Generic placeholder image

Current Alzheimer Research

Editor-in-Chief

ISSN (Print): 1567-2050
ISSN (Online): 1875-5828

Systematic Review Article

Neurodegeneration and Glial Activation Related CSF Biomarker as the Diagnosis of Alzheimer’s Disease: A Systematic Review and an Updated Meta- analysis

Author(s): Yuehan Hao, Xu Liu and Ruixia Zhu*

Volume 19, Issue 1, 2022

Page: [32 - 46] Pages: 15

DOI: 10.2174/1567205018666211208142702

Price: $65

Abstract

Objective: Recently, neuron specific enolase (NSE), Visinin-like protein-1 (VLP-1), neurogranin (Ng), and YKL-40 have been identified as candidates for neuronal degeneration and glial activation biomarkers. Therefore, we perform a comprehensive meta-analysis to assess the diagnostic value of CSF NSE, VLP-1, Ng and YKL-40 in Alzheimer’s disease (AD).

Methods: We searched Pubmed, MEDLINE, EMBASE databases for research about the levels of CSF NSE, VLP-1, Ng and YKL-40 in AD patients compared with controls or other dementia diseases until Dec 2020.

Results: The present meta-analysis contained a total of 51 studies comprising 6248 patients with dementia disorders and 3861 controls. Among them, there were 3262 patients with AD, 2456 patients with mild cognitive impairment (MCI), 173 patients with vascular dementia (VaD), 221 patients with frontotemporal dementia (FTD), and 136 with Lewy bodies dementia (DLB). Our study demonstrated that CSF NSE, VLP-1, Ng and YKL-40 levels were increased in AD as compared to healthy controls. We also observed that the CSF NSE level was higher in AD than VaD, suggesting CSF NSE might act as a key role in distinguishing between AD and VaD. Interestingly, there was a higher VLP-1 expression in AD, and a lower expression in DLB patients. Moreover, we found the CSF Ng level was increased in AD than MCI, implying CSF Ng might be a biomarker for identifying the progression of AD. Additionally, a significantly higher CSF YKL-40 level was detected not only in AD, but also in FTD, DLB, VaD, signifying YKL-40 was not sensitive in the diagnosis of AD.

Conclusion: Our study confirmed that CSF levels of NSE, VLP-1, and Ng could be valuable biomarkers for identifying patients who are more susceptible to AD and distinguishing AD from other neurodegenerative dementia disorders.

Keywords: CSF biomarker, neuron-specific enolase, VLP-1, neurogranin, YKL-40, Alzheimer's disease

