The Potential Neuroprotective Role of Citicoline in Hepatic Encephalopathy

References

• Hadjihambi A, Arias N, Sheikh M, Jalan R. Hepatic encephalopathy: a critical current review. Hepatol Int. 2018;12(1):135–147. doi:10.1007/s12072-017-9812-3
   Web of Science ®Google Scholar
• Heidari R, Jamshidzadeh A, Ommati MM, et al. Ammonia-induced mitochondrial impairment is intensified by manganese co-exposure: relevance to the management of subclinical hepatic encephalopathy and cirrhosis-associated brain injury. Clin exp hepatol. 2019;5(2):109–117. doi:10.5114/ceh.2019.85071
   Web of Science ®Google Scholar
• Heidari R. Brain mitochondria as potential therapeutic targets for managing hepatic encephalopathy. Life Sci. 2019;218:65–80. doi:10.1016/j.lfs.2018.12.030
   Web of Science ®Google Scholar
• Ferenci P. Hepatic encephalopathy. Gastroenterol Rep. 2017;5(2):138–147. doi:10.1093/gastro/gox013
   Google Scholar
• Musgrave H, Hilsabeck RC. Hepatic encephalopathy. In: Ravdin LD, Katzen HL (eds.), Handbook on the Neuropsychology of Aging and Dementia. Springer; 2019:689–710.
   Google Scholar
• Hassan A, Tsuda Y, Asai A, et al. Effects of oral l-carnitine on liver functions after transarterial chemoembolization in intermediate-stage hcc patients. Mediators Inflamm. 2015;2015.
   Web of Science ®Google Scholar
• Sakai Y, Nishikawa H, Enomoto H, et al. Effect of l-carnitine in patients with liver cirrhosis on energy metabolism using indirect calorimetry: a pilot study. J Clin Med Res. 2016;8(12):863. doi:10.14740/jocmr2734w
   Google Scholar
• Saeed RMA, Ahmed HH, Saleh AAS, Ahmed YS. Curative role of lactulose, l-carnitine, alpha-lipoic acid and combination of l-carnitine and alpha-lipoic acid in a rat model of acute hepatic encephalopathy: biochemical observations. Trop J Pharm Res. 2017;16(9):2161–2168. doi:10.4314/tjpr.v16i9.17
   Web of Science ®Google Scholar
• Jamshidzadeh A, Niknahad H, Heidari R, Zarei M, Ommati MM, Khodaei F. Carnosine protects brain mitochondria under hyperammonemic conditions: relevance to hepatic encephalopathy treatment. Pharma Nutri. 2017;5(2):58–63. doi:10.1016/j.phanu.2017.02.004
   Google Scholar
• Milewski K, Hilgier W, Fręśko I, et al. Carnosine reduces oxidative stress and reverses attenuation of righting and postural reflexes in rats with thioacetamide-induced liver failure. Neurochem Res. 2016;41(1–2):376–384. doi:10.1007/s11064-015-1821-9
   Web of Science ®Google Scholar
• Chepkova AN, Sergeeva OA, Haas HL. Taurine rescues hippocampal long-term potentiation from ammonia-induced impairment. Neurobiol Dis. 2006;23(3):512–521. doi:10.1016/j.nbd.2006.04.006
   Web of Science ®Google Scholar
• Boer LA, Panatto JP, Fagundes DA, et al. Inhibition of mitochondrial respiratory chain in the brain of rats after hepatic failure induced by carbon tetrachloride is reversed by antioxidants. Brain Res Bull. 2009;80(1–2):75–78. doi:10.1016/j.brainresbull.2009.04.009
   Web of Science ®Google Scholar
• Bémeur C, Vaquero J, Desjardins P, Butterworth RF. N-acetylcysteine attenuates cerebral complications of non-acetaminophen-induced acute liver failure in mice: antioxidant and anti-inflammatory mechanisms. Metab Brain Dis. 2010;25(2):241–249. doi:10.1007/s11011-010-9201-2
   PubMed Web of Science ®Google Scholar
• Ommati MM, Jamshidzadeh A, Niknahad H, et al. N-acetylcysteine treatment blunts liver failure-associated impairment of locomotor activity. Pharm Nutri. 2017;5(4):141–147. doi:10.1016/j.phanu.2017.10.003
   Google Scholar
• Secades J. Citicoline in the treatment of cognitive impairment. J Neurol Exp Neurosci. 2019;5(1):14–26. doi:10.17756/jnen.2019-047
   Google Scholar
• Secades JJ, Alvarez-Sabin J, Castillo J, et al. Citicoline for acute ischemic stroke: a systematic review and formal meta-analysis of randomized, double-blind, and placebo-controlled trials. J Stroke Cerebrovasc Dis. 2016;25(8):1984–1996. doi:10.1016/j.jstrokecerebrovasdis.2016.04.010
   PubMed Web of Science ®Google Scholar
• Grieb P. Neuroprotective properties of citicoline: facts, doubts and unresolved issues. CNS Drugs. 2014;28(3):185–193.
