Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Modulating Mitochondrial Dynamics Mitigates Cognitive Impairment in Rats with Myocardial Infarction

Author(s): Kewarin Jinawong, Chanon Piamsiri, Nattayaporn Apaijai, Chayodom Maneechote, Busarin Arunsak, Wichwara Nawara, Chanisa Thonusin, Hiranya Pintana, Nipon Chattipakorn and Siriporn C. Chattipakorn*

Volume 22, Issue 10, 2024

Published on: 31 January, 2024

Page: [1749 - 1760] Pages: 12

DOI: 10.2174/1570159X22666240131114913

Price: $65

conference banner
Abstract

Background: We have previously demonstrated that oxidative stress and brain mitochondrial dysfunction are key mediators of brain pathology during myocardial infarction (MI).

Objective: To investigate the beneficial effects of mitochondrial dynamic modulators, including mitochondrial fission inhibitor (Mdivi-1) and mitochondrial fusion promotor (M1), on cognitive function and molecular signaling in the brain of MI rats in comparison with the effect of enalapril.

Methods: Male rats were assigned to either sham or MI operation. In the MI group, rats with an ejection Fraction less than 50% were included, and then they received one of the following treatments for 5 weeks: vehicle, enalapril, Mdivi-1, or M1. Cognitive function was tested, and the brains were used for molecular study.

Results: MI rats exhibited cardiac dysfunction with systemic oxidative stress. Cognitive impairment was found in MI rats, along with dendritic spine loss, blood-brain barrier (BBB) breakdown, brain mitochondrial dysfunction, and decreased mitochondrial and increased glycolysis metabolism, without the alteration of APP, BACE-1, Tau and p-Tau proteins. Treatment with Mdivi-1, M1, and enalapril equally improved cognitive function in MI rats. All treatments decreased dendritic spine loss, brain mitochondrial oxidative stress, and restored mitochondrial metabolism. Brain mitochondrial fusion was recovered only in the Mdivi-1-treated group.

Conclusion: Mitochondrial dynamics modulators improved cognitive function in MI rats through a reduction of systemic oxidative stress and brain mitochondrial dysfunction and the enhancement of mitochondrial metabolism. In addition, this mitochondrial fission inhibitor increased mitochondrial fusion in MI rats.

Keywords: Myocardial infarction, cognitive impairment, brain metabolism, mitochondrial fission, mitochondrial fusion, mitochondrial dysfunction.

