Skip to main content
Top
Published in: BMC Anesthesiology 1/2018

Open Access 01-12-2018 | Research article

High-fat diet aggravates postoperative cognitive dysfunction in aged mice

Authors: Lan Wei, Minmin Yao, Zhimeng Zhao, Hui Jiang, Shengjin Ge

Published in: BMC Anesthesiology | Issue 1/2018

Login to get access

Abstract

Background

Silent Information Regulator 1 (Sirt1) and apoptosis play key roles in postoperative cognitive dysfunction (POCD). Consuming a high-fat diet (HFD), a prevalent type of diet in modern society, has been increasingly recognized as contributing to neurodegenerative diseases. Although Sirt1 and apoptosis are significant responders to HFD in the brain, little is known regarding the functional correlations between HFD and POCD.

Methods

Thirty-two aged C57BL/6 male mice were randomly divided into 2 groups: an ad libitum (AL) group (fed a regular diet) and high-fat diet (HF) group (fed a high-fat diet). After 8 weeks, the animals were divided into four sub-groups: an ad libitum control (ALC) group, ad libitum surgery (ALS) group, high-fat diet control (HFC) group, and high-fat diet surgery (HFS) group. The ALS and HFS groups were exposed to 3% sevoflurane in 33% oxygen for 3 h and were subsequently subjected to exploratory surgery to establish the POCD model. The ALC and HFC groups were treated with 33% oxygen for 3 h without surgery. After 48 h, the learning and memory abilities of mice in each group were tested using the Morris water maze (MWM). The expression levels of Sirt1, Bcl-2, Bax and caspase-3 cleaved were detected by western blot.

Results

The MWM and western blotting results showed that the learning and memory abilities were decreased in the HFC group compared with the ALC group. The learning and memory abilities and the expression of Sirt1 in the hippocampus in the HFS group were significantly decreased compared with the other groups. A significant decrease in Sirt1 expression was also observed in the HFC group compared with the ALS group. The level of Bcl-2 was lower in the HFS group than in the HFC and ALC groups. The expression levels of caspase-3 cleaved and Bax increased in the HFS group compared with the HFC group. Moreover, the expression of caspase-3 cleaved was higher in the HFC group than in the ALS group.

Conclusion

HFD can aggravate POCD in aged C57BL/6 mice, an effect that may be related to the inhibition expression of Sirt1 and the promotion of neuronal apoptosis.
Literature
1.
go back to reference Last AR, Wilson SA. Low-carbohydrate diets. Am Fam Physician. 2006;73(11):1942–8.PubMed Last AR, Wilson SA. Low-carbohydrate diets. Am Fam Physician. 2006;73(11):1942–8.PubMed
2.
go back to reference Cb DLS, Ellis CL, Lee J, Hartman AL, Rutledge JC, Raybould HE. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol. 2010;299(2):G440.CrossRef Cb DLS, Ellis CL, Lee J, Hartman AL, Rutledge JC, Raybould HE. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol. 2010;299(2):G440.CrossRef
3.
go back to reference Serino M, Luche E, Gres S, Baylac A, Bergé M, Cenac C, Waget A, Klopp P, Iacovoni J, Klopp C. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut. 2012;61(4):543–53.CrossRefPubMed Serino M, Luche E, Gres S, Baylac A, Bergé M, Cenac C, Waget A, Klopp P, Iacovoni J, Klopp C. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut. 2012;61(4):543–53.CrossRefPubMed
4.
go back to reference Birse RT, Choi J, Reardon K, Rodriguez J, Graham S, Diop S, Ocorr K, Bodmer R, Oldham S. High fat diet-induced obesity and heart dysfunction is regulated by the TOR pathway in drosophila. Cell Metab. 2010;12(5):533.CrossRefPubMedPubMedCentral Birse RT, Choi J, Reardon K, Rodriguez J, Graham S, Diop S, Ocorr K, Bodmer R, Oldham S. High fat diet-induced obesity and heart dysfunction is regulated by the TOR pathway in drosophila. Cell Metab. 2010;12(5):533.CrossRefPubMedPubMedCentral
5.
go back to reference Tang FY, Pai MH, Chiang EP. Consumption of high-fat diet induces tumor progression and epithelial-mesenchymal transition of colorectal cancer in a mouse xenograft model. J Nutr Biochem. 2012;23(10):1302–13.CrossRefPubMed Tang FY, Pai MH, Chiang EP. Consumption of high-fat diet induces tumor progression and epithelial-mesenchymal transition of colorectal cancer in a mouse xenograft model. J Nutr Biochem. 2012;23(10):1302–13.CrossRefPubMed
6.
go back to reference Fu Z, Wu J, Nesil T, Li MD, Aylor KW, Liu Z. Long-term high-fat diet induces hippocampal microvascular insulin resistance and cognitive dysfunction. Am J Physiol Endocrinol Metab. 2017;312(2):E89.CrossRefPubMed Fu Z, Wu J, Nesil T, Li MD, Aylor KW, Liu Z. Long-term high-fat diet induces hippocampal microvascular insulin resistance and cognitive dysfunction. Am J Physiol Endocrinol Metab. 2017;312(2):E89.CrossRefPubMed
7.
go back to reference Sah SK, Lee C, Jang JH, Park GH. Effect of high-fat diet on cognitive impairment in triple-transgenic mice model of Alzheimer's disease. Biochem Biophys Res Commun. 2017;493(1):731–6.CrossRefPubMed Sah SK, Lee C, Jang JH, Park GH. Effect of high-fat diet on cognitive impairment in triple-transgenic mice model of Alzheimer's disease. Biochem Biophys Res Commun. 2017;493(1):731–6.CrossRefPubMed
8.
go back to reference Goldbart AD, Row BW, Kheirandishgozal L, Cheng Y, Brittian KR, Gozal D. High fat/refined carbohydrate diet enhances the susceptibility to spatial learning deficits in rats exposed to intermittent hypoxia. Brain Res. 2006;1090(1):190–6.CrossRefPubMed Goldbart AD, Row BW, Kheirandishgozal L, Cheng Y, Brittian KR, Gozal D. High fat/refined carbohydrate diet enhances the susceptibility to spatial learning deficits in rats exposed to intermittent hypoxia. Brain Res. 2006;1090(1):190–6.CrossRefPubMed
9.
go back to reference Solfrizzi V, D'Introno A, Colacicco AM, Capurso C, Del PA, Capurso S, Gadaleta A, Capurso A, Panza F. Dietary fatty acids intake: possible role in cognitive decline and dementia. Exp Gerontol. 2005;40(4):257–70.CrossRefPubMed Solfrizzi V, D'Introno A, Colacicco AM, Capurso C, Del PA, Capurso S, Gadaleta A, Capurso A, Panza F. Dietary fatty acids intake: possible role in cognitive decline and dementia. Exp Gerontol. 2005;40(4):257–70.CrossRefPubMed
10.
go back to reference Stranahan AM, Norman ED, Lee K, Cutler RG, Telljohann R, Egan JM, Mattson MP. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus. 2008;18(11):1085–8.CrossRefPubMedPubMedCentral Stranahan AM, Norman ED, Lee K, Cutler RG, Telljohann R, Egan JM, Mattson MP. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus. 2008;18(11):1085–8.CrossRefPubMedPubMedCentral
11.
go back to reference Heyward FD, Walton RG, Carle MS, Coleman MA, Garvey WT, Sweatt JD. Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression. Neurobiol Learn Mem. 2012;98(1):25–32.CrossRefPubMedPubMedCentral Heyward FD, Walton RG, Carle MS, Coleman MA, Garvey WT, Sweatt JD. Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression. Neurobiol Learn Mem. 2012;98(1):25–32.CrossRefPubMedPubMedCentral
12.
go back to reference Wang R, Zhang Y, Li J, Zhang C. Resveratrol ameliorates spatial learning memory impairment induced by Aβ1-42 in rats. Neuroscience. 2016;344:39.CrossRefPubMed Wang R, Zhang Y, Li J, Zhang C. Resveratrol ameliorates spatial learning memory impairment induced by Aβ1-42 in rats. Neuroscience. 2016;344:39.CrossRefPubMed
13.
go back to reference Julien C, Tremblay C, Émond V, Lebbadi M, Norman Salem J, Bennett DA, Calon F. SIRT1 decrease parallels the accumulation of tau in Alzheimer disease. J Neuropathol Exp Neurol. 2009;68(1):48.CrossRefPubMedPubMedCentral Julien C, Tremblay C, Émond V, Lebbadi M, Norman Salem J, Bennett DA, Calon F. SIRT1 decrease parallels the accumulation of tau in Alzheimer disease. J Neuropathol Exp Neurol. 2009;68(1):48.CrossRefPubMedPubMedCentral
14.
go back to reference Gräff J, Kahn M, Samiei A, Gao J, Ota KT, Rei D, Tsai LH. A dietary regimen of caloric restriction or pharmacological activation of SIRT1 to delay the onset of neurodegeneration. J Neurosci. 2013;33(21):8951–60.CrossRefPubMedPubMedCentral Gräff J, Kahn M, Samiei A, Gao J, Ota KT, Rei D, Tsai LH. A dietary regimen of caloric restriction or pharmacological activation of SIRT1 to delay the onset of neurodegeneration. J Neurosci. 2013;33(21):8951–60.CrossRefPubMedPubMedCentral
15.
go back to reference Morris MC, Evans DA, Bienias JL, Tangney CC, Bennett DA, Aggarwal N, Schneider J, Wilson RS. Dietary fats and the risk of incident Alzheimer disease. Arch Neurol. 2003;60(2):194–200.CrossRefPubMed Morris MC, Evans DA, Bienias JL, Tangney CC, Bennett DA, Aggarwal N, Schneider J, Wilson RS. Dietary fats and the risk of incident Alzheimer disease. Arch Neurol. 2003;60(2):194–200.CrossRefPubMed
16.
go back to reference Moraes JC, Coope A, Morari J, Cintra DE, Roman EA, Pauli JR, Romanatto T, Carvalheira JB, Oliveira AL, Saad MJ. High-fat diet induces apoptosis of hypothalamic neurons. PLoS One. 2009;4(4):e5045.CrossRefPubMedPubMedCentral Moraes JC, Coope A, Morari J, Cintra DE, Roman EA, Pauli JR, Romanatto T, Carvalheira JB, Oliveira AL, Saad MJ. High-fat diet induces apoptosis of hypothalamic neurons. PLoS One. 2009;4(4):e5045.CrossRefPubMedPubMedCentral
17.
go back to reference Pistell PJ, Morrison CD, Gupta S, Knight AG, Keller JN, Ingram DK, Bruce-Keller AJ. Cognitive impairment following high fat diet consumption is associated with brain inflammation. J Neuroimmunol. 2010;219(1–2):25.CrossRefPubMed Pistell PJ, Morrison CD, Gupta S, Knight AG, Keller JN, Ingram DK, Bruce-Keller AJ. Cognitive impairment following high fat diet consumption is associated with brain inflammation. J Neuroimmunol. 2010;219(1–2):25.CrossRefPubMed
18.
go back to reference Heera P, Mikyung P, Jehun C, Kunyoung P, Haeyoung C, Jaewon L. A high-fat diet impairs neurogenesis: involvement of lipid peroxidation and brain-derived neurotrophic factor. Neurosci Lett. 2010;482(3):235–9.CrossRef Heera P, Mikyung P, Jehun C, Kunyoung P, Haeyoung C, Jaewon L. A high-fat diet impairs neurogenesis: involvement of lipid peroxidation and brain-derived neurotrophic factor. Neurosci Lett. 2010;482(3):235–9.CrossRef
19.
go back to reference Zhang C, Li C, Xu Z, Zhao S, Li P, Cao J, Mi W. The effect of surgical and psychological stress on learning and memory function in aged C57BL/6 mice. Neuroscience. 2016;320:210.CrossRefPubMed Zhang C, Li C, Xu Z, Zhao S, Li P, Cao J, Mi W. The effect of surgical and psychological stress on learning and memory function in aged C57BL/6 mice. Neuroscience. 2016;320:210.CrossRefPubMed
20.
go back to reference Evered L, Silbert B, Ames D, Maruff P, Scott D. Does general anaesthesia exacerbate Alzheimer's disease? Alzheimers Dement. 2012;8(4):P208–9.CrossRef Evered L, Silbert B, Ames D, Maruff P, Scott D. Does general anaesthesia exacerbate Alzheimer's disease? Alzheimers Dement. 2012;8(4):P208–9.CrossRef
21.
go back to reference Krenk L, Rasmussen LS, Kehlet H. New insights into the pathophysiology of postoperative cognitive dysfunction. Acta Anaesthesiol Scand. 2010;54(8):951–6.CrossRefPubMed Krenk L, Rasmussen LS, Kehlet H. New insights into the pathophysiology of postoperative cognitive dysfunction. Acta Anaesthesiol Scand. 2010;54(8):951–6.CrossRefPubMed
22.
go back to reference Monk TG, Weldon BC, Garvan CW, Dede DE, Mt VDA, Heilman KM, Gravenstein JS. Predictors of cognitive dysfunction after major noncardiac surgery. Anesthesiology. 2008;108(1):18–30.CrossRefPubMed Monk TG, Weldon BC, Garvan CW, Dede DE, Mt VDA, Heilman KM, Gravenstein JS. Predictors of cognitive dysfunction after major noncardiac surgery. Anesthesiology. 2008;108(1):18–30.CrossRefPubMed
23.
go back to reference An LN, Yue Y, Guo WZ, Miao YL, Mi WD, Zhang H, Lei ZL, Han SJ, Dong L. Surgical trauma induces iron accumulation and oxidative stress in a rodent model of postoperative cognitive dysfunction. Biol Trace Elem Res. 2013;151(2):277–83.CrossRefPubMed An LN, Yue Y, Guo WZ, Miao YL, Mi WD, Zhang H, Lei ZL, Han SJ, Dong L. Surgical trauma induces iron accumulation and oxidative stress in a rodent model of postoperative cognitive dysfunction. Biol Trace Elem Res. 2013;151(2):277–83.CrossRefPubMed
24.
go back to reference Wang Z, Fan J, Wang J, Li Y, Xiao L, Duan D, Wang Q. Protective effect of lycopene on high-fat diet-induced cognitive impairment in rats. Neurosci Lett. 2016;627:185–91.CrossRefPubMed Wang Z, Fan J, Wang J, Li Y, Xiao L, Duan D, Wang Q. Protective effect of lycopene on high-fat diet-induced cognitive impairment in rats. Neurosci Lett. 2016;627:185–91.CrossRefPubMed
25.
go back to reference Ling YZ, Li YU, Liang QS, Anesthesiology DO. Changes on cognitive function, Aβ1~40, the expressions of Bax and Bcl-2 after postoperative of femoral neck fractures in aged rats. Chin J Gerontol. 2013; Ling YZ, Li YU, Liang QS, Anesthesiology DO. Changes on cognitive function, Aβ1~40, the expressions of Bax and Bcl-2 after postoperative of femoral neck fractures in aged rats. Chin J Gerontol. 2013;
26.
go back to reference Xie H, She GM, Wang C, Zhang LY, Liu CF. The gender difference in effect of sevoflurane exposure on cognitive function and hippocampus neuronal apoptosis in rats. Eur Rev Med Pharmacol Sci. 2015;19(4):647.PubMed Xie H, She GM, Wang C, Zhang LY, Liu CF. The gender difference in effect of sevoflurane exposure on cognitive function and hippocampus neuronal apoptosis in rats. Eur Rev Med Pharmacol Sci. 2015;19(4):647.PubMed
27.
go back to reference Meineke M, Ii RLA, Rasmussen T, Anderson D, Azer S, Mehdizadeh A, Kim A, Allard M. Cognitive dysfunction following desflurane versus sevoflurane general anesthesia in elderly patients: a randomized controlled trial. Med Gas Res. 2014;4(1):1–9.CrossRef Meineke M, Ii RLA, Rasmussen T, Anderson D, Azer S, Mehdizadeh A, Kim A, Allard M. Cognitive dysfunction following desflurane versus sevoflurane general anesthesia in elderly patients: a randomized controlled trial. Med Gas Res. 2014;4(1):1–9.CrossRef
28.
go back to reference Hovens IB, Schoemaker RG, Ea VDZ, Absalom AR, Heineman E, van Leeuwen BL. Postoperative cognitive dysfunction: involvement of neuroinflammation and neuronal functioning. Brain Behav Immun. 2014;38(5):202–10.CrossRefPubMed Hovens IB, Schoemaker RG, Ea VDZ, Absalom AR, Heineman E, van Leeuwen BL. Postoperative cognitive dysfunction: involvement of neuroinflammation and neuronal functioning. Brain Behav Immun. 2014;38(5):202–10.CrossRefPubMed
29.
go back to reference Luo J, Nikolaev AY, Imai S, Chen D, Su F, Shiloh A, Guarente L, Gu W. Negative control of p53 by Sir2alpha promotes cell survival under stress. Cell. 2001;107(2):137.CrossRefPubMed Luo J, Nikolaev AY, Imai S, Chen D, Su F, Shiloh A, Guarente L, Gu W. Negative control of p53 by Sir2alpha promotes cell survival under stress. Cell. 2001;107(2):137.CrossRefPubMed
30.
go back to reference Lee IH, Cao L, Mostoslavsky R, Lombard DB, Liu J, Bruns NE, Tsokos M, Alt FW, Finkel T. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci U S A. 2008;105(9):3374–9.CrossRefPubMedPubMedCentral Lee IH, Cao L, Mostoslavsky R, Lombard DB, Liu J, Bruns NE, Tsokos M, Alt FW, Finkel T. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci U S A. 2008;105(9):3374–9.CrossRefPubMedPubMedCentral
31.
go back to reference Lagouge M, Argmann C, Gerharthines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell. 2006;127(6):1109.CrossRefPubMed Lagouge M, Argmann C, Gerharthines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell. 2006;127(6):1109.CrossRefPubMed
32.
go back to reference Michán S, Li Y, Chou MM, Parrella E, Ge H, Long JM, Allard JS, Lewis K, Miller M, Xu W. SIRT1 is essential for normal cognitive function and synaptic plasticity. J Neurosci. 2010;30(29):9695.CrossRefPubMedPubMedCentral Michán S, Li Y, Chou MM, Parrella E, Ge H, Long JM, Allard JS, Lewis K, Miller M, Xu W. SIRT1 is essential for normal cognitive function and synaptic plasticity. J Neurosci. 2010;30(29):9695.CrossRefPubMedPubMedCentral
34.
go back to reference Eimer WA, Vassar R. Neuron loss in the 5XFAD mouse model of Alzheimer’s disease correlates with intraneuronal Aβ42 accumulation and Caspase-3 activation. Mol Neurodegener. 2013;8(1):2.CrossRefPubMedPubMedCentral Eimer WA, Vassar R. Neuron loss in the 5XFAD mouse model of Alzheimer’s disease correlates with intraneuronal Aβ42 accumulation and Caspase-3 activation. Mol Neurodegener. 2013;8(1):2.CrossRefPubMedPubMedCentral
35.
go back to reference Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, Korsmeyer ASJ. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 1993;75(2):241–51.CrossRefPubMed Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, Korsmeyer ASJ. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 1993;75(2):241–51.CrossRefPubMed
36.
go back to reference Cheng EH, Kirsch DG, Clem RJ, Ravi R, Kastan MB, Bedi A, Ueno K, Hardwick JM. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science. 1997;278(5345):1966–8.CrossRefPubMed Cheng EH, Kirsch DG, Clem RJ, Ravi R, Kastan MB, Bedi A, Ueno K, Hardwick JM. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science. 1997;278(5345):1966–8.CrossRefPubMed
37.
go back to reference Shingo I, Li G, Hiroshi T, Megumi F, Nobuko M, Ichiro Y, Toshiro A. Change in mRNA expression of sirtuin 1 and sirtuin 3 in cats fed on high fat diet. BMC Vet Res. 2013;9(1):1–8.CrossRef Shingo I, Li G, Hiroshi T, Megumi F, Nobuko M, Ichiro Y, Toshiro A. Change in mRNA expression of sirtuin 1 and sirtuin 3 in cats fed on high fat diet. BMC Vet Res. 2013;9(1):1–8.CrossRef
38.
go back to reference Molteni R, Barnard RJ, Ying Z, Roberts CK, Gómezpinilla F. A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience. 2002;112(4):803.CrossRefPubMed Molteni R, Barnard RJ, Ying Z, Roberts CK, Gómezpinilla F. A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience. 2002;112(4):803.CrossRefPubMed
39.
go back to reference Xu S, Jiang B, Hou X, Shi C, Bachschmid MM, Zang M, Verbeuren TJ, Cohen RA. High-fat diet increases and the polyphenol, S17834, decreases acetylation of the sirtuin-1-dependent lysine-382 on p53 and apoptotic signaling in atherosclerotic lesion-prone aortic endothelium of normal mice. J Cardiovasc Pharmacol. 2011;58(58):263–71.CrossRefPubMedPubMedCentral Xu S, Jiang B, Hou X, Shi C, Bachschmid MM, Zang M, Verbeuren TJ, Cohen RA. High-fat diet increases and the polyphenol, S17834, decreases acetylation of the sirtuin-1-dependent lysine-382 on p53 and apoptotic signaling in atherosclerotic lesion-prone aortic endothelium of normal mice. J Cardiovasc Pharmacol. 2011;58(58):263–71.CrossRefPubMedPubMedCentral
Metadata
Title
High-fat diet aggravates postoperative cognitive dysfunction in aged mice
Authors
Lan Wei
Minmin Yao
Zhimeng Zhao
Hui Jiang
Shengjin Ge
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Anesthesiology / Issue 1/2018
Electronic ISSN: 1471-2253
DOI
https://doi.org/10.1186/s12871-018-0482-z

Other articles of this Issue 1/2018

BMC Anesthesiology 1/2018 Go to the issue