[1]
Spence J, Chintapenta M, Kwon HI, Blaszczyk AT. A brief review of three common supplements used in Alzheimer’s disease. Consult Pharm 2017; 32(7): 412-4.
[http://dx.doi.org/10.4140/TCP.n.2017.412] [PMID: 28701253]
[2]
Llorens F, Thüne K, Tahir W, et al. YKL-40 in the brain and cerebrospinal fluid of neurodegenerative dementias. Mol Neurodegener 2017; 12(1): 83.
[http://dx.doi.org/10.1186/s13024-017-0226-4] [PMID: 29126445]
[3]
Wang L, Gao T, Cai T, Li K, Zheng P, Liu J. Cerebrospinal fluid levels of YKL-40 in prodromal Alzheimer’s disease. Neurosci Lett 2020; 715: 134658.
[http://dx.doi.org/10.1016/j.neulet.2019.134658] [PMID: 31794792]
[4]
Hellwig K, Kvartsberg H, Portelius E, et al. Neurogranin and YKL-40: independent markers of synaptic degeneration and neuroinflammation in Alzheimer’s disease. Alzheimers Res Ther 2015; 7: 74.
[http://dx.doi.org/10.1186/s13195-015-0161-y] [PMID: 26698298]
[5]
Braunewell KH, Klein-Szanto AJ. Visinin-like proteins (VSNLs): interaction partners and emerging functions in signal transduction of a subfamily of neuronal Ca2+ -sensor proteins. Cell Tissue Res 2009; 335(2): 301-16.
[http://dx.doi.org/10.1007/s00441-008-0716-3] [PMID: 18989702]
[6]
Laterza OF, Modur VR, Crimmins DL, et al. Identification of novel brain biomarkers. Clin Chem 2006; 52(9): 1713-21.
[http://dx.doi.org/10.1373/clinchem.2006.070912] [PMID: 16858073]
[7]
Díez-Guerra FJ. Neurogranin, a link between calcium/calmodulin and protein kinase C signaling in synaptic plasticity. IUBMB Life 2010; 62(8): 597-606.
[http://dx.doi.org/10.1002/iub.357] [PMID: 20665622]
[8]
de Wilde MC, Overk CR, Sijben JW, Masliah E. Meta-analysis of synaptic pathology in Alzheimer’s disease reveals selective molecular vesicular machinery vulnerability. Alzheimers Dement 2016; 12(6): 633-44.
[http://dx.doi.org/10.1016/j.jalz.2015.12.005] [PMID: 26776762]
[9]
Kvartsberg H, Lashley T, Murray CE, et al. The intact postsynaptic protein neurogranin is reduced in brain tissue from patients with familial and sporadic Alzheimer’s disease. Acta Neuropathol 2019; 137(1): 89-102.
[http://dx.doi.org/10.1007/s00401-018-1910-3] [PMID: 30244311]
[10]
McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology 1984; 34(7): 939-44.
[http://dx.doi.org/10.1212/WNL.34.7.939] [PMID: 6610841]
[11]
Román GC, Tatemichi TK, Erkinjuntti T, et al. Vascular dementia: diagnostic criteria for research studies. Report of the NINDS-AIREN International Workshop. Neurology 1993; 43(2): 250-60.
[http://dx.doi.org/10.1212/WNL.43.2.250] [PMID: 8094895]
[12]
Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E. Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 1999; 56(3): 303-8.
[http://dx.doi.org/10.1001/archneur.56.3.303] [PMID: 10190820]
[13]
McKeith IG. Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): report of the Consortium on DLB International Workshop. J Alzheimers Dis 2006; 9(3)(Suppl.): 417-23.
[http://dx.doi.org/10.3233/JAD-2006-9S347] [PMID: 16914880]
[14]
Faber R. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 1999; 53(5): 1159.
[http://dx.doi.org/10.1212/WNL.53.5.1158-b] [PMID: 10496296]
[15]
Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010; 25(9): 603-5.
[http://dx.doi.org/10.1007/s10654-010-9491-z] [PMID: 20652370]
