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Neurological Research
A Journal of Progress in Neurosurgery, Neurology and Neurosciences
Volume 35, 2013 - Issue 9
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Original Article

Combination of high-sensitivity C-reactive protein and homocysteine predicts the short-term outcomes of Chinese patients with acute ischemic stroke

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Pages 912-921 | Received 28 Feb 2013, Accepted 28 Apr 2013, Published online: 18 Nov 2013

References

  • Bonita R, Mendis S, Truelsen T, Bogousslavsky J, Toole J, Yatsu F. The global stroke initiative. Lancet Neurol. 2004;3:391–3.
  • Li Z, Sun L, Zhang H, Liao Y, Wang D, Zhao B, et al.. Elevated plasma homocysteine was associated with hemorrhagic and ischemic stroke, but methylenetetrahydrofolate reductase gene C677T polymorphism was a risk factor for thrombotic stroke: a multicenter case-control study in china. Stroke. 2003;34:2085–90.
  • Slot KB, Berge E, Dorman P, Lewis S, Dennis M, Sandercock P, et al.. Impact of functional status at six months on long term survival in patients with ischaemic stroke: prospective cohort studies. BMJ. 2008;336:376–9.
  • Shantikumar S, Grant PJ, Catto AJ, Bamford JM, Carter AM. Elevated C-reactive protein and long-term mortality after ischaemic stroke: relationship with markers of endothelial cell and platelet activation. Stroke. 2009;40:977–9.
  • Muir KW, Weir CJ, Alwan W, Squire IB, Lees KR. C-reactive protein and outcome after ischemic stroke. Stroke. 1999;30:981–5.
  • Di Napoli M, Papa F, Bocola V. C-reactive protein in ischemic stroke: an independent prognostic factor. Stroke. 2001;32:917–24.
  • Di Napoli M, Papa F, Bocola V. Prognostic influence of increased C-reactive protein and fibrinogen levels in ischemic stroke. Stroke. 2001;32:133–8.
  • Arenillas JF, Alvarez-Sabin J, Molina CA, Chacón P, Montaner J, Rovira A, et al.. C-reactive protein predicts further ischemic events in first-ever transient ischemic attack or stroke patients with intracranial large-artery occlusive disease. Stroke. 2003;34:2463–8.
  • Di Napoli M, Godoy DA, Campi V, del Valle M, Piñero G, Mirofsky M, et al.. C-reactive protein level measurement improves mortality prediction when added to the spontaneous intracerebral hemorrhage score. Stroke. 2011;42:1230–6.
  • Rost NS, Wolf PA, Kase CS, Kelly-Hayes M, Silbershatz H, Massaro JM, et al.. Plasma concentration of C-reactive protein and risk of ischemic stroke and transient ischemic attack: the Framingham study. Stroke. 2001;32:2575–9.
  • Huang Y, Jing J, Zhao XQ, Wang CX, Wang YL, Liu GF, et al.. High-sensitivity C-reactive protein is a strong risk factor for death after acute ischemic stroke among Chinese. CNS Neurosci Ther. 2012;18:261–6.
  • Newton LA, Sandhu K, Livingstone C, Leslie R, Davis J. Clinical diagnostics for homocysteine: a rogue amino acid? Expert Rev Mol Diagn. 2010;10:489–500.
  • Tu MC, Huang CW, Chen NC, Chang WN, Lui CC, Chen CF, et al.. Hyperhomocysteinemia in Alzheimer dementia patients and cognitive decline after 6 months follow-up period. Acta Neurol Taiwan. 2010;19:168–77.
  • Chen CS, Chou MC, Yeh YC, Yang YH, Lai CL, Yen CF, et al.. Plasma homocysteine levels and major depressive disorders in Alzheimer disease. Am J Geriatr Psychiatry. 2010;18:1045–8.
  • Seshadri S, Beiser A, Selhub J, Jacques PF, Rosenberg IH, D'Agostino RB, et al.. Plasma homocysteine as a risk factor for dementia and Alzheimer’s disease. N Engl J Med. 2002;346:476–83.
  • Herrmann W, Obeid R. Homocysteine: a biomarker in neurodegenerative diseases. Clin Chem Lab Med. 2011;49:435–41.
  • Humphrey LL, Fu R, Roger K, Freeman M, Helfand M. Homocysteine level and coronary heart disease incidence: a systematic review and meta-analysis. Mayo Clin Proc. 2008;83:1203–12.