   Web of Science ®Google Scholar
• Iulia C, Ruxandra T, Costin L-B, Liliana-Mary V. Citicoline–a neuroprotector with proven effects on glaucomatous disease. Romanian j Ophthalmol. 2017;61(3):152. doi:10.22336/rjo.2017.29
   Google Scholar
• Roohi-Azizi M, Arabzadeh S, Amidfar M, et al. Citicoline combination therapy for major depressive disorder: a randomized, double-blind, placebo-controlled trial. Clin Neuropharmacol. 2017;40(1):1–5. doi:10.1097/WNF.0000000000000185
   Web of Science ®Google Scholar
• Yu H, Qing H, Lei Z. Cytidine diphosphate choline improves the outcome of cardiac arrest vs epinephrine in rat model. Am J Emerg Med. 2013;31(7):1022–1028. doi:10.1016/j.ajem.2013.03.018
   Web of Science ®Google Scholar
• Shabrang B, Jamshidzadeh A, Farjam M, Ebrahimpour A, Koohi-Hosseinabadi O. Concurrent assessment of calpain and caspase3 activities in brains of mice with acetaminophen-induced acute hepatic encephalopathy. Metab Brain Dis. 2017;32(6):2139–2142. doi:10.1007/s11011-017-0096-z
   Web of Science ®Google Scholar
• Carter RJ, Morton J, Dunnett SB. Motor coordination and balance in rodents. Curr Protocols Neurosci. 2001;15(1):8.12.1–8. 4. doi:10.1002/0471142301.ns0812s15
   Google Scholar
• Metz GA, Merkler D, Dietz V, Schwab ME, Fouad K. Efficient testing of motor function in spinal cord injured rats. Brain Res. 2000;883(2):165–177. doi:10.1016/S0006-8993(00)02778-5
   PubMed Web of Science ®Google Scholar
• Heidari R, Jamshidzadeh A, Niknahad H, et al. Effect of taurine on chronic and acute liver injury: focus on blood and brain ammonia. Toxicol Rep. 2016;3:870–879. doi:10.1016/j.toxrep.2016.04.002
   PubMed Web of Science ®Google Scholar
• Ommati MM, Heidari R, Ghanbarinejad V, Aminian A, Abdoli N, Niknahad H. The neuroprotective properties of carnosine in a mouse model of manganism is mediated via mitochondria regulating and antioxidative mechanisms. Nutr Neurosci. 2019;:1–13. doi:10.1080/1028415X.2018.1552399
   Web of Science ®Google Scholar
• Ommati MM, Heidari R, Ghanbarinejad V, Abdoli N, Niknahad H. Taurine treatment provides neuroprotection in a mouse model of manganism. Biol Trace Elem Res. 2019;190(2):384–395. doi:10.1007/s12011-018-1552-2
   PubMed Web of Science ®Google Scholar
• Heidari R, Moezi L, Asadi B, Ommati MM, Azarpira N. Hepatoprotective effect of boldine in a bile duct ligated rat model of cholestasis/cirrhosis. PharmaNutrition. 2017;5(3):109–117. doi:10.1016/j.phanu.2017.07.001
   Google Scholar
• Jamshidzadeh A, Heidari R, Latifpour Z, et al. Carnosine ameliorates liver fibrosis and hyperammonemia in cirrhotic rats. Clin Res Hepatol Gastroenterol. 2017;41(4):424–434. doi:10.1016/j.clinre.2016.12.010
   PubMed Web of Science ®Google Scholar
• Gupta R, Dubey D, Kannan G, Flora S. Concomitant administration of moringa oleifera seed powder in the remediation of arsenic‐induced oxidative stress in mouse. Cell Biol Int. 2007;31(1):44–56. doi:10.1016/j.cellbi.2006.09.007
   PubMed Web of Science ®Google Scholar
• Socci D, Bjugstad K, Jones H, Pattisapu J, Arendash G. Evidence that oxidative stress is associated with the pathophysiology of inherited hydrocephalus in the h-tx rat model. Exp Neurol. 1999;155(1):109–117. doi:10.1006/exnr.1998.6969
   PubMed Web of Science ®Google Scholar
• Ommati MM, Farshad O, Niknahad H, et al. Cholestasis-associated reproductive toxicity in male and female rats: the fundamental role of mitochondrial impairment and oxidative stress. Toxicol Lett. 2019;316:60–72. doi:10.1016/j.toxlet.2019.09.009
   Web of Science ®Google Scholar
• Heidari R, Behnamrad S, Khodami Z, Ommati MM, Azarpira N, Vazin A. The nephroprotective properties of taurine in colistin-treated mice is mediated through the regulation of mitochondrial function and mitigation of oxidative stress. Biomed Pharmacother. 2019;109:103–111. doi:10.1016/j.biopha.2018.10.093
   PubMed Web of Science ®Google Scholar
• Heidari R, Ahmadi A, Mohammadi H, Ommati MM, Azarpira N, Niknahad H. Mitochondrial dysfunction and oxidative stress are involved in the mechanism of methotrexate-induced renal injury and electrolytes imbalance. Biomed Pharmacother. 2018;107:834–840. doi:10.1016/j.biopha.2018.08.050
   PubMed Web of Science ®Google Scholar
• Ommati MM, Jamshidzadeh A, Heidari R, et al. Carnosine and histidine supplementation blunt lead-induced reproductive toxicity through antioxidative and mitochondria-dependent mechanisms. Biol Trace Elem Res. 2019;187(1):151–162. doi:10.1007/s12011-018-1358-2
   PubMed Web of Science ®Google Scholar
• Karamikhah R, Jamshidzadeh A, Azarpira N, Saeedi A, Heidari R. Propylthiouracil-induced liver injury in mice and the protective role of taurine. Pharm Sci. 2015;21(2):94–101. doi:10.15171/PS.2015.23
   Google Scholar
• Heidari R, Babaei H, Roshangar L, Eghbal MA. Effects of enzyme induction and/or glutathione depletion on methimazole-induced hepatotoxicity in mice and the protective role of n-acetylcysteine. Advan Pharm Bull. 2014;4(1):21.
   Google Scholar
• Benzie IF, Strain JJ. The ferric reducing ability of plasma (frap) as a measure of “antioxidant power”: the frap assay. Anal Biochem. 1996;239(1):70–76. doi:10.1006/abio.1996.0292
   PubMed Web of Science ®Google Scholar
• Ozgen M, Reese RN, Tulio AZ, Scheerens JC, Miller AR. Modified 2, 2-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (abts) method to measure antioxidant capacity of selected small fruits and comparison to ferric reducing antioxidant power (frap) and 2, 2 ‘-diphenyl-1-picrylhydrazyl (dpph) methods. J Agric Food Chem. 2006;54(4):1151–1157. doi:10.1021/jf051960d
   PubMed Web of Science ®Google Scholar
• Shafiekhani M, Ommati MM, Azarpira N, Heidari R, Salarian AA. Glycine supplementation mitigates lead-induced renal injury in mice. J Exp Pharmacol. 2019;11:15–22. doi:10.2147/JEP.S190846
   PubMedGoogle Scholar
• Butterworth RF. Hepatic encephalopathy. The Liver. 2020;615–629.