[16]
Martinez-Merino L, Iridoy M, Galbete A, et al. Evaluation of chitotriosidase and CC-chemokine ligand 18 as biomarkers of microglia activation in amyotrophic lateral sclerosis. Neurodegener Dis 2018; 18(4): 208-15.
[http://dx.doi.org/10.1159/000490920] [PMID: 30134252]
[17]
Heneka MT, Carson MJ, El Khoury J, et al. Neuroinflammation in Alzheimer’s disease. Lancet Neurol 2015; 14(4): 388-405.
[http://dx.doi.org/10.1016/S1474-4422(15)70016-5] [PMID: 25792098]
[18]
Isgrò MA, Bottoni P, Scatena R. Neuron-specific enolase as a biomarker: biochemical and clinical aspects. Adv Exp Med Biol 2015; 867: 125-43.
[http://dx.doi.org/10.1007/978-94-017-7215-0_9] [PMID: 26530364]
[19]
Blennow K, Wallin A, Ekman R. Neuron specific enolase in cerebrospinal fluid: a biochemical marker for neuronal degeneration in dementia disorders? J Neural Transm Park Dis Dement Sect 1994; 8(3): 183-91.
[http://dx.doi.org/10.1007/BF02260939] [PMID: 7748462]
[20]
Parnetti L, Palumbo B, Cardinali L, et al. Cerebrospinal fluid neuron-specific enolase in Alzheimer’s disease and vascular dementia. Neurosci Lett 1995; 183(1-2): 43-5.
[http://dx.doi.org/10.1016/0304-3940(94)11110-5] [PMID: 7746484]
[21]
Whitaker-Azmitia PM, Wingate M, Borella A, Gerlai R, Roder J, Azmitia EC. Transgenic mice overexpressing the neurotrophic factor S-100 beta show neuronal cytoskeletal and behavioral signs of altered aging processes: implications for Alzheimer’s disease and Down’s syndrome. Brain Res 1997; 776(1-2): 51-60.
[http://dx.doi.org/10.1016/S0006-8993(97)01002-0] [PMID: 9439795]
[22]
Schmidt FM, Mergl R, Stach B, Jahn I, Gertz HJ, Schönknecht P. Elevated levels of cerebrospinal fluid neuron-specific enolase (NSE) in Alzheimer’s disease. Neurosci Lett 2014; 570: 81-5.
[http://dx.doi.org/10.1016/j.neulet.2014.04.007] [PMID: 24746933]
[23]
Chaves ML, Camozzato AL, Ferreira ED, et al. Serum levels of S100B and NSE proteins in Alzheimer’s disease patients. J Neuroinflammation 2010; 7: 6.
[http://dx.doi.org/10.1186/1742-2094-7-6] [PMID: 20105309]
[24]
Palumbo B, Siepi D, Sabalich I, Tranfaglia C, Parnetti L. Cerebrospinal fluid neuron-specific enolase: a further marker of Alzheimer’s disease? Funct Neurol 2008; 23(2): 93-6.
[PMID: 18671910]
[25]
Andreasen N, Gottfries J, Vanmechelen E, et al. Evaluation of CSF biomarkers for axonal and neuronal degeneration, gliosis, and beta-amyloid metabolism in Alzheimer’s disease. J Neurol Neurosurg Psychiatry 2001; 71(4): 557-8.
[http://dx.doi.org/10.1136/jnnp.71.4.557] [PMID: 11561022]
[26]
Sulkava R, Viinikka L, Erkinjuntti T, Roine R. Cerebrospinal fluid neuron-specific enolase is decreased in multi-infarct dementia, but unchanged in Alzheimer’s disease. J Neurol Neurosurg Psychiatry 1988; 51(4): 549-51.
[http://dx.doi.org/10.1136/jnnp.51.4.549] [PMID: 3379429]
[27]
Braunewell KH. The visinin-like proteins VILIP-1 and VILIP-3 in Alzheimer’s disease-old wine in new bottles. Front Mol Neurosci 2012; 5: 20.
[http://dx.doi.org/10.3389/fnmol.2012.00020] [PMID: 22375104]
[28]
Mavroudis IA, Petridis F, Chatzikonstantinou S, Karantali E, Kazis D. A meta-analysis on the levels of VILIP-1 in the CSF of Alzheimer’s disease compared to normal controls and other neurodegenerative conditions. Aging Clin Exp Res 2021; 33(2): 265-72.