  • Remacha AF, Souto JC, Piñana JL, Sardà MP, Queraltó JM, Martí-Fabregas J, et al.. Vitamin B12 deficiency, hyperhomocysteinemia and thrombosis: a case and control study. Int J Hematol. 2011;93:458–64.
  • Gibelin P, Serre S, Candito M, Houcher B, Berthier F, Baudouy M. Prognostic value of homocysteinemia in patients with congestive heart failure. Clin Chem Lab Med. 2006;44:813–6.
  • Oudi ME, Aouni Z, Mazigh C, Khochkar R, Gazoueni E, Haouela H, et al.. Homocysteine and markers of inflammation in acute coronary syndrome. Exp Clin Cardiol. 2010;15:e25–8.
  • Vibo R, Kõrv J, Roose M, Kampus P, Muda P, Zilmer K, et al.. Acute phase proteins and oxidised low-density lipoprotein in association with ischemic stroke subtype, severity and outcome. Free Radic Res. 2007;41:282–7.
  • Durga J, van Tits LJ, Schouten EG, Kok FJ, Verhoef P. Effect of lowering of homocysteine levels on inflammatory markers: a randomized controlled trial. Arch Intern Med. 2005;165:1388–94.
  • Selhub J, Jacques PF, Bostom AG, D'Agostino RB, Wilson PW, Belanger AJ, et al.. Association between plasma homocysteine concentrations and extracranial carotid-artery stenosis. N Engl J Med. 1995;332:286–91.
  • Bostom AG, Rosenberg IH, Silbershatz H, Jacques PF, Selhub J, D'Agostino RB, et al.. Nonfasting plasma total homocysteine levels and stroke incidence in elderly persons: the Framingham Study. Ann Intern Med. 1999;131:352–5.
  • Tanne D, Haim M, Goldbourt U, Boyko V, Doolman R, Adler Y, et al.. Prospective study of serum homocysteine and risk of ischemic stroke among patients with preexisting coronary heart disease. Stroke. 2003;34:632–6.
  • Yoo J-H, Chung C-S, Kang S-S. Relation of plasma homocyst(e)ine to cerebral infarction and cerebral atherosclerosis. Stroke. 1998;29:2478–83.
  • Kristensen B, Malm J, Nilsson T, Hultdin J, Carlberg B, Dahlén G, et al.. Hyperhomocysteinemia and hypofibrinolysis in young adults with ischemic stroke. Stroke. 1999;30:974–80.
  • Eikelboom J, Hankey G, Anand S, Lofthouse E, Staples N, Baker RI. Association between high homocyst(e)ine and ischemic stroke due to large-and small-artery disease but not other etiologic subtypes of ischemic stroke. Stroke. 2000;31:1069–75.
  • Meiklejohn D, Vickers M, Dijkhuisen R, Greaves M. Plasma homocysteine concentrations in the acute and convalescent periods of atherothrombotic stroke. Stroke. 2001;32:57–62.
  • Karttunen V, Alfthan G, Hiltunen L, Rasi V, Kervinen K, Kesäniemi YA, et al.. Risk factors for cryptogenic ischaemic stroke. Eur J Neurol. 2002;9:625–32.
  • Song IU, Kim YD, Kim JS, Lee KS, Chung SW. Can high-sensitivity C-reactive protein and plasma homocysteine levels independently predict the prognosis of patients with functional disability after first-ever ischemic stroke? Eur Neurol. 2010;64:304–10.
  • Ma Y, Zhao X, Zhang W, Liu L, Wang Y, Fang R, et al.. Homocysteine and ischemic stroke subtype: a relationship study in Chinese patients. Neurol Res. 2010;32:636–41.
  • Biswas A, Ranjan R, Meena A, Akhter MS, Yadav BK, Munisamy M, et al.. Homocystine levels, polymorphisms and the risk of ischemic stroke in young Asian Indians. J Stroke Cerebrovasc Dis. 2009;18:103–10.
  • Song IU, Kim JS, Ryu SY, Lee SB, Lee SJ, Jeong DS, et al.. Are plasma homocysteine levels related to neurological severity and functional outcome after ischemic stroke in the Korean population? J Neurol Sci. 2009;278:60–3.
  • Okubadejo NU, Oladipo OO, Adeyomoye AA, Awosanya GO, Danesi MA. Exploratory study of plasma total homocysteine and its relationship to short-term outcome in acute ischaemic stroke in Nigerians. BMC Neurol. 2008;8:26.
