Electrochemical impedimetric detection of stroke biomarker NT-proBNP using disposable screen-printed gold electrodes

Open access

Abstract

Stroke is the second top leading cause of death globally. It is caused by an abrupt interruption of blood flow to the brain. In that course, brain natriuretic peptide (BNP) and its derivative N-terminal pro b-type natriuretic peptide (NT-proBNP), neurohormones produced mainly by the heart ventricles in response to excessive stretching of cardiomyocytes (heart muscle cells), are proven to be good biomarkers for heart failure diagnosis. Moreover, there is growing clinical interest of the use of NT-proBNP for stroke diagnosis and prognosis because it is significantly associated with cardioembolic stroke and secondary stroke reoccurrence, with sensitivity >90% and specificity >80%. However, in diagnostic settings, there is still a need to address the encountered analytical problems, particularly assay specificity and set up. In this study, a novel approach for NT-proBNP detection is demonstrated using an electrochemical immunoassay method. A label-free impedimetry immunosensor for stroke biomarker was developed using modified disposable screen-printed gold electrodes (SPGE) hosting specific anti-NT-proBNP capture antibody. The performance of our immunosensor was studied in the presence of NT-proBNP in both buffered and mock (porcine) plasma samples. A linear relation between the relative total resistance (ΔRtot) responses and the NT-proBNP concentrations in buffer was observed in a range from 0.1 to 5 ng mL-1 with a correlation coefficient (R2) of 0.94656. Overall, the biosensor has demonstrated the capability to quantitate NT-proBNP and differentiate such concentrations in a low concentration range, especially among 0, 0.1, 0.5, 1, and 3 ng mL-1 in plasma samples within 25 min. This range is valuable not only for classifying cardioembolic stroke (higher or equal to 0.5 ng mL-1), but also predicting the risk of secondary stroke reoccurrence (higher than 0.255 ng mL-1). Our biosensor has the potential to be used as an easy-to-use point-of-care test that is both accurate and affordable.

1. Strong K, Mathers C, Bonita R. Preventing stroke: saving lives around the world. The Lancet Neurology. 2007 Feb;6(2):182-7. PubMed PMID: 17239805. Epub 2007/01/24. eng.

2. Audebert HJ, Saver JL, Starkman S, Lees KR, Endres M. Prehospital stroke care: new prospects for treatment and clinical research. Neurology. 2013 Jul 30;81(5):501-8. PubMed PMID: 23897876. Pubmed Central PMCID: Pmc3776535. Epub 2013/07/31. eng.

3. Lees KR, Bluhmki E, von Kummer R, Brott TG, Toni D, Grotta JC, et al. Time to treatment with intravenous alteplase and outcome in stroke: an updated pooled analysis of ECASS, ATLANTIS, NINDS, and EPITHET trials. Lancet (London, England). 2010 May 15;375(9727):1695-703. PubMed PMID: 20472172. Epub2010/05/18. eng.

4. Leys D, Ringelstein EB, Kaste M, Hacke W. Facilities available in European hospitals treating stroke patients. Stroke; a journal of cerebral circulation. 2007 Nov;38(11):2985-91. PubMed PMID: 17901388. Epub 2007/09/29. eng.

5. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. The New England journal of medicine. 1995 Dec 14;333(24):1581-7. PubMed PMID: 7477192. Epub 1995/12/14.eng.

6. Hacke W, Kaste M, Bluhmki E, Brozman M, Davalos A, Guidetti D, et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. The New England journal of medicine. 2008 Sep 25;359(13):1317-29. PubMed PMID: 18815396. Epub 2008/09/26.eng.

7. Sandercock P, Wardlaw JM, Lindley RI, Dennis M, Cohen G, Murray G, et al. The benefits and harms of intravenous thrombolysis with recombinant tissue plasminogen activator within 6 h of acute ischaemic stroke (the third international stroke trial [IST-3]): a randomised controlled trial. Lancet (London, England). 2012 Jun 23;379(9834):2352-63. PubMed PMID: 22632908. Pubmed Central PMCID: Pmc3386495. Epub 2012/05/29. eng.