[http://dx.doi.org/10.1007/s40520-019-01458-2] [PMID: 31939203]
[29]
Kester MI, Teunissen CE, Sutphen C, et al. Cerebrospinal fluid VILIP-1 and YKL-40, candidate biomarkers to diagnose, predict and monitor Alzheimer’s disease in a memory clinic cohort. Alzheimers Res Ther 2015; 7(1): 59.
[http://dx.doi.org/10.1186/s13195-015-0142-1] [PMID: 26383836]
[30]
Lee JM, Blennow K, Andreasen N, et al. The brain injury biomarker VLP-1 is increased in the cerebrospinal fluid of Alzheimer disease patients. Clin Chem 2008; 54(10): 1617-23.
[http://dx.doi.org/10.1373/clinchem.2008.104497] [PMID: 18703769]
[31]
Babić Leko M, Willumsen N, Nikolac Perković M, et al. Association of MAPT haplotype-tagging polymorphisms with cerebrospinal fluid biomarkers of Alzheimer’s disease: A preliminary study in a Croatian cohort. Brain Behav 2018; 8(11): e01128.
[http://dx.doi.org/10.1002/brb3.1128] [PMID: 30329219]
[32]
Tarawneh R, D’Angelo G, Macy E, et al. Visinin-like protein-1: diagnostic and prognostic biomarker in Alzheimer disease. Ann Neurol 2011; 70(2): 274-85.
[http://dx.doi.org/10.1002/ana.22448] [PMID: 21823155]
[33]
Tarawneh R, Lee JM, Ladenson JH, Morris JC, Holtzman DM. CSF VILIP-1 predicts rates of cognitive decline in early Alzheimer disease. Neurology 2012; 78(10): 709-19.
[http://dx.doi.org/10.1212/WNL.0b013e318248e568] [PMID: 22357717]
[34]
Luo X, Hou L, Shi H, et al. CSF levels of the neuronal injury biomarker visinin-like protein-1 in Alzheimer’s disease and dementia with Lewy bodies. J Neurochem 2013; 127(5): 681-90.
[http://dx.doi.org/10.1111/jnc.12331] [PMID: 23800322]
[35]
Tarawneh R, Head D, Allison S, et al. Cerebrospinal Fluid markers of neurodegeneration and rates of brain atrophy in early Alzheimer Disease. JAMA Neurol 2015; 72(6): 656-65.
[http://dx.doi.org/10.1001/jamaneurol.2015.0202] [PMID: 25867677]
[36]
Babić Leko M, Borovečki F, Dejanović N, Hof PR, Šimić G. Predictive value of cerebrospinal fluid visinin-like protein-1 levels for Alzheimer’s Disease early detection and differential diagnosis in patients with mild cognitive impairment. J Alzheimers Dis 2016; 50(3): 765-78.
[http://dx.doi.org/10.3233/JAD-150705] [PMID: 26836160]
[37]
Zhang H, Ng KP, Therriault J, et al. Cerebrospinal fluid phosphorylated tau, visinin-like protein-1, and chitinase-3-like protein 1 in mild cognitive impairment and Alzheimer’s disease. Transl Neurodegener 2018; 7: 23.
[http://dx.doi.org/10.1186/s40035-018-0127-7] [PMID: 30311914]
[38]
Tarawneh R, D’Angelo G, Crimmins D, et al. Diagnostic and prognostic utility of the synaptic marker neurogranin in Alzheimer disease. JAMA Neurol 2016; 73(5): 561-71.
[http://dx.doi.org/10.1001/jamaneurol.2016.0086] [PMID: 27018940]
[39]
Masliah E, Mallory M, Alford M, et al. Altered expression of synaptic proteins occurs early during progression of Alzheimer’s disease. Neurology 2001; 56(1): 127-9.
[http://dx.doi.org/10.1212/WNL.56.1.127] [PMID: 11148253]
[40]
Petersen A, Gerges NZ. Neurogranin regulates CaM dynamics at dendritic spines. Sci Rep 2015; 5: 11135.
[http://dx.doi.org/10.1038/srep11135] [PMID: 26084473]
[41]
Portelius E, Brinkmalm G, Tran AJ, Zetterberg H, Westman-Brinkmalm A, Blennow K. Identification of novel APP/Abeta isoforms in human cerebrospinal fluid. Neurodegener Dis 2009; 6(3): 87-94.