« Previous
Graphical Abstract

[1]
Virani, S.S.; Alonso, A.; Aparicio, H.J.; Benjamin, E.J.; Bittencourt, M.S.; Callaway, C.W.; Carson, A.P.; Chamberlain, A.M.; Cheng, S.; Delling, F.N.; Elkind, M.S.V.; Evenson, K.R.; Ferguson, J.F.; Gupta, D.K.; Khan, S.S.; Kissela, B.M.; Knutson, K.L.; Lee, C.D.; Lewis, T.T.; Liu, J.; Loop, M.S.; Lutsey, P.L.; Ma, J.; Mackey, J.; Martin, S.S.; Matchar, D.B.; Mussolino, M.E.; Navaneethan, S.D.; Perak, A.M.; Roth, G.A.; Samad, Z.; Satou, G.M.; Schroeder, E.B.; Shah, S.H.; Shay, C.M.; Stokes, A.; VanWagner, L.B.; Wang, N.Y.; Tsao, C.W. Heart disease and stroke statistics-2021 update. Circulation, 2021, 143(8), e254-e743.
[http://dx.doi.org/10.1161/CIR.0000000000000950] [PMID: 33501848]
[2]
Severino, P.; D’Amato, A.; Pucci, M.; Infusino, F.; Adamo, F.; Birtolo, L.I.; Netti, L.; Montefusco, G.; Chimenti, C.; Lavalle, C.; Maestrini, V.; Mancone, M.; Chilian, W.M.; Fedele, F. Ischemic heart disease pathophysiology paradigms overview: From plaque activation to microvascular dysfunction. Int. J. Mol. Sci., 2020, 21(21), 8118.
[http://dx.doi.org/10.3390/ijms21218118] [PMID: 33143256]
[3]
Jinawong, K.; Apaijai, N.; Piamsiri, C.; Maneechote, C.; Arunsak, B.; Chunchai, T.; Pintana, H.; Nawara, W.; Chattipakorn, N.; Chattipakorn, S.C. Mild cognitive impairment occurs in rats during the early remodeling phase of myocardial infarction. Neuroscience, 2022, 493, 31-40.
[http://dx.doi.org/10.1016/j.neuroscience.2022.04.018] [PMID: 35487300]
[4]
Chung, T.D.; Linville, R.M.; Guo, Z.; Ye, R.; Jha, R.; Grifno, G.N.; Searson, P.C. Effects of acute and chronic oxidative stress on the blood-brain barrier in 2D and 3D in vitro models. Fluids Barriers CNS, 2022, 19(1), 33.
[http://dx.doi.org/10.1186/s12987-022-00327-x] [PMID: 35551622]
[5]
Benjanuwattra, J.; Apaijai, N.; Chunchai, T.; Kerdphoo, S.; Jaiwongkam, T.; Arunsak, B.; Wongsuchai, S.; Chattipakorn, N.; Chattipakorn, S.C. Metformin preferentially provides neuroprotection following cardiac ischemia/reperfusion in non-diabetic rats. Biochim. Biophys. Acta Mol. Basis Dis., 2020, 1866(10), 165893.
[http://dx.doi.org/10.1016/j.bbadis.2020.165893] [PMID: 32621957]
[6]
Jinawong, K.; Apaijai, N.; Wongsuchai, S.; Pratchayasakul, W.; Chattipakorn, N.; Chattipakorn, S.C. Necrostatin-1 mitigates cognitive dysfunction in prediabetic rats with no alteration in insulin sensitivity. Diabetes, 2020, 69(7), 1411-1423.
[http://dx.doi.org/10.2337/db19-1128] [PMID: 32345751]
[7]
Leech, T.; Apaijai, N.; Palee, S.; Higgins, L.A.; Maneechote, C.; Chattipakorn, N.; Chattipakorn, S.C. Acute administration of metformin prior to cardiac ischemia/reperfusion injury protects brain injury. Eur. J. Pharmacol., 2020, 885, 173418.
[http://dx.doi.org/10.1016/j.ejphar.2020.173418] [PMID: 32750367]
[8]
Perez Ortiz, J.M.; Swerdlow, R.H. Mitochondrial dysfunction in Alzheimer’s disease: Role in pathogenesis and novel therapeutic opportunities. Br. J. Pharmacol., 2019, 176(18), 3489-3507.
[http://dx.doi.org/10.1111/bph.14585] [PMID: 30675901]
[9]
Apaijai, N.; Inthachai, T.; Lekawanvijit, S.; Chattipakorn, S.C.; Chattipakorn, N. Effects of dipeptidyl peptidase-4 inhibitor in insulin-resistant rats with myocardial infarction. J. Endocrinol., 2016, 229(3), 245-258.
[http://dx.doi.org/10.1530/JOE-16-0096] [PMID: 27044778]
[10]