   Google Scholar
• Lima LCD, Miranda AS, Ferreira RN, Rachid MA, ACS E Silva. Hepatic encephalopathy: lessons from preclinical studies. World J Hepatol. 2019;11(2):173. doi:10.4254/wjh.v11.i2.173
   Web of Science ®Google Scholar
• Butterworth RF, Norenberg MD, Felipo V, et al. Experimental models of hepatic encephalopathy: ishen guidelines. Liver Int. 2009;29(6):783–788. doi:10.1111/j.1478-3231.2009.02034.x
   Web of Science ®Google Scholar
• Ebadollahi Natanzi AR, Mahmoudian S, Minaeie B, Sabzevari O. Hepatoprotective activity of phloretin and hydroxychalcones against acetaminophen induced hepatotoxicity in mice. Iran J Pharm Sci. 2011;7(2):89–97.
   Google Scholar
• Görg B, Karababa A, Schütz E, et al. O-glcnacylation-dependent upregulation of ho1 triggers ammonia-induced oxidative stress and senescence in hepatic encephalopathy. J Hepatol. 2019;71(5):930–941. doi:10.1016/j.jhep.2019.06.020
   Web of Science ®Google Scholar
• Zacharias HD, Zacharias AP, Gluud LL, Morgan MY. Pharmacotherapies that specifically target ammonia for the prevention and treatment of hepatic encephalopathy in adults with cirrhosis. Cochrane Database Syst Rev. 2019;6.
   Web of Science ®Google Scholar
• Griffin JW, Bradshaw PC. Effects of a high protein diet and liver disease in an in silico model of human ammonia metabolism. Theor Biol Med Model. 2019;16(1):11. doi:10.1186/s12976-019-0109-1
   Web of Science ®Google Scholar
• Saleem TH, Shehata GA, Toghan R, et al. Assessments of amino acids, ammonia and oxidative stress among cohort of egyptian autistic children: correlations with electroencephalogram and disease severity. Neuropsychiatr Dis Treat. 2020;16:11. doi:10.2147/NDT.S233105
   Web of Science ®Google Scholar
• Shah SWA, Chen J, Han Q, Xu Y, Ishfaq M, Teng X. Ammonia inhalation impaired immune function and mitochondrial integrity in the broilers bursa of fabricius: implication of oxidative stress and apoptosis. Ecotoxicol Environ Saf. 2020;190:110078. doi:10.1016/j.ecoenv.2019.110078
   PubMed Web of Science ®Google Scholar
• Heidari R. The footprints of mitochondrial impairment and cellular energy crisis in the pathogenesis of xenobiotics-induced nephrotoxicity, serum electrolytes imbalance, and fanconi’s syndrome: a comprehensive review. Toxicology. 2019;423:1–31. doi:10.1016/j.tox.2019.05.002
   Web of Science ®Google Scholar
• Reddy PVB, Murthy CR, Reddanna P. Fulminant hepatic failure induced oxidative stress in nonsynaptic mitochondria of cerebral cortex in rats. Neurosci Lett. 2004;368(1):15–20. doi:10.1016/j.neulet.2004.06.046
   PubMed Web of Science ®Google Scholar
• Fadillioglu E, Gursul C, Iraz M. Effects of caffeic acid phenethyl ester on thioacetamide-induced hepatic encephalopathy in rats. Prog Neuropsychopharmacol Biol Psychiatry. 2010;34(8):1440–1445. doi:10.1016/j.pnpbp.2010.07.034
   Web of Science ®Google Scholar
• Shawcross DL, Shabbir SS, Taylor NJ, Hughes RD. Ammonia and the neutrophil in the pathogenesis of hepatic encephalopathy in cirrhosis. Hepatology. 2010;51(3):1062–1069. doi:10.1002/hep.23367
   PubMed Web of Science ®Google Scholar
• Norenberg MD, Baker L, Norenberg LOB, Blicharska J, Bruce-Gregorios JH, Neary JT. Ammonia-induced astrocyte swelling in primary culture. Neurochem Res. 1991;16(7):833–836. doi:10.1007/BF00965694
   PubMed Web of Science ®Google Scholar
• Bobermin LD, Wartchow KM, Flores MP, Leite MC, Quincozes-Santos A, Gonçalves C-A. Ammonia-induced oxidative damage in neurons is prevented by resveratrol and lipoic acid with participation of heme oxygenase 1. NeuroToxicology. 2015;49:28–35. doi:10.1016/j.neuro.2015.05.005
   PubMed Web of Science ®Google Scholar
• Norenberg MD, Jayakumar A, Rao KR. Oxidative stress in the pathogenesis of hepatic encephalopathy. Metab Brain Dis. 2004;19(3–4):313–329.
   Web of Science ®Google Scholar
• Malaguarnera M, Pistone G, Astuto M, et al. L-carnitine in the treatment of mild or moderate hepatic encephalopathy. Digest Dis. 2003;21(3):271–275. doi:10.1159/000073347
   Web of Science ®Google Scholar
• Grieb P. Citicoline and eye health. In: Handbook of Nutrition, Diet, and the Eye. Elsevier; 2019:585–603.
   Google Scholar
• Zafonte R. Lessons learned from the citicoline brain treatment trial (cobrit). Ann Phys Rehabil Med. 2018;61:e40. doi:10.1016/j.rehab.2018.05.089
   Google Scholar
• Adibhatla RM, Hatcher J, Dempsey R. Citicoline: mechanisms and stroke clinical trials. Neurology. 2019.
   Google Scholar
• Cinar E, Yuce B, Aslan F, Erbakan G. Effect of neuroprotective citicoline eye drops on macular microcirculation. Int Ophthalmol. 2020;40(9):2237–2246. doi:10.1007/s10792-020-01404-6
   Web of Science ®Google Scholar
• Cinar E, Yuce B, Aslan F, Erbakan G. Neuroprotective effect of citicoline eye drops on corneal sensitivity after lasik. J Refract Surg. 2019;35(12):764–770. doi:10.3928/1081597X-20191021-01
   Web of Science ®Google Scholar
• Shaffie N, Shabana ME. Role of citicoline as a protective agent on toluene-induced toxicity in rats. J Arab Soc Med Res. 2019;14(1):14. doi:10.4103/jasmr.jasmr_9_19
   Google Scholar
• Yan M, Huo Y, Yin S, Hu H. Mechanisms of acetaminophen-induced liver injury and its implications for therapeutic interventions. Redox Biol. 2018;17:274–283. doi:10.1016/j.redox.2018.04.019
   PubMed Web of Science ®Google Scholar
• Aminzadeh A, Salarinejad A. Citicoline protects against lead-induced oxidative injury in neuronal pc12 cells. Biochem Cell Biol. 2019;97(6):715–721. doi:10.1139/bcb-2018-0218
   Web of Science ®Google Scholar
• Safavi M, Hosseini-Sharifabad A, Seyed-Yousefi Y, Rabbani M. Protective effects of citicoline and benfotiamine each alone and in combination on streptozotocin-induced memory impairment in mice. Clin Psychopharmacol Neurosci. 2020;18(1):81–92. doi:10.9758/cpn.2020.18.1.81
   Web of Science ®Google Scholar
• Secades JJ, Alvarez-Sabín J, Castillo J, et al. Citicoline for acute ischemic stroke: a systematic review and formal meta-analysis of randomized, double-blind, and placebo-controlled trials. J Stroke Cerebrovasc Dis. 2016;25(8):1984–1996. doi:10.1016/j.jstrokecerebrovasdis.2016.04.010
   PubMed Web of Science ®Google Scholar