[http://dx.doi.org/10.1159/000203774] [PMID: 19229112]
[42]
Kester MI, Teunissen CE, Crimmins DL, et al. Neurogranin as a cerebrospinal fluid biomarker for synaptic loss in symptomatic Alzheimer disease. JAMA Neurol 2015; 72(11): 1275-80.
[http://dx.doi.org/10.1001/jamaneurol.2015.1867] [PMID: 26366630]
[43]
Kvartsberg H, Duits FH, Ingelsson M, et al. Cerebrospinal fluid levels of the synaptic protein neurogranin correlates with cognitive decline in prodromal Alzheimer’s disease. Alzheimers Dement 2015; 11(10): 1180-90.
[http://dx.doi.org/10.1016/j.jalz.2014.10.009] [PMID: 25533203]
[44]
Portelius E, Olsson B, Höglund K, et al. Cerebrospinal fluid neurogranin concentration in neurodegeneration: relation to clinical phenotypes and neuropathology. Acta Neuropathol 2018; 136(3): 363-76.
[http://dx.doi.org/10.1007/s00401-018-1851-x] [PMID: 29700597]
[45]
Janelidze S, Hertze J, Zetterberg H, et al. Cerebrospinal fluid neurogranin and YKL-40 as biomarkers of Alzheimer’s disease. Ann Clin Transl Neurol 2015; 3(1): 12-20.
[http://dx.doi.org/10.1002/acn3.266] [PMID: 26783546]
[46]
Pereira JB, Westman E, Hansson O. Association between cerebrospinal fluid and plasma neurodegeneration biomarkers with brain atrophy in Alzheimer’s disease. Neurobiol Aging 2017; 58: 14-29.
[http://dx.doi.org/10.1016/j.neurobiolaging.2017.06.002] [PMID: 28692877]
[47]
De Vos A, Struyfs H, Jacobs D, et al. The cerebrospinal fluid neurogranin/bace1 ratio is a potential correlate of cognitive decline in Alzheimer’s disease. J Alzheimers Dis 2016; 53(4): 1523-38.
[http://dx.doi.org/10.3233/JAD-160227] [PMID: 27392859]
[48]
Wang L. Association of cerebrospinal fluid Neurogranin with Alzheimer’s disease. Aging Clin Exp Res 2019; 31(2): 185-91.
[http://dx.doi.org/10.1007/s40520-018-0948-3] [PMID: 29667155]
[49]
Headley A, De Leon-Benedetti A, Dong C, et al. Neurogranin as a predictor of memory and executive function decline in MCI patients. Neurology 2018; 90(10): e887-95.
[http://dx.doi.org/10.1212/WNL.0000000000005057] [PMID: 29429972]
[50]
Sanfilippo C, Forlenza O, Zetterberg H, Blennow K. Increased neurogranin concentrations in cerebrospinal fluid of Alzheimer’s disease and in mild cognitive impairment due to AD. J Neural Transm (Vienna) 2016; 123(12): 1443-7.
[http://dx.doi.org/10.1007/s00702-016-1597-3] [PMID: 27531278]
[51]
Lista S, Toschi N, Baldacci F, et al. Cerebrospinal fluid neurogranin as a biomarker of neurodegenerative diseases: a cross-sectional study. J Alzheimers Dis 2017; 59(4): 1327-34.
[http://dx.doi.org/10.3233/JAD-170368] [PMID: 28731449]
[52]
Antonell A, Tort-Merino A, Ríos J, et al. Synaptic, axonal damage and inflammatory cerebrospinal fluid biomarkers in neurodegenerative dementias. Alzheimers Dement 2020; 16(2): 262-72.
[http://dx.doi.org/10.1016/j.jalz.2019.09.001] [PMID: 31668967]
[53]
Merluzzi AP, Carlsson CM, Johnson SC, et al. Neurodegeneration, synaptic dysfunction, and gliosis are phenotypic of Alzheimer dementia. Neurology 2018; 91(5): e436-43.
[http://dx.doi.org/10.1212/WNL.0000000000005901] [PMID: 29959263]
[54]
Sutphen CL, McCue L, Herries EM, et al. Longitudinal decreases in multiple cerebrospinal fluid biomarkers of neuronal injury in symptomatic late onset Alzheimer’s disease. Alzheimers Dement 2018; 14(7): 869-79.