Althammer, F.; Ferreira-Neto, H.C.; Rubaharan, M.; Roy, R.K.; Patel, A.A.; Murphy, A.; Cox, D.N.; Stern, J.E. Three-dimensional morphometric analysis reveals time-dependent structural changes in microglia and astrocytes in the central amygdala and hypothalamic paraventricular nucleus of heart failure rats. J. Neuroinflammation, 2020, 17(1), 221.
[http://dx.doi.org/10.1186/s12974-020-01892-4] [PMID: 32703230]
[11]
Surinkaew, P.; Apaijai, N.; Sawaddiruk, P.; Jaiwongkam, T.; Kerdphoo, S.; Chattipakorn, N.; Chattipakorn, S.C. Mitochondrial fusion promoter alleviates brain damage in rats with cardiac ischemia/reperfusion injury. J. Alzheimers Dis., 2020, 77(3), 993-1003.
[http://dx.doi.org/10.3233/JAD-200495] [PMID: 32804148]
[12]
Cassidy-Stone, A.; Chipuk, J.E.; Ingerman, E.; Song, C.; Yoo, C.; Kuwana, T.; Kurth, M.J.; Shaw, J.T.; Hinshaw, J.E.; Green, D.R.; Nunnari, J. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev. Cell, 2008, 14(2), 193-204.
[http://dx.doi.org/10.1016/j.devcel.2007.11.019] [PMID: 18267088]
[13]
Ongnok, B.; Maneechote, C.; Chunchai, T.; Pantiya, P.; Arunsak, B.; Nawara, W.; Chattipakorn, N.; Chattipakorn, S.C. Modulation of mitochondrial dynamics rescues cognitive function in rats with ‘doxorubicin‐induced chemobrain’ via mitigation of mitochondrial dysfunction and neuroinflammation. FEBS J., 2022, 289(20), 6435-6455.
[http://dx.doi.org/10.1111/febs.16474] [PMID: 35514149]
[14]
Faria-Pereira, A.; Morais, V.A. Synapses: The brain’s energy-demanding sites. Int. J. Mol. Sci., 2022, 23(7), 3627.
[http://dx.doi.org/10.3390/ijms23073627] [PMID: 35408993]
[15]
Mergenthaler, P.; Lindauer, U.; Dienel, G.A.; Meisel, A. Sugar for the brain: The role of glucose in physiological and pathological brain function. Trends Neurosci., 2013, 36(10), 587-597.
[http://dx.doi.org/10.1016/j.tins.2013.07.001] [PMID: 23968694]
[16]
Shah, K.; DeSilva, S.; Abbruscato, T. The role of glucose transporters in brain disease: Diabetes and Alzheimer’s Disease. Int. J. Mol. Sci., 2012, 13(12), 12629-12655.
[http://dx.doi.org/10.3390/ijms131012629] [PMID: 23202918]
[17]
Zhang, X.; Alshakhshir, N.; Zhao, L. Glycolytic metabolism, brain resilience, and Alzheimer’s disease. Front. Neurosci., 2021, 15, 662242.
[http://dx.doi.org/10.3389/fnins.2021.662242] [PMID: 33994936]
[18]
Ponikowski, P.; Voors, A.A.; Anker, S.D.; Bueno, H.; Cleland, J.G.F.; Coats, A.J.S.; Falk, V.; González-Juanatey, J.R.; Harjola, V.P.; Jankowska, E.A.; Jessup, M.; Linde, C.; Nihoyannopoulos, P.; Parissis, J.T.; Pieske, B.; Riley, J.P.; Rosano, G.M.C.; Ruilope, L.M.; Ruschitzka, F.; Rutten, F.H.; van der Meer, P. 2016 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure. Eur. Heart J., 2016, 37(27), 2129-2200.
[http://dx.doi.org/10.1093/eurheartj/ehw128] [PMID: 27206819]
[19]
Inthachai, T.; Lekawanvijit, S.; Kumfu, S.; Apaijai, N.; Pongkan, W.; Chattipakorn, S.C.; Chattipakorn, N. Dipeptidyl peptidase-4 inhibitor improves cardiac function by attenuating adverse cardiac remodelling in rats with chronic myocardial infarction. Exp. Physiol., 2015, 100(6), 667-679.
[http://dx.doi.org/10.1113/EP085108] [PMID: 25823534]
[20]
Borchert, T.; Hess, A.; Lukačević, M.; Ross, T.L.; Bengel, F.M.; Thackeray, J.T. Angiotensin-converting enzyme inhibitor treatment early after myocardial infarction attenuates acute cardiac and neuroinflammation without effect on chronic neuroinflammation. Eur. J. Nucl. Med. Mol. Imaging, 2020, 47(7), 1757-1768.
