Preoperative Sleep Disturbance Exaggerates Surgery-Induced Neuroinflammation and Neuronal Damage in Aged Mice
Pengfei Ni, Hongquan Dong, Qin Zhou, Yiwei Wang, Menghan Sun, Yanning Qian, Jie Sun, Pengfei Ni, Hongquan Dong, Qin Zhou, Yiwei Wang, Menghan Sun, Yanning Qian, Jie Sun
Abstract
Postoperative cognitive dysfunction (POCD) is defined as new cognitive impairment (memory impairment and impaired performance) after surgery, especially in aged patients. Sleep disturbance is a common phenomenon before surgery that has been increasingly thought to affect patient recovery. However, little is known about the functional impact of preoperative sleep disturbance on POCD. Here, we showed that tibial fracture surgery induced cognitive deficit and production of proinflammatory cytokines interleukin-6 (IL-6) and IL-1β, along with microglia and astrocyte activation, neuronal damage, and blood-brain barrier (BBB) disruption. Preoperative sleep disturbance enhanced the surgery-induced neuroinflammation, neuronal damage, BBB disruption, and memory impairment 24 h after surgery. Taken together, these results demonstrated that preoperative sleep disturbance aggravated postoperative cognitive function in aged mice and the mechanism may be related to central nervous system (CNS) inflammation and neuronal damage.
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References
- Monk T. G., Weldon B. C., Garvan C. W., et al. Predictors of cognitive dysfunction after major noncardiac surgery. Anesthesiology. 2008;108(1):18–30. doi: 10.1097/01.anes.0000296071.19434.1e.
- Mashour G. A., Woodrum D. T., Avidan M. S. Neurological complications of surgery and anaesthesia. British Journal of Anaesthesia. 2015;114(2):194–203. doi: 10.1093/bja/aeu296.
- Berger M., Nadler J. W., Browndyke J., et al. Postoperative cognitive dysfunction: minding the gaps in our knowledge of a common postoperative complication in the elderly. Anesthesiology Clinics. 2015;33(3):517–550. doi: 10.1016/j.anclin.2015.05.008.
- Terrando N., Brzezinski M., Degos V., et al. Perioperative cognitive decline in the aging population. Mayo Clinic Proceedings. 2011;86(9):885–893. doi: 10.4065/mcp.2011.0332.
- Culley D. J., Flaherty D., Fahey M. C., et al. Poor performance on a preoperative cognitive screening test predicts postoperative complications in older orthopedic surgical patients. Anesthesiology. 2017;127(5):765–774. doi: 10.1097/ALN.0000000000001859.
- Aleisa A. M., Alzoubi K. H., Alkadhi K. A. Post-learning REM sleep deprivation impairs long-term memory: reversal by acute nicotine treatment. Neuroscience Letters. 2011;499(1):28–31. doi: 10.1016/j.neulet.2011.05.025.
- Cordeira J., Kolluru S. S., Rosenblatt H., Kry J., Strecker R. E., McCarley R. W. Learning and memory are impaired in the object recognition task during metestrus/diestrus and after sleep deprivation. Behavioural Brain Research. 2018;339:124–129. doi: 10.1016/j.bbr.2017.11.033.
- Rasch B., Born J. About sleep’s role in memory. Physiological Reviews. 2013;93(2):681–766. doi: 10.1152/physrev.00032.2012.
- Diekelmann S., Born J. The memory function of sleep. Nature Reviews Neuroscience. 2010;11(2):114–126. doi: 10.1038/nrn2762.
- Lucey B. P., Hicks T. J., McLeland J. S., et al. Effect of sleep on overnight cerebrospinal fluid amyloid β kinetics. Annals of Neurology. 2018;83(1):197–204. doi: 10.1002/ana.25117.
- Tononi G., Cirelli C. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron. 2014;81(1):12–34. doi: 10.1016/j.neuron.2013.12.025.
- Xie L., Kang H., Xu Q., et al. Sleep drives metabolite clearance from the adult brain. Science. 2013;342(6156):373–377. doi: 10.1126/science.1241224.
- Mckinley J., Mccarthy A., Lynch T. Don’t lose sleep over neurodegeneration-it helps clear amyloid Beta. Frontiers in Neurology. 2013;4:p. 206. doi: 10.3389/fneur.2013.00206.
- Kain Z. N., Caldwell-Andrews A. A. Sleeping characteristics of adults undergoing outpatient elective surgery: a cohort study. Journal of Clinical Anesthesia. 2003;15(7):505–509. doi: 10.1016/j.jclinane.2003.02.002.
- Gogenur I., Middleton B., Burgdorf S., Rasmussen L. S., Skene D. J., Rosenberg J. Impact of sleep and circadian disturbances in urinary 6-sulphatoxymelatonin levels, on cognitive function after major surgery. Journal of Pineal Research. 2007;43(2):179–184. doi: 10.1111/j.1600-079X.2007.00460.x.
