Neonatal Exposure to Sevoflurane Induces Abnormal Social Behaviors and Deficits in Fear Conditioning in Mice
Open accessAbstract
Background: Neonatal exposure to anesthetics that block N-methyl-D-aspartate receptors and/or hyperactivate gamma-aminobutyric acid type A receptor has been shown to cause neuronal degeneration in the developing brain, leading to functional deficits later in adulthood. The authors investigated whether exposure of neonatal mice to inhaled sevoflurane causes deficits in social behavior as well as learning disabilities. Methods: Six-day-old C57BL/6 mice were exposed to 3% sevoflurane for 6 h. Activated cleaved caspase-3 immunohistochemical staining was used for detection of apoptosis. Cognitive functions were tested by pavlovian conditioned fear test. Social behavior was tested by social recognition and interaction tests. Results: Neonatal exposure to sevoflurane significantly increased the number of apoptotic cells in the brain immediately after anesthesia. It caused persistent learning deficits later in adulthood as evidenced by decreased freezing response in both contextual and cued fear conditioning. The social recognition test demonstrated that mice with neonatal exposure to sevoflurane did not develop social memory. Furthermore, these mice showed decreased interactions with a social target compared with controls in the social interaction test, indicating a social interaction deficit. The authors did not attribute these abnormalities in social behavior to impairments of general interest in novelty or olfactory sensation, because they did not detect significant differences in the test for novel inanimate object interaction or for olfaction. Conclusions: This study shows that exposure of neonatal mice to inhaled sevoflurane could cause not only learning deficits but also abnormal social behaviors resembling autism spectrum disorder.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Interruption of neural activity during the critical period could cause deficits in brain functioning later in adulthood, including social deficits similar to ASD.
“Furthermore, these interruption could cause deficits in brain functioning later in adulthood6, including social deficits similar to those seen in autistic spectrum disorder (ASD)7.”
From Transient blockade of ERK phosphorylation in the critical period causes autistic phenotypes as an adult in mice (2015) · cites this paper as [7]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Neuronal Oscillations in Cortical Networks
Buzsáki, G., & Draguhn, A. (2004) · Science · doi:10.1126/science.1099745 · Cited by 6,576 · see citing works
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.2.274 · Cited by 3,292 · see citing works
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.2.274 · Cited by 3,262 · see citing works
Rice, D., & Barone, S. (2000) · Environmental Health Perspectives · doi:10.1289/ehp.00108s3511 · Cited by 2,944 · see citing works
Model of autism: increased ratio of excitation/inhibition in key neural systems
Rubenstein, J. L. R., & Merzenich, M. M. (2003) · Genes, Brain and Behavior · doi:10.1034/j.1601-183x.2003.00037.x · Cited by 2,768 · see citing works
Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE
Lazebnik, Y. A., Kaufmann, S. H., Desnoyers, S., Poirier, G. G., & Earnshaw, W. C. (1994) · Nature · doi:10.1038/371346a0 · Cited by 2,563 · see citing works
Comparative aspects of the brain growth spurt
Dobbing, J., & Sands, J. (1979) · Early Human Development · doi:10.1016/0378-3782(79)90022-7 · Cited by 2,506 · see citing works
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
Neural synchrony in brain disorders: Relevance for cognitive dysfunctions and pathophysiology
Uhlhaas, P. J., & Singer, W. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.020 · Cited by 2,194 · see citing works
Jevtovic-Todorovic, V., Hartman, R. E., Izumi, Y., Benshoff, N. D., Dikranian, K., Zorumski, C. F., Olney, J. W., & Wozniak, D. F. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-03-00876.2003 · Cited by 1,983 · see citing works
Ethanol-Induced Apoptotic Neurodegeneration and Fetal Alcohol Syndrome
Ikonomidou, C., Bittigau, P., Ishimaru, M. J., Wozniak, D. F., Koch, C. A., Genz, K., Price, M. T., Stefovska, V. G., Hörster, F., Tenkova, T., et al. (2000) · Science · doi:10.1126/science.287.5455.1056 · Cited by 1,357 · see citing works
Pten Regulates Neuronal Arborization and Social Interaction in Mice
Kwon, C.-H., Luikart, B. W., Powell, C. M., Zhou, J., Matheny, S. A., Zhang, W., Li, Y., Baker, S. J., & Parada, L. F. (2006) · Neuron · doi:10.1016/j.neuron.2006.03.023 · Cited by 970 · see citing works
Bayer, S. A., Altman, J., Russo, R. J., & Zhang, X. (1993) · PubMed · Cited by 912 · see citing works
CD38 is critical for social behaviour by regulating oxytocin secretion
Jin, D., Liu, H.-X., Hirai, H., Torashima, T., Nagai, T., Lopatina, O., Shnayder, N. A., Yamada, K., Noda, M., Seike, T., et al. (2007) · Nature · doi:10.1038/nature05526 · Cited by 665 · see citing works
The Pharmacology of Sevoflurane in Infants and Children
Lerman, J., Sikich, N., Kleinman, S., & Yentis, S. M. (1994) · Anesthesiology · doi:10.1097/00000542-199404000-00014 · Cited by 497 · see citing works
Young, C., Jevtović‐Todorović, V., Qin, Y.-Q., Tenkova, T. I., Wang, H., Labruyere, J., & Olney, J. W. (2005) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706301 · Cited by 470 · see citing works
Social interaction and sensorimotor gating abnormalities in mice lacking Dvl1
Lijam, N., Paylor, R., McDonald, M. P., Crawley, J. N., Deng, C.-X., Herrup, K., Stevens, K. E., Maccaferri, G., McBain, C. J., Sussman, D. J., et al. (1997) · Cell · doi:10.1016/s0092-8674(00)80354-2 · Cited by 470 · see citing works
Fredriksson, A., Pontén, E., Gordh, T., & Eriksson, P. (2007) · Anesthesiology · doi:10.1097/01.anes.0000278892.62305.9c · Cited by 419 · see citing works
Abnormalities of social interactions and home-cage behavior in a mouse model of Rett syndrome
Moretti, P. M., Bouwknecht, J. A., Teague, R. M., Paylor, R. E., & Zoghbi, H. Y. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddi016 · Cited by 343 · see citing works
Ethanol-induced apoptotic neurodegeneration in the developing C57BL/6 mouse brain
Olney, J. W., Tenkova, T. I., Dikranian, K. T., Qin, Y.-Q., Labruyere, J., & Ikonomidou, C. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00279-1 · Cited by 305 · see citing works
Wozniak, D. F., Hartman, R. E., Boyle, M. A., Vogt, S. K., Brooks, A., Tenkova, T. I., YOUNG, C., Olney, J. W., & Muglia, L. J. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.08.006 · Cited by 302 · see citing works
van Boxel-Dezaire, A. H. H., Hoff, S. C. J., van Oosten, B. W., Verweij, C. L., Dräger, A. M., Adèr, H. J., van Houwelingen, H. C., Barkhof, F., Polman, C. H., & Nagelkerken, L. M. (1999) · Annals of Neurology · doi:10.1002/1531-8249(199906)45:6 · Cited by 266 · see citing works
General anesthesia activates BDNF-dependent neuroapoptosis in the developing rat brain
Lu, L. X., Yon, J. H., Carter, L. B., & Jevtović‐Todorović, V. (2006) · APOPTOSIS · doi:10.1007/s10495-006-8762-3 · Cited by 236 · see citing works
Toward a developmental neurobiology of autism
Polleux, F., & Lauder, J. M. (2004) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.20044 · Cited by 216 · see citing works
Satoh, Y., Endo, S., Ikeda, T., Yamada, K., Ito, M., Kuroki, M., Hiramoto, T., Imamura, O., Kobayashi, Y., Watanabe, Y., et al. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0117-07.2007 · Cited by 162 · see citing works
Self-citationIsoflurane-induced Neuroapoptosis in the Developing Brain of Nonhypoglycemic Mice
Johnson, S. A., Young, C., & Olney, J. W. (2008) · Journal of Neurosurgical Anesthesiology · doi:10.1097/ana.0b013e3181271850 · Cited by 161 · see citing works
Hollmann, M. W., Liu, H.-T., Hönemann, C., Liu, W., & Durieux, M. E. (2001) · Anesthesia & Analgesia · doi:10.1097/00000539-200105000-00020 · Cited by 147 · see citing works
Bishop, S., Gahagan, S., & Lord, C. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2007.01782.x · Cited by 143 · cited 1× · see citing works
“In this regard, it is noteworthy that there is evidence that prenatal exposure to ethanol may be a factor in social difficulties in humans.(33) Further research, including electrophysiologic study, will be needed to address the molecular mechanisms that explain the relevance between neonatal exposure to sevoflurane an…”
BackgroundThe Actions of Sevoflurane and Desflurane on the γ-Aminobutyric Acid Receptor Type A
Nishikawa, K., & Harrison, N. L. (2003) · Anesthesiology · doi:10.1097/00000542-200309000-00024 · Cited by 121 · see citing works
Early caspase‐3 activation independent of apoptosis is required for cellular function
Rosado, J. A., López, J. J., Gómez-Arteta, E., Redondo, P. C., Salido, G. M., & Pariente, J. A. (2006) · Journal of Cellular Physiology · doi:10.1002/jcp.20715 · Cited by 87 · see citing works
A question of balance: a proposal for new mouse models of autism
Murcia, C. L., Gulden, F. O., & Herrup, K. (2004) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.07.001 · Cited by 50 · see citing works
Histogenesis of the Intravitreal Membrane and Secondary Vitreous in the Mouse
Ito, M., Nakashima, M., Tsuchida, N., Imaki, J., & Yoshioka, M. (2007) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.06-0325 · Cited by 7 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 2
- Bittigau P, Sifringer M, Pohl D, Stadthaus D, Ishimaru M, Shimizu H, Ikeda M, Lang D, Speer A, Olney JW, Ikonomidou C: Apoptotic neurodegeneration following trauma is markedly enhanced in the immature brain. Ann Neurol 1999; 45:724-35
- Hussman JP: Suppressed GABAergic inhibition as a common factor in suspected etiologies of autism. Autism Dev Disord 2001; 2:247-8
Cited by
Sorted by citations
Sun, L. S., Li, G., Miller, T. L. K., Salorio, C., Byrne, M. W., Bellinger, D. C., Ing, C., Park, R., Radcliffe, J., Hays, S. R., et al. (2016) · JAMA · doi:10.1001/jama.2016.6967 · Cited by 949 · see citing works
Long-term Differences in Language and Cognitive Function After Childhood Exposure to Anesthesia
Ing, C. H., DiMaggio, C. J., Whitehouse, A., Hegarty, M. K., Brady, J. E., von Ungern-Sternberg, B. S., Davidson, A. J., Wood, A. J. J., Li, G., & Sun, L. S. (2012) · PEDIATRICS · doi:10.1542/peds.2011-3822 · Cited by 605 · see citing works
Isoflurane-induced Neuroapoptosis in the Neonatal Rhesus Macaque Brain
Brambrink, A. M., Evers, A. S., Avidan, M. S., Farber, N. B., Smith, D. J., Zhang, X., Dissen, G. A., Creeley, C. E., & Olney, J. W. (2010) · Anesthesiology · doi:10.1097/aln.0b013e3181d049cd · Cited by 587 · see citing works
Paule, M. G., Li, M., Allen, R. R., Liu, F., Zou, X., Hotchkiss, C. E., Hanig, J. P., Patterson, T. A., Slikker, W., & Wang, C. (2011) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2011.01.001 · Cited by 570 · see citing works
Creeley, C. E., Dikranian, K. T., Dissen, G. A., Martin, L., Olney, J. W., & Brambrink, A. M. (2013) · British Journal of Anaesthesia · doi:10.1093/bja/aet173 · Cited by 466 · see citing works
Ketamine-induced Neuroapoptosis in the Fetal and Neonatal Rhesus Macaque Brain
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. (2012) · Anesthesiology · doi:10.1097/aln.0b013e318242b2cd · Cited by 427 · see citing works
Selective Anesthesia-induced Neuroinflammation in Developing Mouse Brain and Cognitive Impairment
Shen, X., Dong, Y., Xu, Z., Wang, H., Miao, C., Soriano, S. G., Sun, D., Baxter, M. G., Zhang, Y., & Xie, Z. (2013) · Anesthesiology · doi:10.1097/aln.0b013e3182834d77 · Cited by 393 · see citing works
Early childhood general anaesthesia exposure and neurocognitive development
Sun, L. S. (2010) · British Journal of Anaesthesia · doi:10.1093/bja/aeq302 · Cited by 364 · see citing works
Mahmoud, M., & Mason, K. P. (2015) · British Journal of Anaesthesia · doi:10.1093/bja/aev226 · Cited by 363 · see citing works
Academic Performance in Adolescence after Inguinal Hernia Repair in Infancy
Hansen, T. G., Pedersen, J. K., Henneberg, S. W., Pedersen, D. A., Murray, J. C., Morton, N. S., & Christensen, K. (2011) · Anesthesiology · doi:10.1097/aln.0b013e31820e77a0 · Cited by 315 · see citing works
Association of Anesthesia and Surgery During Childhood With Long-term Academic Performance
Glatz, P., Sandin, R., Pedersen, N. L., Bonamy, A. E., Eriksson, L. I., & Granath, F. N. (2016) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2016.3470 · Cited by 278 · see citing works
Istaphanous, G. K., Howard, J., Nan, X., Hughes, E. A., McCann, J., McAuliffe, J. J., Danzer, S. C., & Loepke, A. W. (2011) · Anesthesiology · doi:10.1097/aln.0b013e3182084a70 · Cited by 268 · see citing works