[http://dx.doi.org/10.1016/j.jalz.2018.01.012] [PMID: 29580670]
[55]
Blennow K, Diaz-Lucena D, Zetterberg H, et al. CSF neurogranin as a neuronal damage marker in CJD: a comparative study with AD. J Neurol Neurosurg Psychiatry 2019; 90(8): 846-53.
[http://dx.doi.org/10.1136/jnnp-2018-320155] [PMID: 31097472]
[56]
Vogt NM, Romano KA, Darst BF, et al. The gut microbiota-derived metabolite trimethylamine N-oxide is elevated in Alzheimer’s disease. Alzheimers Res Ther 2018; 10(1): 124.
[http://dx.doi.org/10.1186/s13195-018-0451-2] [PMID: 30579367]
[57]
Falgàs N, Ruiz-Peris M, Pérez-Millan A, et al. Contribution of CSF biomarkers to early-onset Alzheimer’s disease and frontotemporal dementia neuroimaging signatures. Hum Brain Mapp 2020; 41(8): 2004-13.
[http://dx.doi.org/10.1002/hbm.24925] [PMID: 31944489]
[58]
Galasko D, Xiao M, Xu D, et al. Synaptic biomarkers in CSF aid in diagnosis, correlate with cognition and predict progression in MCI and Alzheimer’s disease. Alzheimers Dement (N Y) 2019; 5: 871-82.
[http://dx.doi.org/10.1016/j.trci.2019.11.002] [PMID: 31853477]
[59]
Kvartsberg H, Portelius E, Andreasson U, et al. Characterization of the postsynaptic protein neurogranin in paired cerebrospinal fluid and plasma samples from Alzheimer’s disease patients and healthy controls. Alzheimers Res Ther 2015; 7(1): 40.
[http://dx.doi.org/10.1186/s13195-015-0124-3] [PMID: 26136856]
[60]
Wang J, Zhang X, Zhu B, Fu P. Association of clusterin levels in cerebrospinal fluid with synaptic degeneration across the Alzheimer’s disease continuum. Neuropsychiatr Dis Treat 2020; 16: 183-90.
[http://dx.doi.org/10.2147/NDT.S224877] [PMID: 32021212]
[61]
Bos I, Vos S, Verhey F, et al. Cerebrospinal fluid biomarkers of neurodegeneration, synaptic integrity, and astroglial activation across the clinical Alzheimer’s disease spectrum. Alzheimers Dement 2019; 15(5): 644-54.
[http://dx.doi.org/10.1016/j.jalz.2019.01.004] [PMID: 30853464]
[62]
De Vos A, Jacobs D, Struyfs H, et al. C-terminal neurogranin is increased in cerebrospinal fluid but unchanged in plasma in Alzheimer’s disease. Alzheimers Dement 2015; 11(12): 1461-9.
[http://dx.doi.org/10.1016/j.jalz.2015.05.012] [PMID: 26092348]
[63]
Ye X, Zhou W, Zhang J. Association of CSF CD40 levels and synaptic degeneration across the Alzheimer’s disease spectrum. Neurosci Lett 2019; 694: 41-5.
[http://dx.doi.org/10.1016/j.neulet.2018.11.019] [PMID: 30447377]
[64]
Weydt P, Oeckl P, Huss A, et al. Neurofilament levels as biomarkers in asymptomatic and symptomatic familial amyotrophic lateral sclerosis. Ann Neurol 2016; 79(1): 152-8.
[http://dx.doi.org/10.1002/ana.24552] [PMID: 26528863]
[65]
Schultz NA, Johansen JS. YKL-40-a protein in the field of translational medicine: A role as a biomarker in cancer patients? Cancers (Basel) 2010; 2(3): 1453-91.
[http://dx.doi.org/10.3390/cancers2031453] [PMID: 24281168]
[66]
Shao R. YKL-40 acts as an angiogenic factor to promote tumor angiogenesis. Front Physiol 2013; 4: 122.
[http://dx.doi.org/10.3389/fphys.2013.00122] [PMID: 23755018]
[67]
Qin G, Li X, Chen Z, et al. Prognostic value of YKL-40 in patients with Glioblastoma: a systematic review and meta-analysis. Mol Neurobiol 2017; 54(5): 3264-70.