8. Adams HP, del Zoppo G, Alberts MJ, Bhatt DL, Brass L, Furlan A, et al. Guidelines for the Early Management of Adults With Ischemic Stroke. Circulation. 2007;115(20):e478.

9. Hemmen TM, Meyer BC, McClean TL, Lyden PD. Identification of Nonischemic Stroke Mimics Among 411 Code Strokes at the University of California, San Diego, Stroke Center. Journal of Stroke and Cerebrovascular Diseases.17(1):23-5.

10. Albers GW, Amarenco P, Easton JD, Sacco RL, Teal P. Antithrombotic and Thrombolytic Therapy for Ischemic Stroke: The Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy. Chest. 2004 9//;126(3, Supplement):483S-512S.

11. Thom T, Haase N, Rosamond W, Howard VJ, Rumsfeld J, Manolio T, et al. Heart Disease and Stroke Statistics-2006 Update. Circulation. 2006;113(6):e85.

12. Cummins BM, Ligler FS, Walker GM. Point-of-care diagnostics for niche applications. Biotechnology advances. 2016 May- Jun;34(3):161-76. PubMed PMID: 26837054. Pubmed Central PMCID: Pmc4833668. Epub 2016/02/03. Eng.

13. Llombart V, Antolin-Fontes A, Bustamante A, Giralt D, Rost NS, Furie K, et al. B-Type Natriuretic Peptides Help in Cardioembolic Stroke Diagnosis. Stroke; a journal of cerebral circulation. 2015;46(5):1187.

14. Sudoh T, Kangawa K, Minamino N, Matsuo H. A new natriuretic eptide in porcine brain. Nature. 1988 Mar 03;332(6159):78-81. PubMed PMID: 2964562. Epub 1988/03/03. eng.

15. Ziskoven D FW, Holthausen U, Menz G, Addicks K, Rippegater G. In Kaufmann W, Wambach G. . Calcium Calmodulin antagonists Influences the release of Cardiodilatin/ANP from Atrial Cardiocytes. Handbook Endocrinology of the Heart 1989 (Berlin: Verlag: Springer. pp. 233-4. ISBN 978-3-540-51409-1).

16. Hunt PJ, Yandle TG, Nicholls MG, Richards AM, Espiner EA. The amino- terminal portion of pro-brain natriuretic peptide (Pro-BNP) circulates in human plasma. Biochem Biophys Res Commun. 1995 Sep 25;214(3):1175-83. PubMed PMID: 7575527.

17. Atisha D, Bhalla MA, Morrison LK, Felicio L, Clopton P, Gardetto N, et al. A prospective study in search of an optimal B-natriuretic peptide level to screen patients for cardiac dysfunction. Am Heart J. 2004 Sep;148(3):518-23. PubMed PMID: 15389242. Epub2004/09/25. eng.

18. Cowie MR, Jourdain P, Maisel A, Dahlstrom U, Follath F, Isnard R, et al. Clinical applications of B-type natriuretic peptide (BNP) testing. Eur Heart J. 2003 Oct;24(19):1710-8. PubMed PMID: 14522565.

19. Kawase S, Kowa H, Suto Y, Fukuda H, Kusumi M, Nakayasu H, et al. Plasma Brain Natriuretic Peptide is a Marker of Prognostic Functional Outcome in Non-Cardioembolic Infarction. Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association. 2015 Oct;24(10):2285-90. PubMed PMID: 26232887. Epub 2015/08/04. eng.

20. Llombart V, Antolin-Fontes A, Bustamante A, Giralt D, Rost NS, Furie K, et al. B-type natriuretic peptides help in cardioembolic stroke diagnosis: pooled data meta-analysis. Stroke; a journal of cerebral circulation. 2015 May;46(5):1187-95. PubMed PMID: 25765726. Epub 2015/03/15. eng.

21. Wu Z, Zhao M, He M, Zeng H, Tan F, Li K, et al. Validation of the use of B-type natriuretic peptide point-of-care test platform in preliminary recognition of cardioembolic stroke patients in the ED. Am J Emerg Med. 2015 Apr;33(4):521-6. PubMed PMID: 25669874. Epub 2015/02/12. eng.

22. Chaudhuri JR, Sharma VK, Mridula KR, Balaraju B, Bandaru VC. Association of plasma brain natriuretic peptide levels in acute ischemic stroke subtypes and outcome. Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association. 2015 Feb;24(2):485-91. PubMed PMID: 25524015. Epub 2014/12/20. eng.

23. Cojocaru IM, Cojocaru M, Sapira V, Ionescu A, Barlan S, Tacu N. Could pro-BNP, uric acid, bilirubin, albumin and transferrin be used in making the distinction between stroke subtypes? Rom J Intern Med. 2013 Jul-Dec;51(3-4):188-95. PubMed PMID: 24620632. Epub 2014/03/14. eng.

24. Kara K, Gronewold J, Neumann T, Mahabadi AA, Weimar C, Lehmann N, et al. B-type natriuretic peptide predicts stroke of presumable cardioembolic origin in addition to coronary artery calcification. European journal of neurology. 2014 Jun;21(6):914-21. PubMed PMID: 24661834. Epub 2014/03/26. eng.

25. Maruyama K, Shiga T, Iijima M, Moriya S, Mizuno S, Toi S, et al. Brain natriuretic peptide in acute ischemic stroke. Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association. 2014 May-Jun;23(5):967-72. PubMed PMID: 24119617. Epub 2013/10/15. eng.

26. Sakai K, Shibazaki K, Kimura K, Aoki J, Kobayashi K, Fujii S, et al. Brain natriuretic peptide as a predictor of cardioembolism in acute ischemic stroke patients: brain natriuretic peptide stroke prospective study. European neurology. 2013;69(4):246-51. PubMed PMID: 23406829. Epub 2013/02/15. eng.

27. Balion C, McKelvie R, Don-Wauchope AC, Santaguida PL, Oremus M, Keshavarz H, et al. B-type natriuretic peptide-guided therapy: a systematic review. Heart Fail Rev. 2014 Aug;19(4):553-64. PubMed PMID: 25074674. Epub 2014/07/31. eng.

28. Clerico A, Franzini M, Masotti S, Prontera C, Passino C. State of the art of immunoassay methods for B-type natriuretic peptides: An update. Crit Rev Clin Lab Sci. 2015;52(2):56-69. PubMed PMID: 25547534. Epub 2014/12/31. eng.

29. Hajsadeghi S, Kashani Amin L, Bakhshandeh H, Rohani M, Azizian AR, Jafarian Kerman SR. The diagnostic value of N-terminal probrain natriuretic peptide in differentiating cardioembolic ischemic stroke. Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association. 2013 May;22(4):554-60. PubMed PMID: 23422348. Epub 2013/02/21. eng.

30. Qihong G, Zhixin W, Mingfeng H, Lianhong Y, Wenchong X. Experiences and the use of BNP POCT platform on suspected stroke patients by a Chinese emergency department. Ann Indian Acad Neurol. 2014 Apr;17(2):243-4. PubMed PMID: 25024591. Pubmed Central PMCID: PMC4090866. Epub 2014/07/16. eng.

31. Shibazaki K, Kimura K, Iguchi Y, Okada Y, Inoue T. Plasma brain natriuretic peptide can be a biological marker to distinguish cardioembolic stroke from other stroke types in acute ischemic stroke. Internal medicine (Tokyo, Japan). 2009;48(5):259-64. PubMed PMID: 19252345. Epub 2009/03/03. eng.

32. Yang HL, Lin YP, Long Y, Ma QL, Zhou C. Predicting cardioembolic stroke with the B-type natriuretic peptide test: a systematic review and meta-analysis. Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association. 2014 Aug;23(7):1882-9. PubMed PMID: 24795095. Epub 2014/05/06.eng.

33. Fonseca AC, Matias JS, Pinho e Melo T, Falcao F, Canhao P, Ferro JM. N-terminal probrain natriuretic peptide as a biomarker of cardioembolic stroke. Int J Stroke. 2011 Oct;6(5):398-403. PubMed PMID: 21645267. Epub 2011/06/08. eng.

34. Parker SA, Bowry R, Wu TC, Noser EA, Jackson K, Richardson L, et al. Establishing the first mobile stroke unit in the United States. Stroke; a journal of cerebral circulation. 2015 May;46(5):1384-91. PubMed PMID: 25782464. Epub 2015/03/19. eng.

35. Garcia-Berrocoso T, Giralt D, Bustamante A, Etgen T, Jensen JK, Sharma JC, et al. B-type natriuretic peptides and mortality after stroke: a systematic review and meta-analysis. Neurology. 2013 Dec 3;81(23):1976-85. PubMed PMID: 24186915. Pubmed Central PMCID: Pmc3854833. Epub 2013/11/05. Eng.

36. Jickling GC, Foerch C. Predicting stroke mortality: BNP could it be? Neurology. 2013 Dec 3;81(23):1970-1. PubMed PMID: 24186914. Epub 2013/11/05. Eng.

37. Shibazaki K, Kimura K, Sakai K, Fujii S, Aoki J, Saji N. Brain natriuretic peptide on admission as a biological marker of long-term mortality in ischemic stroke survivors. European neurology. 2013;70(3-4):218-24. PubMed PMID: 23988439. Epub 2013/08/31. Eng.

38. Chen X, Zhan X, Chen M, Lei H, Wang Y, Wei D, et al. The prognostic value of combined NT-pro-BNP levels and NIHSS scores in patients with acute ischemic stroke. Internal medicine (Tokyo, Japan). 2012;51(20):2887-92. PubMed PMID: 23064562. Epub 2012/10/16. Eng.

39. Montaner J, Garcia-Berrocoso T, Mendioroz M, Palacios M, Perea- Gainza M, Delgado P, et al. Brain natriuretic peptide is associated with worsening and mortality in acute stroke patients but adds no prognostic value to clinical predictors of outcome. Cerebrovascular diseases (Basel, Switzerland). 2012;34(3):240-5. PubMed PMID: 23018289. Epub 2012/09/29. Eng.

40. Makikallio AM, Makikallio TH, Korpelainen JT, Vuolteenaho O, Tapanainen JM, Ylitalo K, et al. Natriuretic Peptides and Mortality After Stroke. Stroke; a journal of cerebral circulation. 2005;36(5):1016-20.

41. Shibazaki K, Kimura K, Okada Y, Iguchi Y, Uemura J, Terasawa Y, et al. Plasma Brain Natriuretic Peptide as an Independent Predictor of In-Hospital Mortality after Acute Ischemic Stroke. Internal Medicine. 2009;48(18):1601-6.

42. Jensen JK, Atar D, Kristensen SR, Mickley H, Januzzi JL, Jr. Usefulness of Natriuretic Peptide Testing for Long-Term Risk Assessment Following Acute Ischemic Stroke. American Journal of Cardiology. 2009;104(2):287-91.

43. Shibazaki K, Kimura K, Aoki J, Sakai K, Saji N, Uemura J. Brain natriuretic peptide level on admission predicts recurrent stroke after discharge in stroke survivors with atrial fibrillation. Clinical neurology and neurosurgery. 2014 Dec;127:25-9. PubMed PMID: 25459239. Epub 2014/12/03. Eng.

44. Shibazaki K, Kimura K, Aoki J, Sakai K, Saji N, Uemura J. Plasma brain natriuretic Peptide as a predictive marker of early recurrent stroke in cardioembolic stroke patients. Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association. 2014 Nov-Dec;23(10):2635-40. PubMed PMID: 25238924. Epub 2014/09/23. Eng.

45. Mortezabeigi HR, Taghizadeh A, Talebi M, Amini K, Goldust M. ABCD2 score and BNP level in patients with TIA and cerebral stroke. Pakistan journal of biological sciences : PJBS. 2013 Nov 1;16(21):1393-7. PubMed PMID: 24511754. Epub 2014/02/12. Eng.

46. Mir IN, Chalak LF. Serum biomarkers to evaluate the integrity of the neurovascular unit. Early human development. 2014 Oct;90(10):707-11. PubMed PMID: 25064445. Epub 2014/07/30.eng.

47. Tayal V, Kalra BS. Cytokines and anti-cytokines as therapeutics--an update. European journal of pharmacology. 2008 Jan 28;579(1- 3):1-12. PubMed PMID: 18021769. Epub 2007/11/21. Eng.

48. Rostene W, Dansereau MA, Godefroy D, Van Steenwinckel J, Reaux-Le Goazigo A, Melik-Parsadaniantz S, et al. Neurochemokines: a menage a trois providing new insights on the functions of chemokines in the central nervous system. Journal of neurochemistry. 2011 Sep;118(5):680-94. PubMed PMID: 21722132. Epub 2011/07/05. Eng.

49. Tuttolomondo A, Di Raimondo D, Pecoraro R, Arnao V, Pinto A, Licata G. Inflammation in ischemic stroke subtypes. Current pharmaceutical design. 2012;18(28):4289-310. PubMed PMID: 22390641. Epub 2012/03/07. Eng.

50. Licata G, Tuttolomondo A, Di Raimondo D, Corrao S, Di Sciacca R, Pinto A. Immuno-inflammatory activation in acute cardio-embolic strokes in comparison with other subtypes of ischaemic stroke. Thrombosis and haemostasis. 2009 May;101(5):929-37. PubMed PMID: 19404547. Epub 2009/05/01. Eng.

51. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nature reviews Neuroscience. 2006 Jan;7(1):41-53. PubMed PMID: 16371949. Epub 2005/12/24.eng.

52. Bailey SL, Carpentier PA, McMahon EJ, Begolka WS, Miller SD. Innate and adaptive immune responses of the central nervous system. Critical reviews in immunology. 2006;26(2):149-88. PubMed PMID: 16700651. Epub 2006/05/17. eng.

53. Vela JM, Molina-Holgado E, Arevalo-Martin A, Almazan G, Guaza C. Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells. Molecular and cellular neurosciences. 2002 Jul;20(3):489-502. PubMed PMID: 12139924. Epub2002/07/26. eng.

54. Rodriguez-Yanez M, Castillo J. Role of inflammatory markers in brain ischemia. Current opinion in neurology. 2008 Jun;21(3):353-7. PubMed PMID: 18451722. Epub 2008/05/03. Eng.

55. Herrmann M, Ehrenreich H. Brain derived proteins as markers of acute stroke: their relation to pathophysiology, outcome prediction and neuroprotective drug monitoring. Restorative neurology and neuroscience. 2003;21(3-4):177-90. PubMed PMID: 14530580. Epub 2003/10/08. eng.

56. Herrmann M, Vos P, Wunderlich MT, de Bruijn CH, Lamers KJ. Release of glial tissue-specific proteins after acute stroke: A comparative analysis of serum concentrations of protein S-100B and glial fibrillary acidic protein. Stroke; a journal of cerebral circulation. 2000 Nov;31(11):2670-7. PubMed PMID: 11062293. Epub

2000/11/04. Eng.

57. Wunderlich MT, Ebert AD, Kratz T, Goertler M, Jost S, Herrmann M. Early neurobehavioral outcome after stroke is related to release of neurobiochemical markers of brain damage. Stroke; a journal of cerebral circulation. 1999 Jun;30(6):1190-5. PubMed PMID: 10356098. Epub 1999/06/04. Eng.

58. Cata JP, Abdelmalak B, Farag E. Neurological biomarkers in the perioperative period. British journal of anaesthesia. 2011 Dec;107(6):844-58. PubMed PMID: 22065690. Epub 2011/11/09.eng.

59. Yokobori S, Hosein K, Burks S, Sharma I, Gajavelli S, Bullock R. Biomarkers for the clinical differential diagnosis in traumatic brain injury-- a systematic review. CNS neuroscience & therapeutics. 2013 Aug;19(8):556-65. PubMed PMID: 23710877. Epub 2013/05/29.eng.

60. Kapural M, Krizanac-Bengez L, Barnett G, Perl J, Masaryk T, Apollo D, et al. Serum S-100beta as a possible marker of blood-brain barrier disruption. Brain research. 2002 Jun 14;940(1-2):102-4. PubMed PMID: 12020881. Epub 2002/05/22. Eng.

61. Gazzolo D, Abella R, Frigiola A, Giamberti A, Tina G, Nigro F, et al. Neuromarkers and unconventional biological fluids. The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstet. 2010 Oct;23 Suppl 3:66-9. PubMed PMID: 20836729. Epub 2010/09/15. Eng.

62. Basile AM, Fusi C, Conti AA, Paniccia R, Trefoloni G, Pracucci G, et al. S-100 protein and neuron-specific enolase as markers of subclinical cerebral damage after cardiac surgery: preliminary observation of a 6-month follow-up study. European neurology. 2001;45(3):151-9. PubMed PMID: 11306858. Epub 2001/04/18.Eng.

63. Karkela J, Bock E, Kaukinen S. CSF and serum brain-specific creatine kinase isoenzyme (CK-BB), neuron-specific enolase (NSE) and neural cell adhesion molecule (NCAM) as prognostic markers for hypoxic brain injury after cardiac arrest in man. Journal of the neurological sciences. 1993 May;116(1):100-9. PubMed PMID: 8509798. Epub 1993/05/01. Eng.

64. Wunderlich MT, Lins H, Skalej M, Wallesch CW, Goertler M. Neuron- specific enolase and tau protein as neurobiochemical markers of neuronal damage are related to early clinical course and long-term outcome in acute ischemic stroke. Clinical neurology and neurosurgery. 2006 Sep;108(6):558-63. PubMed PMID: 16457947. Epub 2006/02/07. Eng.

65. Glickman SW, Phillips S, Anstrom KJ, Laskowitz DT, Cairns CB. Discriminative capacity of biomarkers for acute stroke in the emergency department. The Journal of emergency medicine. 2011 Sep;41(3):333-9. PubMed PMID: 20417054. Epub 2010/04/27. eng.

66. Adam SS, Key NS, Greenberg CS. D-dimer antigen: current concepts and future prospects. Blood. 2009 Mar 26;113(13):2878-87. PubMed PMID: 19008457. Epub 2008/11/15. Eng.

67. Mai H, Xia J, Wu Y, Ke J, Li J, Pan J, et al. Clinical presentation and imaging characteristics of occult lung cancer associated ischemic stroke. Journal of clinical neuroscience : official journal of the Neurosurgical Society of Australasia. 2015 Feb;22(2):296-302. PubMed PMID: 25443087. Epub 2014/12/03. Eng.

68. Kim K, Lee JH. Risk factors and biomarkers of ischemic stroke in cancer patients. Journal of stroke. 2014 May;16(2):91-6. PubMed PMID: 24949315. Pubmed Central PMCID: Pmc4060273. Epub 2014/06/21. Eng.

69. Liu LB, Li M, Zhuo WY, Zhang YS, Xu AD. The role of hs-CRP, D-dimer and fibrinogen in differentiating etiological subtypes of ischemic stroke. PloS one. 2015;10(2):e0118301. PubMed PMID: 25680111. Pubmed Central PMCID: Pmc4332510. Epub 2015/02/14. eng.

70. Zi WJ, Shuai J. Plasma D-dimer levels are associated with stroke subtypes and infarction volume in patients with acute ischemic stroke. PloS one. 2014;9(1):e86465. PubMed PMID: 24466108. Pubmed Central PMCID: Pmc3896474. Epub 2014/01/28. eng.

71. Zecca B, Mandelli C, Maino A, Casiraghi C, Bolla G, Consonni D, et al. A bioclinical pattern for the early diagnosis of cardioembolic stroke. Emergency medicine international. 2014;2014:242171. PubMed PMID: 24734185. Pubmed Central PMCID: Pmc3963221. Epub 2014/04/16. eng.

72. Yuan W, Shi ZH. The relationship between plasma D-dimer levels and outcome of Chinese acute ischemic stroke patients in different stroke subtypes. Journal of neural transmission (Vienna, Austria : 1996). 2014 Apr;121(4):409-13. PubMed PMID: 24201836. Epub 2013/11/10. eng.

73. Wiseman S, Marlborough F, Doubal F, Webb DJ, Wardlaw J. Blood markers of coagulation, fibrinolysis, endothelial dysfunction and inflammation in lacunar stroke versus non-lacunar stroke and non-stroke: systematic review and meta-analysis. Cerebrovascular diseases (Basel, Switzerland). 2014;37(1):64-75. PubMed PMID: 24401164. Epub 2014/01/10. eng.

74. Okazaki T, Yamamoto Y, Yoda K, Nagahiro S. The ratio of D-dimer to brain natriuretic peptide may help to differentiate between cerebral infarction with and without acute aortic dissection. Journal of the neurological sciences. 2014 May 15;340(1-2):133-8. PubMed PMID: 24655734. Epub 2014/03/25. eng.

75. Isenegger J, Meier N, Lammle B, Alberio L, Fischer U, Nedeltchev K, et al. D-dimers predict stroke subtype when assessed early. Cerebrovascular diseases (Basel, Switzerland). 2010;29(1):82-6. PubMed PMID: 19907168. Epub 2009/11/13. eng.

76. Ilhan D, Ozbabalik D, Gulcan E, Ozdemir O, Gulbacs Z. Evaluation of platelet activation, coagulation, and fibrinolytic activation in patients with symptomatic lacunar stroke. The neurologist. 2010 May;16(3):188-91. PubMed PMID: 20445428. Epub 2010/05/07.eng.

77. Haapaniemi E, Tatlisumak T. Is D-dimer helpful in evaluating stroke patients? A systematic review. Acta neurologica Scandinavica. 2009 Mar;119(3):141-50. PubMed PMID: 18705677. Epub 2008/08/19. eng.

78. Montaner J, Perea-Gainza M, Delgado P, Ribo M, Chacon P, Rosell A, et al. Etiologic diagnosis of ischemic stroke subtypes with plasma biomarkers. Stroke; a journal of cerebral circulation. 2008 Aug;39(8):2280-7. PubMed PMID: 18535284. Epub 2008/06/07.eng.

79. Dougu N, Takashima S, Sasahara E, Taguchi Y, Toyoda S, Hirai T, et al. Differential diagnosis of cerebral infarction using an algorithm combining atrial fibrillation and D-dimer level. European journal of neurology. 2008 Mar;15(3):295-300. PubMed PMID: 18290851. Epub 2008/02/23. eng.

80. Squizzato A, Ageno W, Finazzi S, Mera V, Romualdi E, Bossi A, et al. D-dimer is not a long-term prognostic marker following acute cerebral ischemia. Blood coagulation & fibrinolysis : an international journal in haemostasis and thrombosis. 2006 Jun;17(4):303-6. PubMed PMID: 16651873. Epub 2006/05/03. eng.

81. Squizzato A, Ageno W. D-dimer testing in ischemic stroke and cerebral sinus and venous thrombosis. Seminars in vascular medicine. 2005 Nov;5(4):379-86. PubMed PMID: 16302160. Epub 2005/11/23. eng.

82. Koch HJ, Horn M, Bogdahn U, Ickenstein GW. The relationship between plasma D-dimer concentrations and acute ischemic stroke subtypes. Journal of stroke and cerebrovascular diseases: the official journal of National Stroke Association. 2005 Mar- Apr;14(2):75-9. PubMed PMID: 17904004. Epub 2007/10/02. eng.

83. Ageno W, Finazzi S, Steidl L, Biotti MG, Mera V, Melzi D’Eril G, et al. Plasma measurement of D-dimer levels for the early diagnosis of ischemic stroke subtypes. Archives of internal medicine. 2002 Dec 9-23;162(22):2589-93. PubMed PMID: 12456231. Epub2002/12/03. eng.

84. Takano K, Yamaguchi T, Uchida K. Markers of a hypercoagulable state following acute ischemic stroke. Stroke; a journal of cerebral circulation. 1992 Feb;23(2):194-8. PubMed PMID: 1561647. Epub 1992/02/01. eng.