Isoflurane‐induced apoptosis of oligodendrocytes in the neonatal primate brain
Brambrink, A. M., Back, S. A., Riddle, A., Gong, X., Moravec, M. D., Dissen, G. A., Creeley, C. E., Dikranian, K. T., & Olney, J. W. (2012) · Annals of Neurology · doi:10.1002/ana.23652 · Cited by 264 · see citing works
Zhang, Y., Xu, Z., Wang, H., Dong, Y., Shi, H. N., Culley, D. J., Crosby, G. J., Marcantonio, E. R., Tanzi, R. E., & Xie, Z. (2012) · Annals of Neurology · doi:10.1002/ana.23536 · Cited by 239 · see citing works
Sleep disturbance induces neuroinflammation and impairment of learning and memory
Zhu, B., Dong, Y., Xu, Z., Gompf, H. S., Ward, S. A. P., Xue, Z., Miao, C., Zhang, Y., Chamberlin, N. L., & Xie, Z. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.06.022 · Cited by 226 · see citing works
Isoflurane-induced Apoptosis of Neurons and Oligodendrocytes in the Fetal Rhesus Macaque Brain
Creeley, C. E., Dikranian, K. T., Dissen, G. A., Back, S. A., Olney, J. W., & Brambrink, A. M. (2013) · Anesthesiology · doi:10.1097/aln.0000000000000037 · Cited by 224 · see citing works
Impact of anaesthetics and surgery on neurodevelopment: an update
Sanders, R. D., Hassell, J. K., Davidson, A. J., Robertson, N. J., & Ma, D. (2013) · British Journal of Anaesthesia · doi:10.1093/bja/aet054 · Cited by 213 · see citing works
Liang, G., Ward, C., Peng, J., Zhao, Y., Huang, B., & Wei, H. (2010) · Anesthesiology · doi:10.1097/aln.0b013e3181d94da5 · Cited by 210 · see citing works
Anesthesia for Cesarean Delivery and Learning Disabilities in a Population-based Birth Cohort
Šprung, J., Flick, R. P., Wilder, R. T., Katusic, S. K., Pike, T. L., Dingli, M., Gleich, S. J., Schroeder, D. R., Barbaresi, W. J., Hanson, A. C., et al. (2009) · Anesthesiology · doi:10.1097/aln.0b013e3181adf481 · Cited by 203 · see citing works
Kodama, M., Satoh, Y., Otsubo, Y., Araki, Y., Yonamine, R., Masui, K., & Kazama, T. (2011) · Anesthesiology · doi:10.1097/aln.0b013e318234228b · Cited by 201 · see citing works
Self-citationMultiple Anesthetic Exposure in Infant Monkeys Alters Emotional Reactivity to an Acute Stressor
Raper, J., Alvarado, M. C., Murphy, K. L., & Baxter, M. G. (2015) · Anesthesiology · doi:10.1097/aln.0000000000000851 · Cited by 195 · see citing works
Lu, Y., Wu, X., Dong, Y., Xu, Z., Zhang, Y., & Xie, Z. (2010) · Anesthesiology · doi:10.1097/aln.0b013e3181d94de1 · Cited by 193 · see citing works
Chen, L., Dong, R., Lu, Y., Zhou, Y., Li, K., Zhang, Z., & Peng, M. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.01.020 · Cited by 185 · see citing works
Coleman, K., Robertson, N. D., Dissen, G. A., Neuringer, M. D., Martin, L., Carlson, V. C. C., Kroenke, C. D., Fair, D. A., & Brambrink, A. M. (2016) · Anesthesiology · doi:10.1097/aln.0000000000001383 · Cited by 173 · see citing works
Wang, X., Xu, Z., & Miao, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085760 · Cited by 168 · see citing works
Which Neuroprotective Agents are Ready for Bench to Bedside Translation in the Newborn Infant?
Robertson, N. J., Tan, S., Groenendaal, F., van Bel, F., Juul, S. E., Bennet, L., Derrick, M., Back, S. A., Chavez‐Valdez, R., Northington, F. J., et al. (2012) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2011.12.052 · Cited by 159 · see citing works
Delayed Environmental Enrichment Reverses Sevoflurane-induced Memory Impairment in Rats
Shih, J., May, L. D. V., Gonzalez, H., Lee, E. W., Alvi, R. S., Sall, J. W., Rau, V., Bickler, P. E., Lalchandani, G. R., Yusupova, M., et al. (2012) · Anesthesiology · doi:10.1097/aln.0b013e318247564d · Cited by 154 · see citing works
Amrock, L. G., Starner, M. L., Murphy, K. L., & Baxter, M. G. (2014) · Anesthesiology · doi:10.1097/aln.0000000000000477 · Cited by 151 · see citing works
Effect of General Anesthesia in Infancy on Long-Term Recognition Memory in Humans and Rats
Stratmann, G., Lee, J. K., Sall, J. W., Lee, B. H., Alvi, R. S., Shih, J., Rowe, A. M., Ramage, T. M., Chang, F. L., Alexander, T. G., et al. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.134 · Cited by 151 · see citing works
Ing, C. H., DiMaggio, C. J., Malacova, E., Whitehouse, A., Hegarty, M. K., Feng, T., Brady, J. E., von Ungern-Sternberg, B. S., Davidson, A. J., Wall, M. M., et al. (2014) · Anesthesiology · doi:10.1097/aln.0000000000000248 · Cited by 146 · see citing works
ERK2 Contributes to the Control of Social Behaviors in Mice
Satoh, Y., Endo, S., Nakata, T., Kobayashi, Y., Yamada, K., Ikeda, T., Takeuchi, A., Hiramoto, T., Watanabe, Y., & Kazama, T. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.2349-11.2011 · Cited by 145 · see citing works
Self-citationSevoflurane Induces Tau Phosphorylation and Glycogen Synthase Kinase 3β Activation in Young Mice
Tao, G., Zhang, J., Zhang, L., Dong, Y., Yu, B., Crosby, G. J., Culley, D. J., Zhang, Y., & Xie, Z. (2014) · Anesthesiology · doi:10.1097/aln.0000000000000278 · Cited by 143 · see citing works
Li, Y., Zeng, M.-T., Chen, W., Liu, C., Wang, F., Han, X., Zuo, Z., & Peng, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093639 · Cited by 142 · see citing works
Bumetanide Alleviates Epileptogenic and Neurotoxic Effects of Sevoflurane in Neonatal Rat Brain
Edwards, D. A., Shah, H. P., Cao, W., Gravenstein, N. L., Seubert, C. N., & Martynyuk, A. E. (2010) · Anesthesiology · doi:10.1097/aln.0b013e3181cf9138 · Cited by 141 · see citing works
Propofol Neurotoxicity Is Mediated by p75 Neurotrophin Receptor Activation
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. (2011) · Anesthesiology · doi:10.1097/aln.0b013e318242a48c · Cited by 139 · see citing works
Perez‐Zoghbi, J. F., Zhu, W., Grafe, M. R., & Brambrink, A. M. (2017) · British Journal of Anaesthesia · doi:10.1093/bja/aex222 · Cited by 138 · see citing works
Learning, memory and synaptic plasticity in hippocampus in rats exposed to sevoflurane
Xiao, H., Liu, B., Chen, Y., & Zhang, J. (2015) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2015.11.001 · Cited by 129 · see citing works
Rats Exposed to Isoflurane In Utero during Early Gestation Are Behaviorally Abnormal as Adults
Palanisamy, A., Baxter, M. G., Keel, P. K., Xie, Z., Crosby, G. J., & Culley, D. J. (2011) · Anesthesiology · doi:10.1097/aln.0b013e318209aa71 · Cited by 125 · see citing works
The Young: Neuroapoptosis Induced by Anesthetics and What to Do About It
Creeley, C. E., & Olney, J. W. (2010) · Anesthesia & Analgesia · doi:10.1213/ane.0b013e3181c6b9ca · Cited by 119 · see citing works
Molecular Hydrogen as a Neuroprotective Agent
Iketani, M., & Ohsawa, I. (2016) · Current Neuropharmacology · doi:10.2174/1570159x14666160607205417 · Cited by 118 · see citing works
Isoflurane Neurotoxicity Is Mediated by p75NTR-RhoA Activation and Actin Depolymerization
Lemkuil, B. P., Head, B. P., Pearn, M. L., Patel, H. H., Drummond, J. C., & Patel, P. M. (2010) · Anesthesiology · doi:10.1097/aln.0b013e318201dcb3 · Cited by 117 · see citing works
Fang, F., Xue, Z., & Cang, J. (2012) · Neuroscience Bulletin · doi:10.1007/s12264-012-1260-4 · Cited by 116 · see citing works
Neurodevelopmental implications of the general anesthesia in neonate and infants
Lee, J. H., Zhang, J., Wei, L., & Yu, S. P. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.03.028 · Cited by 113 · see citing works
The glial perspective of autism spectrum disorders
Zeidán‐Chuliá, F., Salmina, A. B., Malinovskaya, N. A., Noda, M., Verkhratsky, A., & Moreira, J. C. F. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.11.008 · Cited by 111 · see citing works
Gleich, S. J., Flick, R. P., Hu, D., Zaccariello, M. J., Colligan, R. C., Katusic, S. K., Schroeder, D. R., Hanson, A. C., Buenvenida, S. L., Wilder, R. T., et al. (2014) · Contemporary Clinical Trials · doi:10.1016/j.cct.2014.12.020 · Cited by 108 · see citing works
Ding, M.-L., Ma, H., Man, Y., & Hong-yan, L. V. (2017) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2016-0333 · Cited by 108 · see citing works
Raper, J., Biasio, J. C. D., Murphy, K. L., Alvarado, M. C., & Baxter, M. G. (2018) · British Journal of Anaesthesia · doi:10.1016/j.bja.2018.01.014 · Cited by 105 · see citing works
Isoflurane exposure in newborn rats induces long-term cognitive dysfunction in males but not females
Lee, B. H., Chan, J. T., Kraeva, E., Peterson, K., & Sall, J. W. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.03.011 · Cited by 105 · see citing works
Nociceptive stimuli enhance anesthetic-induced neuroapoptosis in the rat developing brain