[http://dx.doi.org/10.1007/s12035-016-9878-2] [PMID: 27090900]
[68]
Baldacci F, Lista S, Cavedo E, Bonuccelli U, Hampel H. Diagnostic function of the neuroinflammatory biomarker YKL-40 in Alzheimer’s disease and other neurodegenerative diseases. Expert Rev Proteomics 2017; 14(4): 285-99.
[http://dx.doi.org/10.1080/14789450.2017.1304217] [PMID: 28281838]
[69]
Abu-Rumeileh S, Steinacker P, Polischi B, et al. CSF biomarkers of neuroinflammation in distinct forms and subtypes of neurodegenerative dementia. Alzheimers Res Ther 2019; 12(1): 2.
[http://dx.doi.org/10.1186/s13195-019-0562-4] [PMID: 31892365]
[70]
Gispert JD, Monté GC, Falcon C, et al. CSF YKL-40 and pTau181 are related to different cerebral morphometric patterns in early AD. Neurobiol Aging 2016; 38: 47-55.
[http://dx.doi.org/10.1016/j.neurobiolaging.2015.10.022] [PMID: 26827642]
[71]
Antonell A, Mansilla A, Rami L, et al. Cerebrospinal fluid level of YKL-40 protein in preclinical and prodromal Alzheimer’s disease. J Alzheimers Dis 2014; 42(3): 901-8.
[http://dx.doi.org/10.3233/JAD-140624] [PMID: 25024322]
[72]
Craig-Schapiro R, Perrin RJ, Roe CM, et al. YKL-40: a novel prognostic fluid biomarker for preclinical Alzheimer’s disease. Biol Psychiatry 2010; 68(10): 903-12.
[http://dx.doi.org/10.1016/j.biopsych.2010.08.025] [PMID: 21035623]
[73]
Olsson B, Hertze J, Lautner R, et al. Microglial markers are elevated in the prodromal phase of Alzheimer’s disease and vascular dementia. J Alzheimers Dis 2013; 33(1): 45-53.
[http://dx.doi.org/10.3233/JAD-2012-120787] [PMID: 22890100]
[74]
Rosén C, Andersson CH, Andreasson U, et al. Increased levels of chitotriosidase and YKL-40 in cerebrospinal fluid from patients with Alzheimer’s disease. Dement Geriatr Cogn Disord Extra 2014; 4(2): 297-304.
[http://dx.doi.org/10.1159/000362164] [PMID: 25254036]
[75]
Alcolea D, Martínez-Lage P, Sánchez-Juan P, et al. Amyloid precursor protein metabolism and inflammation markers in preclinical Alzheimer disease. Neurology 2015; 85(7): 626-33.
[http://dx.doi.org/10.1212/WNL.0000000000001859] [PMID: 26180139]
[76]
Mattsson N, Tabatabaei S, Johansson P, et al. Cerebrospinal fluid microglial markers in Alzheimer’s disease: elevated chitotriosidase activity but lack of diagnostic utility. Neuromolecular Med 2011; 13(2): 151-9.
[http://dx.doi.org/10.1007/s12017-011-8147-9] [PMID: 21567187]
[77]
Alcolea D, Carmona-Iragui M, Suárez-Calvet M, et al. Relationship between β-Secretase, inflammation and core cerebrospinal fluid biomarkers for Alzheimer’s disease. J Alzheimers Dis 2014; 42(1): 157-67.
[http://dx.doi.org/10.3233/JAD-140240] [PMID: 24820015]
[78]
Olsson B, Lautner R, Andreasson U, et al. CSF and blood biomarkers for the diagnosis of Alzheimer’s disease: a systematic review and meta-analysis. Lancet Neurol 2016; 15(7): 673-84.
[http://dx.doi.org/10.1016/S1474-4422(16)00070-3] [PMID: 27068280]
[79]
Dulewicz M, Kulczyńska-Przybik A, Mroczko B. Neurogranin and VILIP-1 as molecular indicators of neurodegeneration in Alzheimer’s disease: a systematic review and meta-analysis. Int J Mol Sci 2020; 21(21): 8335.
[http://dx.doi.org/10.3390/ijms21218335] [PMID: 33172069]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy