Vol 30, No 3 (2024)
Research paper
Published online: 2024-10-18
Effect of carotid endarterectomy on the serum level of neurogranin
1
, 2, 2, 2, 3
, 2, 2, 2, 3
DOI: 10.5603/aa.101334
Acta Angiologica 2024;30(3):97-105.
Abstract
Introduction: Stroke remains the leading cause of disability and death worldwide. Carotid endarterectomy
(CEA) reduces the incidence of ischemic stroke or death in patients with symptomatic carotid artery stenosis
more effective than pharmacological therapy alone. Neurogranin is a potential marker of brain injury previously
investigated mainly in neurodegenerative diseases (Alzheimer disease), but also in ischemic stroke and
traumatic brain injury.
Material and methods: The aim of the research was to investigate the changes in serum level concentrations
of neurogranin in patients undergoing CEA. 22 patients with severe carotid artery stenosis underwent CEA.
Serum levels of Neurogranin were measured by an enzyme-linked immunosorbent assay (ELISA) test at 24 h
before CEA, 12 and 48 h after the surgery.
Results: Serum neurogranin levels show a tendency to decrease after an uncomplicated CEA, however the
difference is not statistically significant (p > 0.05).
Conclusions: Serum neurogranin level does not significantly change after the CEA, therefore it may not be
an useful marker of brain damage after the procedure. There is still need for further studies on bigger group of
patients and patients with neurological complications to confirm these findings.
Keywords: neurogranincarotid endarterectomybiomarkers
References
- Favate AS, Younger DS. Epidemiology of Ischemic Stroke. Neurol Clin. 2016; 34(4): 967–980.
- Yip HK, Sung PH, Wu CJ, et al. Carotid stenting and endarterectomy. Int J Cardiol. 2016; 214: 166–174.
- Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European Carotid Surgery Trial (ECST). Lancet. 1998; 351(9113): 1379–1387.
- Mayberg MR, Wilson SE, Yatsu F, et al. Carotid endarterectomy and prevention of cerebral ischemia in symptomatic carotid stenosis. Veterans Affairs Cooperative Studies Program 309 Trialist Group. JAMA. 1991; 266(23): 3289–3294.
- Barnett HJ, Taylor DW, Eliasziw M, et al. Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 1998; 339(20): 1415–1425.
- Barnett HJM, Taylor DW, Haynes RB, et al. North American Symptomatic Carotid Endarterectomy Trial Collaborators. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med. 1991; 325(7): 445–453.
- Gupta N, Corriere MA, Dodson TF, et al. The incidence of microemboli to the brain is less with endarterectomy than with percutaneous revascularization with distal filters or flow reversal. J Vasc Surg. 2011; 53(2): 316–322.
- Backhaus R, Boy S, Fuchs K, et al. Hyperperfusion syndrome after MCA embolectomy - a rare complication? Am J Case Rep. 2013; 14: 513–517.
- Lieb M, Shah U, Hines GL. Cerebral hyperperfusion syndrome after carotid intervention: a review. Cardiol Rev. 2012; 20(2): 84–89.
- Capoccia L, Sbarigia E, Rizzo AR, et al. Contralateral occlusion increases the risk of neurological complications associated with carotid endarterectomy. Int J Vasc Med. 2015; 2015: 942146.
- Xiang Y, Xin J, Le W, et al. Neurogranin: A Potential Biomarker of Neurological and Mental Diseases. Front Aging Neurosci. 2020; 12: 584743.
- Represa A, Deloulme JC, Sensenbrenner M, et al. Neurogranin: immunocytochemical localization of a brain-specific protein kinase C substrate. J Neurosci. 1990; 10(12): 3782–3792.
- Zhong L, Cherry T, Bies CE, et al. Neurogranin enhances synaptic strength through its interaction with calmodulin. EMBO J. 2009; 28(19): 3027–3039.
- Zhong L, Gerges NZ. Neurogranin and synaptic plasticity balance. Commun Integr Biol. 2010; 3(4): 340–342.
- Yilmaz A, Fuchs D, Price RW, et al. Cerebrospinal Fluid Concentrations of the Synaptic Marker Neurogranin in Neuro-HIV and Other Neurological Disorders. Curr HIV/AIDS Rep. 2019; 16(1): 76–81.
- Pak JH, Huang FL, Li J, et al. Involvement of neurogranin in the modulation of calcium/calmodulin-dependent protein kinase II, synaptic plasticity, and spatial learning: a study with knockout mice. Proc Natl Acad Sci U S A. 2000; 97(21): 11232–11237.
- Díez-Guerra FJ. Neurogranin, a link between calcium/calmodulin and protein kinase C signaling in synaptic plasticity. IUBMB Life. 2010; 62(8): 597–606.
- Glynne R, Ghandour G, Rayner J, et al. B-lymphocyte quiescence, tolerance and activation as viewed by global gene expression profiling on microarrays. Immunol Rev. 2000; 176: 216–246.
- Gnatenko DV, Dunn JJ, McCorkle SR, et al. Transcript profiling of human platelets using microarray and serial analysis of gene expression. Blood. 2003; 101(6): 2285–2293.
- Casaletto KB, Elahi FM, Bettcher BM, et al. Neurogranin, a synaptic protein, is associated with memory independent of Alzheimer biomarkers. Neurology. 2017; 89(17): 1782–1788.
- DeKosky ST, Scheff SW. Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol. 1990; 27(5): 457–464.
- Terry RD, Masliah E, Salmon DP, et al. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol. 1991; 30(4): 572–580.
- Selkoe DJ. Alzheimer's disease is a synaptic failure. Science. 2002; 298(5594): 789–791.
- Fyfe I. Alzheimer disease: neurogranin in the CSF signals early Alzheimer disease and predicts disease progression. Nat Rev Neurol. 2015; 11(11): 609.
- 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.
- 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): 1275–1280.
- Portelius E, Zetterberg H, Skillbäck T, et al. Alzheimer’s Disease Neuroimaging Initiative. Cerebrospinal fluid neurogranin: relation to cognition and neurodegeneration in Alzheimer's disease. Brain. 2015; 138(Pt 11): 3373–3385.
- 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): 561–571.
- 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): 363–376.
- Wellington H, Paterson RW, Portelius E, et al. Increased CSF neurogranin concentration is specific to Alzheimer disease. Neurology. 2016; 86(9): 829–835.
- Selnes P, Stav AL, Johansen KK, et al. Impaired synaptic function is linked to cognition in Parkinson's disease. Ann Clin Transl Neurol. 2017; 4(10): 700–713.
- Hall S, Janelidze S, Zetterberg H, et al. Cerebrospinal fluid levels of neurogranin in Parkinsonian disorders. Mov Disord. 2020; 35(3): 513–518.
- Bereczki E, Bogstedt A, Höglund K, et al. Synaptic proteins in CSF relate to Parkinson's disease stage markers. NPJ Parkinsons Dis. 2017; 3: 7.
- 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): 846–853.
- Yeşilyurt Ö, Cömertpay E, Vural S, et al. The diagnostic value of neurogranin in patients with carbon monoxide poisoning: Can it show early neurological damage? Am J Emerg Med. 2021; 50: 191–195.
- Kalkan A, Demirel A, Atiş ŞE, et al. A new biomarker in the differential diagnosis of epileptic seizure: Neurogranin. Am J Emerg Med. 2022; 54: 147–150.
- Yang J, Korley FK, Dai M, et al. Serum neurogranin measurement as a biomarker of acute traumatic brain injury. Clin Biochem. 2015; 48(13-14): 843–848.
- Çevik S, Özgenç MM, Güneyk A, et al. NRGN, S100B and GFAP levels are significantly increased in patients with structural lesions resulting from mild traumatic brain injuries. Clin Neurol Neurosurg. 2019; 183: 105380.
- Peacock WF, Van Meter TE, Mirshahi N, et al. Derivation of a Three Biomarker Panel to Improve Diagnosis in Patients with Mild Traumatic Brain Injury. Front Neurol. 2017; 8: 641.
- Kuşdoğan M, Vural S, Albayrak L, et al. The diagnostic and prognostic value of serum neurogranin in acute ischemic stroke. J Stroke Cerebrovasc Dis. 2023; 32(2): 106889.
- De Vos A, Bjerke M, Brouns R, et al. Neurogranin and tau in cerebrospinal fluid and plasma of patients with acute ischemic stroke. BMC Neurol. 2017; 17(1): 170.
- Thorsell A, Bjerke M, Gobom J, et al. Neurogranin in cerebrospinal fluid as a marker of synaptic degeneration in Alzheimer's disease. Brain Res. 2010; 1362: 13–22.
- 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): 1180–1190.
- 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): 1275–1280.
- 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): 1461–1469.
- 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.
- Rajeev V, Fann DY, Dinh QN, et al. Pathophysiology of blood brain barrier dysfunction during chronic cerebral hypoperfusion in vascular cognitive impairment. Theranostics. 2022; 12(4): 1639–1658.
- Rasmussen LS, Christiansen M, Johnsen J, et al. Subtle brain damage cannot be detected by measuring neuron-specific enolase and S-100beta protein after carotid endarterectomy. J Cardiothorac Vasc Anesth. 2000; 14(2): 166–170.
- Connolly ES, Winfree CJ, Rampersad A, et al. Serum S100B protein levels are correlated with subclinical neurocognitive declines after carotid endarterectomy. Neurosurgery. 2001; 49(5): 1076–82; discussion 1082.
- Brightwell RE, Sherwood RA, Athanasiou T, et al. The neurological morbidity of carotid revascularisation: using markers of cellular brain injury to compare CEA and CAS. Eur J Vasc Endovasc Surg. 2007; 34(5): 552–560.
- Mussack T, Hauser C, Klauss V, et al. Serum S-100B protein levels during and after successful carotid artery stenting or carotid endarterectomy. J Endovasc Ther. 2006; 13(1): 39–46.
- Terlecki P, Pawlik P, Iwaniuk A, et al. Carotid surgery affects plasma kynurenic acid concentration: a pilot study. Med Sci Monit. 2014; 20: 303–310.
- Iłżecki M, Iłżecka J, Przywara S, et al. Effect of carotid endarterectomy on brain damage markers. Acta Neurol Scand. 2017; 135(3): 352–359.
- Ilzecki M, Przywara S, Ilzecka J, et al. Serum glial fibrillary acidic protein as a marker of brain damage in patients after carotid endarterectomy. Acta Angiologica. 2016; 22(1): 1–4.
- Ilzecki M, Ilzecka J, Przywara S, et al. Serum Carnosine Dipeptidase 1 and Ubiquitin C - Terminal Hydrolase L1 as Markers of Brain Damage in Patients After Carotid Endarterectomy. THE ULUTAS MEDICAL JOURNAL. 2016; 2(3): 132.
- Ilzecki M, Przywara S, Ilzecka J, et al. Serum microtubule associated protein tau and myelin basic protein as the potential markers of brain ischaemia-reperfusion injury in patients undergoing carotid endarterectomy. Acta Angiologica. 2016; 22(2): 37–43.
- Iłżecki M, Iłżecka J, Przywara S, et al. Serum Neuron-Specific Enolase as a Marker of Brain Ischemia-Reperfusion Injury in Patients Undergoing Carotid Endarterectomy. Acta Clin Croat. 2016; 55(4): 579–584.