Shu, Y., Zhou, Z., Wan, Y., Sanders, R. D., Li, M., Pac-Soo, C., Maze, M., & Ma, D. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.10.021 · Cited by 104 · see citing works
Feasibility and Pilot Study of the Pediatric Anesthesia NeuroDevelopment Assessment (PANDA) Project
Sun, L. S., Li, G., DiMaggio, C. J., Byrne, M. W., Ing, C. H., Miller, T. L. K., Bellinger, D. C., Han, S., & McGowan, F. X. J. (2012) · Journal of Neurosurgical Anesthesiology · doi:10.1097/ana.0b013e31826a0371 · Cited by 102 · see citing works
Review of preclinical studies on pediatric general anesthesia-induced developmental neurotoxicity
Walters, J. L., & Paule, M. G. (2016) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2016.11.005 · Cited by 101 · see citing works
Maternal anesthesia and fetal neurodevelopment
Palanisamy, A. (2012) · International Journal of Obstetric Anesthesia · doi:10.1016/j.ijoa.2012.01.005 · Cited by 98 · see citing works
Zhao, T., Li, Y., Wei, W., Savage, S., Zhou, L., & Ma, D. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.02.009 · Cited by 97 · see citing works
Isoflurane exposure for three hours triggers apoptotic cell death in neonatal macaque brain
Noguchi, K. K., Johnson, S. A., Dissen, G. A., Martin, L., Manzella, F. M., Schenning, K. J., Olney, J. W., & Brambrink, A. M. (2017) · British Journal of Anaesthesia · doi:10.1093/bja/aex123 · Cited by 95 · see citing works
Early life exposure to sevoflurane impairs adulthood spatial memory in the rat
Shen, X., Liu, Y., Xu, S., Zhao, Q., Guo, X., Shen, R., & Wang, F. (2013) · NeuroToxicology · doi:10.1016/j.neuro.2013.08.007 · Cited by 90 · see citing works
Zhou, B., Chen, L., Liao, P. S., Huang, L., Chen, Z., Liao, D., Yang, L., Wang, J., Yu, G., Wang, L., et al. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000086 · Cited by 89 · see citing works
Oxidative Stress as a Common Key Event in Developmental Neurotoxicity
Nishimura, Y., Kanda, Y., Sone, H., & Aoyama, H. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/6685204 · Cited by 89 · see citing works
Chen, G., Gong, M., Yan, M., & Zhang, X. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057870 · Cited by 89 · see citing works
Neurotoxicity of General Anesthetics
Perouansky, M. A., Hemmings, H. C., & Riou, B. (2009) · Anesthesiology · doi:10.1097/aln.0b013e3181bf1d61 · Cited by 89 · see citing works
Stratmann, G., Sall, J. W., May, L. D. V., Loepke, A. W., & Lee, M. T. (2010) · Anesthesia & Analgesia · doi:10.1213/ane.0b013e3181af8015 · Cited by 87 · see citing works
Coenzyme Q10 reduces sevoflurane-induced cognitive deficiency in young mice
Xu, G., Han, L., Dong, Y., Shapoval, D., Soriano, S. G., Liu, X., Zhang, Y., & Xie, Z. (2017) · British Journal of Anaesthesia · doi:10.1093/bja/aex071 · Cited by 85 · see citing works
Sevoflurane causes neuronal apoptosis and adaptability changes of neonatal rats
Zheng, S., An, L., Cheng, X., & Wang, Y. J. (2013) · Acta Anaesthesiologica Scandinavica · doi:10.1111/aas.12163 · Cited by 85 · see citing works
Alcohol-induced apoptosis of oligodendrocytes in the fetal macaque brain
Creeley, C. E., Dikranian, K. T., Johnson, S. A., Farber, N. B., & Olney, J. W. (2013) · Acta Neuropathologica Communications · doi:10.1186/2051-5960-1-23 · Cited by 84 · see citing works
Understanding autism spectrum disorders with animal models: applications, insights, and perspectives
Zhu, L., 昆明650500,中国, 云., Zhu, Y., Gu, L., & Cheng, Y. (2021) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2021.251 · Cited by 84 · see citing works
Ko, W., Liaw, Y., Huang, J., Zhao, D., Chang, H., Ko, P., Jan, S., Nfor, O. N., Chiang, Y., & Lin, L. (2014) · Pediatric Anesthesia · doi:10.1111/pan.12371 · Cited by 83 · see citing works
Han, L., Liufu, N., Dong, Y., Xu, G., Zhang, Y., Shu, L., Soriano, S. G., Zheng, H., Yu, B., & Xie, Z. (2017) · Anesthesiology · doi:10.1097/aln.0000000000001889 · Cited by 81 · see citing works
Yonamine, R., Satoh, Y., Kodama, M., Araki, Y., & Kazama, T. (2012) · Anesthesiology · doi:10.1097/aln.0b013e318275146d · Cited by 77 · see citing works
Self-citationTang, X., Wang, X., Fang, G., Zhao, Y., Yan, J., Zhou, Z., Sun, R., Luo, A., & Li, S. (2020) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2020.108579 · Cited by 77 · see citing works
General anesthesia in children and long-term neurodevelopmental deficits: A systematic review
Xiao, A., Feng, Y., Yu, S. P., Xu, C., Chen, J., Wang, T., & Xiao, W. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.972025 · Cited by 76 · see citing works
Dexmedetomidine Attenuates Neurotoxicity Induced by Prenatal Propofol Exposure
Li, J., Xiong, M., Nadavaluru, P. R., Zuo, W., Ye, J. H., Eloy, J. D., & Bekker, A. (2015) · Journal of Neurosurgical Anesthesiology · doi:10.1097/ana.0000000000000181 · Cited by 76 · see citing works
Hua, F., Ying, J., Zhang, J., Wang, X., Hu, Y.-H., Liang, Y., Liu, Q., & Xu, G. (2016) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2016.2715 · Cited by 75 · see citing works
Apai, C., Shah, R., Tran, K., & Shah, S. P. (2021) · Clinical Therapeutics · doi:10.1016/j.clinthera.2021.01.024 · Cited by 75 · see citing works
Propofol Administration During Early Postnatal Life Suppresses Hippocampal Neurogenesis
Huang, J., Jing, S., Chen, X., Bao, X., Du, Z., Li, H., Tian-de, Y., & Fan, X. (2015) · Molecular Neurobiology · doi:10.1007/s12035-014-9052-7 · Cited by 75 · see citing works
Long-Term Effects of Neonatal Single or Multiple Isoflurane Exposures on Spatial Memory in Rats
Murphy, K. L., & Baxter, M. G. (2013) · Frontiers in Neurology · doi:10.3389/fneur.2013.00087 · Cited by 74 · see citing works
Liao, Z., Cao, D., Han, X., Liu, C., Peng, J., Zuo, Z., Wang, F., & Li, Y. (2014) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2014.07.001 · Cited by 74 · see citing works
Ing, C. H., Hegarty, M. K., Perkins, J. W., Whitehouse, A., DiMaggio, C. J., Sun, M., Andrews, H., Li, G., Sun, L., & von Ungern-Sternberg, B. S. (2016) · British Journal of Anaesthesia · doi:10.1093/bja/aew413 · Cited by 74 · see citing works
Jiang, T., Wang, X., Ding, C., & Du, X. (2017) · Korean Journal of Physiology and Pharmacology · doi:10.4196/kjpp.2017.21.6.579 · Cited by 73 · see citing works
Zhang, X., Xin, X., Dong, Y., Zhang, Y., Yu, B., Mao, J., & Xie, Z. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2049-13.2013 · Cited by 69 · see citing works
Behavioral and emotional effects of repeated general anesthesia in young children
Bakri, M. H., Ismail, E. A., Ali, M. S., Elsedfy, G. O., Sayed, T. A., & Ibrahim, A. G. A. (2015) · Saudi Journal of Anaesthesia · doi:10.4103/1658-354x.152843 · Cited by 67 · see citing works
Wang, S.-Q., Fang, F., Xue, Z.-G., Cang, J., & Zhang, X.-G. (2013) · PubMed · Cited by 67 · see citing works
Satoh, Y., Kobayashi, Y., Takeuchi, A., Pagès, G., Pouysségur, J., & Kazama, T. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.2243-10.2011 · Cited by 66 · see citing works
Self-citationMechanistic Insights into Neurotoxicity Induced by Anesthetics in the Developing Brain
Lei, X., Guo, Q., & Zhang, J. (2012) · International Journal of Molecular Sciences · doi:10.3390/ijms13066772 · Cited by 66 · see citing works
Pediatric anesthesia and neurotoxicity: what the radiologist needs to know
Barton, K., Nickerson, J. P., Higgins, T. J., & Williams, R. K. (2017) · Pediatric Radiology · doi:10.1007/s00247-017-3871-4 · Cited by 66 · see citing works
Kang, E., Jiang, D., Ryu, Y. K., Lim, S., Kwak, M., Gray, C., Xu, M., Choi, J. H., Junn, S., Kim, J., et al. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2001246 · Cited by 66 · see citing works
Cognitive and social functions and growth factors in a mouse model of Rett syndrome
Schaevitz, L. R., Moriuchi, J. M., Nag, N., Mellott, T. J., & Berger-Sweeney, J. E. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.12.025 · Cited by 65 · see citing works
Neurodevelopmental Outcomes After Initial Childhood Anesthetic Exposure Between Ages 3 and 10 Years
Ing, C. H., DiMaggio, C. J., Whitehouse, A., Hegarty, M. K., Sun, M., von Ungern-Sternberg, B. S., Davidson, A. J., Wall, M. M., Li, G., & Sun, L. S. (2014) · Journal of Neurosurgical Anesthesiology · doi:10.1097/ana.0000000000000121 · Cited by 65 · see citing works
Ramage, T. M., Chang, F. L., Shih, J., Alvi, R. S., Quitoriano, G. R., Rau, V., Barbour, K., Elphick, S. A., Kong, C., Tantoco, N. K., et al. (2013) · British Journal of Anaesthesia · doi:10.1093/bja/aet103 · Cited by 65 · see citing works
Zhang, X., Liu, S., Newport, G. D., Paule, M. G., Callicott, R. J., Thompson, J., Liu, F., Patterson, T. A., Berridge, M. S., Apana, S. M., et al. (2016) · Anesthesiology · doi:10.1097/aln.0000000000001154 · Cited by 65 · see citing works
Pasternak, J. J., & Lanier, W. L. (2009) · Journal of Neurosurgical Anesthesiology · doi:10.1097/ana.0000000000000048 · Cited by 60 · see citing works
Transient Effects of Anesthetics on Dendritic Spines and Filopodia in the Living Mouse Cortex
Yang, G., Chang, P. C.-Y., Bekker, A., Blanck, T. J. J., & Gan, W. (2011) · Anesthesiology · doi:10.1097/aln.0b013e318229a660 · Cited by 59 · see citing works
Anesthesia/Surgery Induces Cognitive Impairment in Female Alzheimer’s Disease Transgenic Mice
Zhang, C., Zhang, Y., Shen, Y., Zhao, G., Xie, Z., & Dong, Y. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-161268 · Cited by 59 · see citing works
Sun, Z., Satomoto, M., Adachi, Y., Kinoshita, H., & Makita, K. (2016) · British Journal of Anaesthesia · doi:10.1093/bja/aew064 · Cited by 58 · see citing works
Self-citationYufune, S., Satoh, Y., Takamatsu, I., Ohta, H., Kobayashi, Y., Takaenoki, Y., Pagès, G., Pouysségur, J., Endo, S., & Kazama, T. (2015) · Scientific Reports · doi:10.1038/srep10252 · Cited by 57 · see citing works
Self-citationLiu, J.-S., Li, L., Xie, P., Zhao, X., Shi, D., Zhang, Y., Pan, C., & Li, T. (2022) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2022.01.031 · Cited by 57 · see citing works
Yang, T., Zhuang, L., Fidalgo, A. R., Petrides, E., Terrando, N., Xin-min, W., Sanders, R. D., Robertson, N. J., Johnson, M. R., Maze, M., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037020 · Cited by 57 · see citing works
Anesthesia, brain changes, and behavior: Insights from neural systems biology
Colon, É., Bittner, E. A., Kussman, B. D., McCann, M. E., Soriano, S. G., & Borsook, D. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.01.005 · Cited by 57 · see citing works
Creeley, C. E., & Olney, J. W. (2013) · Brain Sciences · doi:10.3390/brainsci3031153 · Cited by 56 · see citing works
Nguyen, P. T., Nakamura, T., Hori, E., Urakawa, S., Uwano, T., Zhao, J., Li, R., Bac, N. D., Hamashima, T., Ishii, Y., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018004 · Cited by 56 · see citing works
Wang, W., Wang, H., Luo, Y., Jia, L., Zhao, J., Zhang, H., Ma, Z., Xue, Q.-S., & Yu, B. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.12.039 · Cited by 55 · see citing works
Wang, W., Jia, L., Luo, Y., Zhang, H., Cai, F., Mao, H., Xu, W., Fang, J., Peng, Z., Ma, Z., et al. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-9005-1 · Cited by 55 · see citing works
- Authors
- Satomoto, M., Satoh, Y., Terui, K., Miyao, H., Takishima, K., Ito, M., & Imaki, J.
- Affiliations
- National Defense Medical College (JP)
- Assistant Professor.
- Associate Professor, Department of Obstetric Anesthesia.
- Saitama Medical Center, Saitama Medical University (JP)
- Associate Professor.
- Professor, Department of Developmental Anatomy and Regenerative Biology.
- Venue
- Anesthesiology
- Published
- 2009-03-01
- Volume
- 110
- Issue
- 3
- Pages
- 628-637
- ISSN
- 0003-3022 (ISSN-L)
- OpenAlex
- W2036450246
- Cited by
- 496
- References
- 31
- Citations by year
- 2026: 5 · 2025: 12 · 2024: 18 · 2023: 15 · 2022: 30 · 2021: 34 · 2020: 31 · 2019: 26 · 2018: 30 · 2017: 37 · 2016: 62 · 2015: 37 · 2014: 47 · 2013: 36 · 2012: 32
- FWCI
- 7.83
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Anesthesiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Defense Medical College
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Anesthesia and Neurotoxicity Research
- Health Sciences › Medicine › Anesthesiology and Pain Medicine › Anesthesia and Sedative Agents
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- sevoflurane, neonatal anesthesia, inhalational anesthetics, social behavior, social recognition memory, fear conditioning, learning deficits, apoptosis, caspase-3, autism spectrum disorder, NMDA receptor antagonism, developmental neurotoxicity
- MeSH terms
- Sevoflurane, Animals, Animals, Newborn, Conditioning, Psychological, Fear, Learning Disabilities, Male, Memory Disorders, Methyl Ethers, Mice, Inbred C57BL, Social Behavior, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review