[http://dx.doi.org/10.1007/s00259-020-04736-8] [PMID: 32125488]
[21]
Cha, K.; Jeong, W.J.; Kim, H.M.; So, B.H. Intravenous zoletil administration for the purpose of suicide. Clin. Exp. Emerg. Med., 2021, 8(2), 149-151.
[http://dx.doi.org/10.15441/ceem.20.050] [PMID: 34237821]
[22]
Lin, H.C.; Thurmon, J.C.; Benson, G.J.; Tranquilli, W.J. Review: Telazol - A review of its pharmacology and use in veterinary medicine. J. Vet. Pharmacol. Ther., 1993, 16(4), 383-418.
[http://dx.doi.org/10.1111/j.1365-2885.1993.tb00206.x] [PMID: 8126757]
[23]
Joint FAO/WHO Expert Committee on Food Additives. Evaluation of certain veterinary drug residues in food: Forty-seventh report of the Joint FAO/WHO Expert Committee on Food Additives; World Health Organization: Geneva, 1998.
[24]
Vogel-Ciernia, A; Wood, MA Examining object location and object recognition memory in mice. Curr. Protoc. Neurosci., 2014, 69, 8.31-1.17.
[http://dx.doi.org/10.1002/0471142301.ns0831s69]
[25]
Pintana, H.; Apaijai, N.; Pratchayasakul, W.; Chattipakorn, N.; Chattipakorn, S.C. Effects of metformin on learning and memory behaviors and brain mitochondrial functions in high fat diet induced insulin resistant rats. Life Sci., 2012, 91(11-12), 409-414.
[http://dx.doi.org/10.1016/j.lfs.2012.08.017] [PMID: 22925597]
[26]
Ongnok, B.; Khuanjing, T.; Chunchai, T.; Pantiya, P.; Kerdphoo, S.; Arunsak, B.; Nawara, W.; Jaiwongkam, T.; Apaijai, N.; Chattipakorn, N.; Chattipakorn, S.C. Donepezil protects against doxorubicin-induced chemobrain in rats via attenuation of inflammation and oxidative stress without interfering with doxorubicin efficacy. Neurotherapeutics, 2021, 18(3), 2107-2125.
[http://dx.doi.org/10.1007/s13311-021-01092-9] [PMID: 34312765]
[27]
Thonusin, C.; IglayReger, H.B.; Soni, T.; Rothberg, A.E.; Burant, C.F.; Evans, C.R. Evaluation of intensity drift correction strategies using MetaboDrift, a normalization tool for multi-batch metabolomics data. J. Chromatogr. A, 2017, 1523, 265-274.
[http://dx.doi.org/10.1016/j.chroma.2017.09.023] [PMID: 28927937]
[28]
Halling, J.F.; Pilegaard, H. PGC-1α-mediated regulation of mitochondrial function and physiological implications. Appl. Physiol. Nutr. Metab., 2020, 45(9), 927-936.
[http://dx.doi.org/10.1139/apnm-2020-0005] [PMID: 32516539]
[29]
Chen, L.; Qin, Y.; Liu, B.; Gao, M.; Li, A.; Li, X.; Gong, G. PGC-1α-mediated mitochondrial quality control: Molecular mechanisms and implications for heart failure. Front. Cell Dev. Biol., 2022, 10, 871357.
[http://dx.doi.org/10.3389/fcell.2022.871357] [PMID: 35721484]
[30]
Huijts, M.; van Oostenbrugge, R.J.; Duits, A.; Burkard, T.; Muzzarelli, S.; Maeder, M.T.; Schindler, R.; Pfisterer, M.E.; Brunner-La Rocca, H.P. Cognitive impairment in heart failure: Results from the Trial of Intensified versus standard Medical therapy in Elderly patients with Congestive Heart Failure (TIME-CHF) randomized trial. Eur. J. Heart Fail., 2013, 15(6), 699-707.
[http://dx.doi.org/10.1093/eurjhf/hft020] [PMID: 23384944]
[31]
Wei, B.; Wu, S.; Wang, Z.; Song, W.; Zhu, J. Comparison of cognitive performance and cardiac function between three different rat models of vascular dementia. Neuropsychiatr. Dis. Treat., 2022, 18, 19-28.
[http://dx.doi.org/10.2147/NDT.S338226] [PMID: 35018098]
[32]
Chouchani, E.T.; Pell, V.R.; Gaude, E.; Aksentijević, D.; Sundier, S.Y.; Robb, E.L.; Logan, A.; Nadtochiy, S.M.; Ord, E.N.J.; Smith, A.C.; Eyassu, F.; Shirley, R.; Hu, C.H.; Dare, A.J.; James, A.M.; Rogatti, S.; Hartley, R.C.; Eaton, S.; Costa, A.S.H.; Brookes, P.S.; Davidson, S.M.; Duchen, M.R.; Saeb-Parsy, K.; Shattock, M.J.; Robinson, A.J.; Work, L.M.; Frezza, C.; Krieg, T.; Murphy, M.P. Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature, 2014, 515(7527), 431-435.
[http://dx.doi.org/10.1038/nature13909] [PMID: 25383517]
[33]
Yu, T.; Robotham, J.L.; Yoon, Y. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc. Natl. Acad. Sci., 2006, 103(8), 2653-2658.
[http://dx.doi.org/10.1073/pnas.0511154103] [PMID: 16477035]
[34]
Addington, C.P.; Roussas, A.; Dutta, D.; Stabenfeldt, S.E. Endogenous repair signaling after brain injury and complementary bioengineering approaches to enhance neural regeneration. Biomark. Insights, 2015, 10s1(Suppl. 1), BMI.S20062.
[http://dx.doi.org/10.4137/BMI.S20062] [PMID: 25983552]
[35]
Cobbs, C.S.; Fenoy, A.; Bredt, D.S.; Noble, L.J. Expression of nitric oxide synthase in the cerebral microvasculature after traumatic brain injury in the rat. Brain Res., 1997, 751(2), 336-338.
[http://dx.doi.org/10.1016/S0006-8993(96)01429-1] [PMID: 9099824]
[36]
Kaplan, A.; Yabluchanskiy, A.; Ghali, R.; Altara, R.; Booz, G.W.; Zouein, F.A. Cerebral blood flow alteration following acute myocardial infarction in mice. Biosci. Rep., 2018, 38(5), BSR20180382.
[http://dx.doi.org/10.1042/BSR20180382] [PMID: 30061176]
[37]
Dewanjee, S.; Chakraborty, P.; Bhattacharya, H.; Chacko, L.; Singh, B.; Chaudhary, A.; Javvaji, K.; Pradhan, S.R.; Vallamkondu, J.; Dey, A.; Kalra, R.S.; Jha, N.K.; Jha, S.K.; Reddy, P.H.; Kandimalla, R. Altered glucose metabolism in Alzheimer’s disease: Role of mitochondrial dysfunction and oxidative stress. Free Radic. Biol. Med., 2022, 193(Pt 1), 134-157.
[http://dx.doi.org/10.1016/j.freeradbiomed.2022.09.032] [PMID: 36206930]
[38]
Fukumitsu, K.; Fujishima, K.; Yoshimura, A.; Wu, Y.K.; Heuser, J.; Kengaku, M. Synergistic action of dendritic mitochondria and creatine kinase maintains ATP homeostasis and actin dynamics in growing neuronal dendrites. J. Neurosci., 2015, 35(14), 5707-5723.
[http://dx.doi.org/10.1523/JNEUROSCI.4115-14.2015] [PMID: 25855183]
[39]
Satoh, J.; Yamamoto, Y.; Asahina, N.; Kitano, S.; Kino, Y. RNA-Seq data mining: Downregulation of NeuroD6 serves as a possible biomarker for Alzheimer’s disease brains. Dis. Markers, 2014, 2014, 1-10.
[http://dx.doi.org/10.1155/2014/123165] [PMID: 25548427]
[40]
Deng, S.; Ai, Y.; Gong, H.; Feng, Q.; Li, X.; Chen, C.; Liu, Z.; Wang, Y.; Peng, Q.; Zhang, L. Mitochondrial dynamics and protective effects of a mitochondrial division inhibitor, Mdivi-1, in lipopolysaccharide-induced brain damage. Biochem. Biophys. Res. Commun., 2018, 496(3), 865-871.
[http://dx.doi.org/10.1016/j.bbrc.2018.01.136] [PMID: 29395086]
[41]
Maneechote, C.; Chunchai, T.; Apaijai, N.; Chattipakorn, N.; Chattipakorn, S.C. Pharmacological targeting of mitochondrial fission and fusion alleviates cognitive impairment and brain pathologies in pre-diabetic rats. Mol. Neurobiol., 2022, 59(6), 3690-3702.
[http://dx.doi.org/10.1007/s12035-022-02813-7] [PMID: 35364801]
[42]
Bordt, E.A.; Zhang, N.; Waddell, J.; Polster, B.M. The non-specific Drp1 inhibitor mdivi-1 has modest biochemical antioxidant activity. Antioxidants, 2022, 11(3), 450.
[http://dx.doi.org/10.3390/antiox11030450] [PMID: 35326100]
[43]
Maneechote, C.; Palee, S.; Kerdphoo, S.; Jaiwongkam, T.; Chattipakorn, S.C.; Chattipakorn, N. Balancing mitochondrial dynamics via increasing mitochondrial fusion attenuates infarct size and left ventricular dysfunction in rats with cardiac ischemia/reperfusion injury. Clin. Sci., 2019, 133(3), 497-513.
[http://dx.doi.org/10.1042/CS20190014] [PMID: 30705107]
[44]
Guo, C.; Sun, L.; Chen, X.; Zhang, D. Oxidative stress, mitochondrial damage and neurodegenerative diseases. Neural Regen. Res., 2013, 8(21), 2003-2014.
[PMID: 25206509]
[45]
Yao, C.H.; Wang, R.; Wang, Y.; Kung, C.P.; Weber, J.D.; Patti, G.J. Mitochondrial fusion supports increased oxidative phosphorylation during cell proliferation. eLife, 2019, 8, e41351.
[http://dx.doi.org/10.7554/eLife.41351] [PMID: 30694178]
[46]
Dabrowska, A.; Venero, J.L.; Iwasawa, R.; Hankir, M.; Rahman, S.; Boobis, A.; Hajji, N. PGC-1α controls mitochondrial biogenesis and dynamics in lead-induced neurotoxicity. Aging, 2015, 7(9), 629-643.
[http://dx.doi.org/10.18632/aging.100790] [PMID: 26363853]
[47]
Picca, A.; Lezza, A.M.S. Regulation of mitochondrial biogenesis through TFAM-mitochondrial DNA interactions. Mitochondrion, 2015, 25, 67-75.
[http://dx.doi.org/10.1016/j.mito.2015.10.001] [PMID: 26437364]
[48]
Kang, I.; Chu, C.T.; Kaufman, B.A. The mitochondrial transcription factor TFAM in neurodegeneration: Emerging evidence and mechanisms. FEBS Lett., 2018, 592(5), 793-811.
[http://dx.doi.org/10.1002/1873-3468.12989] [PMID: 29364506]
[49]
Zuccalà, G.; Onder, G.; Marzetti, E.; Monaco, M.R.L.; Cesari, M.; Cocchi, A.; Carbonin, P.; Bernabei, R. Use of angiotensin-converting enzyme inhibitors and variations in cognitive performance among patients with heart failure. Eur. Heart J., 2005, 26(3), 226-233.
[http://dx.doi.org/10.1093/eurheartj/ehi058] [PMID: 15618043]
[50]
Maneechote, C.; Palee, S.; Kerdphoo, S.; Jaiwongkam, T.; Chattipakorn, S.C.; Chattipakorn, N. Modulating mitochondrial dynamics attenuates cardiac ischemia-reperfusion injury in prediabetic rats. Acta Pharmacol. Sin., 2022, 43(1), 26-38.
[http://dx.doi.org/10.1038/s41401-021-00626-3] [PMID: 33712720]
[51]
Maneechote, C.; Pintana, H.; Kerdphoo, S.; Janjek, S.; Chattipakorn, N.; Chattipakorn, S.C. Differential temporal therapies with pharmacologically targeted mitochondrial fission/fusion protect the brain against acute myocardial ischemia-reperfusion injury in prediabetic rats: The crosstalk between mitochondrial apoptosis and inflammation. Eur. J. Pharmacol., 2023, 956, 175939.
[http://dx.doi.org/10.1016/j.ejphar.2023.175939] [PMID: 37536625]
[52]
Thong, E.H.E.; Quek, E.J.W.; Loo, J.H.; Yun, C.Y.; Teo, Y.N.; Teo, Y.H.; Leow, A.S.T.; Li, T.Y.W.; Sharma, V.K.; Tan, B.Y.Q.; Yeo, L.L.L.; Chong, Y.F.; Chan, M.Y.; Sia, C.H. Acute myocardial infarction and risk of cognitive impairment and dementia: A review. Biology, 2023, 12(8), 1154.
[http://dx.doi.org/10.3390/biology12081154] [PMID: 37627038]

Rights & Permissions Print Cite
Article Metrics
27
2
Wayfinder Image
© 2024 Bentham Science Publishers | Privacy Policy