005, 102, 970-976
22. Nunez, J.L.; Alt, J.J.; McCarthy, M.M. A novel model for prenatal brain damage. II. Long-term deficits in hippocampal cell number and hippocampal-dependent behavior following neonatal GABAA receptor activation. Exp. Neurol. 2003, 181, 270-280
23. Olton, D.S.; Walker, J.A.; Gage, F.H. Hippocampal connections and spatial discrimination. Brain Res. 1978, 139, 295-308
24. Xia, L.; Jiang, Z.L.; Wang, G.H.; Hu, B.Y.; Ke, K.F. Treatment with ginseng total saponins reduces the secondary brain injury in rat after cortical impact. J. Neurosci. Res. 2012, 90, 1424-1436
25. Li, J.; Sun, Y.; Ye, J.H. Electroacupuncture decreases excessive alcohol consumption involving reduction of FosB/DeltaFosB levels in reward-related brain regions. PLoS One 2012, 7, e40347
26. Li, J.; Cheng, Y.; Bian, W.; Liu, X.; Zhang, C.; Ye, J.H. Region-specific induction of FosB/ΔFosB by voluntary alcohol intake: Effects of naltrexone. Alcohol. Clin. Exp. Res. 2010, 34, 1742-1750
27. Zheng, H.; Dong, Y.; Xu, Z.; Crosby, G.; Culley, D.J.; Zhang, Y.; Xie, Z. Sevoflurane anesthesia in pregnant mice induces neurotoxicity in fetal and offspring mice. Anesthesiology 2013, 118, 516-526
28. Liu, P.; Bilkey, D.K. The effect of excitotoxic lesions centered on the perirhinal cortex in two versions of the radial arm maze task. Behav. Neurosci. 1999, 113, 672-682
29. Soylemezoglu, F.; Onder, S.; Tezel, G.G.; Berker, M. Neuronal nuclear antigen (NeuN): A new tool in the diagnosis of central neurocytoma. Pathol. Res. Pract. 2003, 199, 463-468
30. Popic, J.; Pesic, V.; Milanovic, D.; Todorovic, S.; Kanazir, S.; Jevtovic-Todorovic, V.; Ruzdijic, S. Propofol-induced changes in neurotrophic signaling in the developing nervous system in vivo. PLoS One 2012, 7, e34396
31. Kahraman, S.; Zup, S.L.; McCarthy, M.M.; Fiskum, G. GABAergic mechanism of propofol toxicity in immature neurons. J. Neurosurg. Anesthesiol. 2008, 20, 233-240
32. Sanchez-Alcaraz, A.; Quintana, M.B.; Laguarda, M. Placental transfer and neonatal effects of propofol in caesarean section. J. Clin. Pharm. Ther. 1998, 23, 19-23
33. Briner, A.; Nikonenko, I.; de Roo, M.; Dayer, A.; Muller, D.; Vutskits, L. Developmental Stage-dependent persistent impact of propofol anesthesia on dendritic spines in the rat medial prefrontal cortex. Anesthesiology 2011, 115, 282-293
34. Whishaw, I.Q.; Rod, M.R.; Auer, R.N. Behavioral deficits revealed by multiple tests in rats with ischemic damage limited to half of the CA1 sector of the hippocampus. Brain Res. Bull. 1994, 34, 283-289
35. Brambrink, A.M.; Evers, A.S.; Avidan, M.S.; Farber, N.B.; Smith, D.J.; Martin, L.D.; Dissen, G.A.; Creeley, C.E.; Olney, J.W. Ketamine-induced neuroapoptosis in the fetal and neonatal rhesus macaque brain. Anesthesiology 2012, 116, 372-384
36. Stratmann, G. Review article: Neurotoxicity of anesthetic drugs in the developing brain. Anesth. Analg. 2011, 113, 1170-1179
37. Jevtovic-Todorovic, V. Anesthesia and the developing brain: Are we getting closer to understanding the truth? Curr. Opin. Anaesthesiol. 2011, 24, 395-399.