- Barrientos R. M., Hein A. M., Frank M. G., Watkins L. R., Maier S. F. Intracisternal interleukin-1 receptor antagonist prevents postoperative cognitive decline and neuroinflammatory response in aged rats. The Journal of Neuroscience. 2012;32(42):14641–14648. doi: 10.1523/JNEUROSCI.2173-12.2012.
- Androsova G., Krause R., Winterer G., Schneider R. Biomarkers of postoperative delirium and cognitive dysfunction. Frontiers in Aging Neuroscience. 2015;7:p. 112. doi: 10.3389/fnagi.2015.00112.
- Riedel B., Browne K., Silbert B. Cerebral protection: inflammation, endothelial dysfunction, and postoperative cognitive dysfunction. Current Opinion in Anaesthesiology. 2014;27(1):89–97. doi: 10.1097/ACO.0000000000000032.
- Ransohoff R. M. How neuroinflammation contributes to neurodegeneration. Science. 2016;353(6301):777–783. doi: 10.1126/science.aag2590.
- Herrera A. J., Tomás-Camardiel M., Venero J. L., Cano J., Machado A. Inflammatory process as a determinant factor for the degeneration of substantia nigra dopaminergic neurons. Journal of Neural Transmission (Vienna) 2005;112(1):111–119. doi: 10.1007/s00702-004-0121-3.
- Philips T., Robberecht W. Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. The Lancet Neurology. 2011;10(3):253–263. doi: 10.1016/S1474-4422(11)70015-1.
- Mcmahon D., Hynynen K. Acute inflammatory response following increased blood-brain barrier permeability induced by focused ultrasound is dependent on microbubble dose. Theranostics. 2017;7(16):3989–4000. doi: 10.7150/thno.21630.
- Obermeier B., Daneman R., Ransohoff R. M. Development, maintenance and disruption of the blood-brain barrier. Nature Medicine. 2013;19(12):1584–1596. doi: 10.1038/nm.3407.
- Naidoo N., Ferber M., Master M., Zhu Y., Pack A. I. Aging impairs the unfolded protein response to sleep deprivation and leads to proapoptotic signaling. The Journal of Neuroscience. 2008;28(26):6539–6548. doi: 10.1523/JNEUROSCI.5685-07.2008.
- Lu S. M., Yu C. J., Liu Y. H., et al. S100A8 contributes to postoperative cognitive dysfunction in mice undergoing tibial fracture surgery by activating the TLR4/MyD88 pathway. Brain, Behavior, and Immunity. 2015;44:221–234. doi: 10.1016/j.bbi.2014.10.011.
- Terrando N., Eriksson L. I., Kyu Ryu J., et al. Resolving postoperative neuroinflammation and cognitive decline. Annals of Neurology. 2011;70(6):986–995. doi: 10.1002/ana.22664.
- Kreutzmann J. C., Havekes R., Abel T., Meerlo P. Sleep deprivation and hippocampal vulnerability: changes in neuronal plasticity, neurogenesis and cognitive function. Neuroscience. 2015;309:173–190. doi: 10.1016/j.neuroscience.2015.04.053.
- McMahon W. R., Ftouni S., Drummond S. P. A., et al. The wake maintenance zone shows task dependent changes in cognitive function following one night without sleep. Sleep. 2018;41(10) doi: 10.1093/sleep/zsy148.
- Lee M. L., Katsuyama A. M., Duge L. S., et al. Fragmentation of rapid eye movement and nonrapid eye movement sleep without total sleep loss impairs hippocampus-dependent fear memory consolidation. Sleep. 2016;39(11):2021–2031. doi: 10.5665/sleep.6236.
- Femenía T., Giménez-Cassina A., Codeluppi S., et al. Disrupted neuroglial metabolic coupling after peripheral surgery. The Journal of Neuroscience. 2018;38(2):452–464. doi: 10.1523/JNEUROSCI.1797-17.2017.
- Gambús P. L., Trocóniz I. F., Feng X., et al. Relation between acute and long-term cognitive decline after surgery: influence of metabolic syndrome. Brain, Behavior, and Immunity. 2015;50:203–208. doi: 10.1016/j.bbi.2015.07.005.
- Merali Z., Presti-Torres J., MacKay J. C., et al. Long-term behavioral effects of neonatal blockade of gastrin-releasing peptide receptors in rats: similarities to autism spectrum disorders. Behavioural Brain Research. 2014;263:60–69. doi: 10.1016/j.bbr.2014.01.008.
- Heneka M. T., Carson M. J., Khoury J. E., et al. Neuroinflammation in Alzheimer’s disease. The Lancet Neurology. 2015;14(4):388–405. doi: 10.1016/S1474-4422(15)70016-5.
- Gonzalez H., Pacheco R. T-cell-mediated regulation of neuroinflammation involved in neurodegenerative diseases. Journal of Neuroinflammation. 2014;11(1):p. 201. doi: 10.1186/s12974-014-0201-8.
- Rosenberger K., Derkow K., Dembny P., Kruger C., Schott E., Lehnardt S. The impact of single and pairwise toll-like receptor activation on neuroinflammation and neurodegeneration. Journal of Neuroinflammation. 2014;11(1):p. 166. doi: 10.1186/s12974-014-0166-7.
- Skvarc D. R., Berk M., Byrne L. K., et al. Post-operative cognitive dysfunction: an exploration of the inflammatory hypothesis and novel therapies. Neuroscience & Biobehavioral Reviews. 2018;84:116–133. doi: 10.1016/j.neubiorev.2017.11.011.
- Shi D. D., Dong C. M., Ho L. C., et al. Resveratrol, a natural polyphenol, prevents chemotherapy-induced cognitive impairment: involvement of cytokine modulation and neuroprotection. Neurobiology of Disease. 2018;114:164–173. doi: 10.1016/j.nbd.2018.03.006.
- Vacas S., Degos V., Feng X., Maze M. The neuroinflammatory response of postoperative cognitive decline. British Medical Bulletin. 2013;106(1):161–178. doi: 10.1093/bmb/ldt006.
- Taylor J. M., Main B. S., Crack P. J. Neuroinflammation and oxidative stress: co-conspirators in the pathology of Parkinson’s disease. Neurochemistry International. 2013;62(5):803–819. doi: 10.1016/j.neuint.2012.12.016.
- Ye L., Huang Y., Zhao L., et al. IL-1β and TNF-α induce neurotoxicity through glutamate production: a potential role for neuronal glutaminase. Journal of Neurochemistry. 2013;125(6):897–908. doi: 10.1111/jnc.12263.
- Zhang X., Dong H., Li N., et al. Activated brain mast cells contribute to postoperative cognitive dysfunction by evoking microglia activation and neuronal apoptosis. Journal of Neuroinflammation. 2016;13(1):p. 127. doi: 10.1186/s12974-016-0592-9.
- Nadjar A., Wigren H.-K. M., Tremblay M.-E. Roles of microglial phagocytosis and inflammatory mediators in the pathophysiology of sleep disorders. Frontiers in Cellular Neuroscience. 2017;11:p. 250. doi: 10.3389/fncel.2017.00250.
- Stokholm M. G., Iranzo A., Østergaard K., et al. Assessment of neuroinflammation in patients with idiopathic rapid-eye-movement sleep behaviour disorder: a case-control study. The Lancet Neurology. 2017;16(10):789–796. doi: 10.1016/S1474-4422(17)30173-4.
- Motivala S. J. Sleep and inflammation: psychoneuroimmunology in the context of cardiovascular disease. Annals of Behavioral Medicine. 2011;42(2):141–152. doi: 10.1007/s12160-011-9280-2.
- Bellesi M., de Vivo L., Chini M., Gilli F., Tononi G., Cirelli C. Sleep loss promotes astrocytic phagocytosis and microglial activation in mouse cerebral cortex. The Journal of Neuroscience. 2017;37(21):5263–5273. doi: 10.1523/JNEUROSCI.3981-16.2017.
- He J., Hsuchou H., He Y., Kastin A. J., Wang Y., Pan W. Sleep restriction impairs blood–brain barrier function. The Journal of Neuroscience. 2014;34(44):14697–14706. doi: 10.1523/JNEUROSCI.2111-14.2014.
- Zhu B., Dong Y., Xu Z., et al. Sleep disturbance induces neuroinflammation and impairment of learning and memory. Neurobiology of Disease. 2012;48(3):348–355. doi: 10.1016/j.nbd.2012.06.022.
- Luca G., Haba Rubio J., Andries D., et al. Age and gender variations of sleep in subjects without sleep disorders. Annals of Medicine. 2015;47(6):482–491. doi: 10.3109/07853890.2015.1074271.
- Fonken L. K., Frank M. G., D'Angelo H. M., et al. Mycobacterium vaccae immunization protects aged rats from surgery-elicited neuroinflammation and cognitive dysfunction. Neurobiology of Aging. 2018;71:105–114. doi: 10.1016/j.neurobiolaging.2018.07.012.
- Johar H., Kawan R., Thwing R. E., Karl-Heinz L. Impaired sleep predicts cognitive decline in old people: findings from the prospective KORA age study. Sleep. 2016;39(1):217–226. doi: 10.5665/sleep.5352.
- Palmer K., Mitolo M., Burgio F., Meneghello F., Venneri A. Sleep disturbance in mild cognitive impairment and association with cognitive functioning. A case-control study. Frontiers in Aging Neuroscience. 2018;10:p. 360. doi: 10.3389/fnagi.2018.00360.
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