  • Yoldas T, Gonen M, Godekmerdan A, Ilhan F, Bayram E. The serum high-sensitive C reactive protein and homocysteine levels to evaluate the prognosis of acute ischemic stroke. Mediators Inflamm. 2007;2007:15929.
  • Haapaniemi E, Helenius J, Soinne L, Syrjälä M, Kaste M, Tatlisumak T. Serial measurements of plasma homocysteine levels in early and late phases of ischemic stroke. Eur J Neurol. 2007;14:12–7.
  • Mizrahi EH, Fleissig Y, Arad M, Adunsky A. Plasma homocysteine level and functional outcome of patients with ischemic stroke. Arch Phys Med Rehabil. 2005;86:60–3.
  • Yan J, Liao JK, Wang D. Elevated homocysteine and C-reactive protein levels independently predict worsening prognosis after stroke in Chinese patients. J Huazhong Univ Sci Technolog Med Sci. 2010;30:643–7.
  • Hatano S. Experience from a multicentre stroke register: a preliminary report. Bull World Health Organ. 1976;54:541–53.
  • Brott T, Marler JR, Olinger CP, Adams HP, Tomsick T, Barsan WG, et al.. Measurements of acute cerebral infarction: lesion size by computed tomography. Stroke. 1989;20:871–5.
  • Adams HP, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, et al.. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke. 1993;24:35–41.
  • Bonita RBR. Modification of Rankin Scale: recovery of motor function after stroke. Stroke. 1988;19:1497–500.
  • Broderick JP, Brott TG, Duldner JE, Tomsick T, Huster G. Volume of intracerebral hemorrhage. A powerful and easy-to-use predictor of 30-day mortality. Stroke. 1993;24:987–93.
  • Szabo K, Kern R, Gass A, Hirsch J, Hennerici M. Acute stroke patterns in patients with internal carotid artery disease: a diffusion-weighted magnetic resonance imaging study. Stroke. 2001;32:1323–9.
  • Omrani HQ, Shandiz EE, Qabai M, Chaman R, Fard HA, Qaffarpoor M. Hyperhomocysteinemia, folateo and B12 vitamin in Iranian patients with acute ischemic stroke. ARYA Atheroscler. 2011;7:97–101.
  • Homocysteine Studies Collaboration. Homocysteine and risk of ischemic heart disease and stroke: a meta-analysis. JAMA. 2002;288:2015–22.
  • Howard V, Sides E, Newman G, Cohen SN, Howard G, Malinow MR, et al.. Changes in plasma homocyst(e)ine in the acute phase after stroke. Stroke. 2002;33:473–8.
  • Ubbink J, Vermaak W, Delport R, van der Merwe A, Becker PJ, Potgieter H. Effective homocysteine metabolism may protect South African blacks against coronary heart disease. Am J Clin Nutr. 1995;62:802–8.
  • Welsh P, Barber M, Langhorne P, Rumley A, Lowe GD, Stott DJ.. Associations of inflammatory biomarkers with poor outcome inacute ischaemic stroke. Cerebrovasc Dis. 2009;27:247–53.
  • Song IU, Kim JS, Kim YI, Lee KS, Jeong DS, Chung SW, et al.. Relationship between high-sensitivity C-reactive protein and clinical functional outcome after acute ischemic stroke in a Korean population. Cerebrovasc Dis. 2009;28:545–50.
  • Endres M, Ahmadi M, Kruman I, Biniszkiewicz D, Meisel A, Gertz K. Folate deficiency increases postischemic brain injury. Stroke. 2005;36:321–5.
  • Hao L, Ma J, Zhu J, Stampfer MJ, Tian Y, Willett WC, et al.. High prevalence of hyperhomocysteinemia in Chinese adults is associated with low folate, vitamin B-12, and vitamin B-6 status. J Nutr. 2007;137:407–13.
  • Sacco RL, Boden-Albala B, Chen X, Lin IF, Kargman DE, Paik MC. Relationship of 6-month functional outcome and stroke severity: implications for acute stroke trials from the Northern Manhattan Stroke Study [abstract]. Neurology. 1998;50:A327.
  • Adams HP, Davis PH, Leira EC, Chang KC, Bendixen BH, Clarke WR, et al.. Baseline NIH Stroke Scale score strongly predicts outcome after stroke: a report of the Trial of Org 10172 in Acute Stroke Treatment (TOAST). Neurology. 1999;53:126–31.
  • Elkind MS, Tai W, Coates K, Paik MC, Sacco RL. High-sensitivity C-reactive protein, lipoprotein-associated phospholipase A2, and outcome after ischemic stroke. Arch Intern Med. 2006;166:2073–80.
  • Cermak J, Key NS, Bach RR, Balla J, Jacob HS, Vercellotti GM. C-reactive protein induces human peripheral blood monocytes to synthesize tissue factor. Blood. 1993;82:513–20.
  • de Ruijter W, Westendorp RG, Assendelft WJ, den Elzen WP, de Craen AJ, le Cessie S, et al.. Use of Framingham risk score and new biomarkers to predict cardiovascular mortality in older people: population based observational cohort study. BMJ. 2009;338:A3083.
  • Pasterkamp G, Algra A, Grobbee DE, de Jaegere PP, Banga JD, van der Graaf Y. Homocysteine and the stage of atherosclerotic disease: a study in patients suffering from clinically silent and clinically manifest atherosclerotic disease. Eur J Clin Invest. 2002;32:309–15.
  • Pietro EL, Pier LC, Enrico S, Lorenzini S, Bisogno S, Galeazzi M, et al.. Hyperhomocysteinemia, inflammation and autoimmunity. Autoimmunity Rev. 2007;6:503–9.
  • Symons JD, Mullick AE, Ensunsa JL, Ma AA, Rutledge JC. Hyperhomocysteinemia evoked by folate depletion: effects on coronary and carotid arterial function. Arterioscler Thromb Vasc Biol. 2002;22:772–80.
  • Hofmann MA, Lalla E, Lu Y, Gleason MR, Wolf BM, Tanji N, et al.. Hyperhomocysteinemia enhances vascular inflammation and accelerates atherosclerosis in a murine model. J Clin Invest. 2001;107:675–83.
  • Manolescu BN, Oprea E, Farcasanu IC, Berteanu M, Cercasov C. Homocysteine and vitamin therapy in stroke prevention and treatment: a review. Acta Biochim Pol. 2010;57:467–77.
  • Undas A, Perla J, Lacinski M, Trzeciak W, Kaźmierski R, Jakubowski H. Auto antibodies against N-homocysteinylated proteins in humans: implications for atherosclerosis. Stroke. 2004;35:1299–304.
  • Kawasaki R, Xie J, Cheung N, Lamoureux E, Klein R, Klein BE, et al.. Retinal microvascular signs and risk of stroke: the multi-ethnic study of atherosclerosis (MESA). Stroke. 2012;43:3245–51.
  • Pavlovic AM, Pekmezovic T, Obrenovic R, Novakovic I, Tomic G, Mijajlovic M, et al.. Increased total homocysteine level is associated with clinical status and severity of white matter changes in symptomatic patients with subcortical small vessel disease. Clin Neurol Neurosurg. 2011;113:711–5.
  • Kloppenborg RP, Nederkoorn PJ, van der Graaf Y, Geerlings MI. Homocysteine and cerebral small vessel disease in patients with symptomatic atherosclerotic disease. The SMART-MR study. Atherosclerosis. 2011;216:461–6.
  • Cavalieri M, Schmidt R, Chen C, Mok V, de Freitas GR, Song S, et al.. B vitamins and magnetic resonance imaging-detected ischemic brain lesions in patients with recent transient ischemic attack or stroke: the VITAmins TO Prevent Stroke (VITATOPS) MRI-substudy. Stroke. 2012;43:3266–70.
  • Bonaa KH, Njolstad I, Ueland PM, Schirmer H, Tverdal A, Steigen T, et al.. Homocysteine lowering and cardiovascular events after acute myocardial infarction. N Engl J Med. 2006;354:1578–88.
  • Toole JF, Malinow MR, Chambless LE, Spence JD, Pettigrew LC, Howard VJ, et al.. Lowering homocysteine in patients with ischemic stroke to prevent recurrent stroke, myocardial infarction, and death: the Vitamin Intervention for Stroke Prevention (VISP) randomized controlled trial. JAMA. 2004;291:565–75.
  • Lonn E, Yusuf S, Arnold MJ, Sheridan P, Pogue J, Micks M, et al.. Homocysteine lowering with folic acid and B vitamins in vascular disease. N Engl J Med. 2006;354:1567–77.
  • Ebbing M, Bønaa KH, Arnesen E, Ueland PM, Nordrehaug JE, Rasmussen K, et al.. Combined analyses and extended follow-up of two randomized controlled homocysteine-lowering B-vitamin trials. J Intern Med. 2010;268:367–82.

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