85. Alvarez-Perez FJ, Castelo-Branco M, Alvarez-Sabin J. Albumin level and stroke. Potential association between lower albumin level and cardioembolic aetiology. The International journal of neuroscience. 2011 Jan;121(1):25-32. PubMed PMID: 20954836. Epub 2010/10/20. Eng.

86. Barugh AJ, Gray P, Shenkin SD, MacLullich AM, Mead GE. Cortisol levels and the severity and outcomes of acute stroke: a systematic review. Journal of neurology. 2014 Mar;261(3):533-45. PubMed PMID: 24477489. Pubmed Central PMCID: Pmc4928702. Epub2014/01/31. Eng.

87. Zi WJ, Shuai J. Cortisol as a prognostic marker of short-term outcome in chinese patients with acute ischemic stroke. PloS one. 2013;8(9):e72758. PubMed PMID: 24069157. Pubmed Central PMCID: Pmc3771965. Epub 2013/09/27. Eng.

88. Tu WJ, Dong X, Zhao SJ, Yang DG, Chen H. Prognostic value of plasma neuroendocrine biomarkers in patients with acute ischaemic stroke. Journal of neuroendocrinology. 2013 Sep;25(9):771-8. PubMed PMID: 23701638. Epub 2013/05/25. Eng.

89. Marklund N, Peltonen M, Nilsson TK, Olsson T. Low and high circulating cortisol levels predict mortality and cognitive dysfunction early after stroke. Journal of internal medicine. 2004 Jul;256(1):15-21. PubMed PMID: 15189361. Epub 2004/06/11. Eng.

90. Cummings DM, King DE, Mainous AG, Geesey ME. Combining serum biomarkers: the association of C-reactive protein, insulin sensitivity, and homocysteine with cardiovascular disease history in the general US population. European journal of cardiovascular prevention and rehabilitation : official journal of the European Society of Cardiology, Working Groups on Epidemiology & Prevention and Cardiac Rehabilitation and Exercise Physiology. 2006 Apr;13(2):180-5. PubMed PMID: 16575270. Epub 2006/04/01. Eng.

91. Chollet F, Albucher JF. Strategies to augment recovery after stroke. Current treatment options in neurology. 2012 Dec;14(6):531-40. PubMed PMID: 22865294. Epub 2012/08/07. eng.

92. Greenberg E, Treger J, Ring H. Post-stroke follow-up in a rehabilitation center outpatient clinic. The Israel Medical Association journal : IMAJ. 2004 Oct;6(10):603-6. PubMed PMID: 15473587. Epub 2004/10/12. eng.

93. Teo K, Slark J. A systematic review of studies investigating the care of stroke survivors in long-term care facilities. Disability and rehabilitation. 2015 Jun 29:1-9. PubMed PMID: 26104106. Epub 2015/06/25. Eng.

94. Advances in Clinical Chemistry. Makowski G, editor: Elsevier; 2016.

95. Jacobsen CE. CobasR h 232 POC system A system for measurement of cardiac biomarkers and a biomarker for venous thromboembolism manufactured by Roche Diagnostics GmbH. Report from the evaluation SKUP/2013/97 of NT-proBNP on Cobas h 232 organised by SKUP at the request of Roche Diagnostics Norway AS.

96. Zhuo Y, Yi WJ, Lian WB, Yuan R, Chai YQ, Chen A, et al. Ultrasensitive electrochemical strategy for NT-proBNP detection with gold nanochains and horseradish peroxidase complex amplification. Biosens Bioelectron. 2011 Jan 15;26(5):2188-93. PubMed PMID: 20952179.

97. de Avila BE, Escamilla-Gomez V, Campuzano S, Pedrero M, Pingarron JM. Disposable amperometric magnetoimmunosensor for the sensitive detection of the cardiac biomarker amino-terminal pro-B-type natriuretic peptide in human serum. Anal Chim Acta. 2013 Jun 19;784:18-24. PubMed PMID: 23746403.

98. Sinawang PD, Rai V, Ionescu RE, Marks RS. Electrochemical lateral flow immunosensor for detection and quantification of dengue NS1 protein. Biosens Bioelectron. 2016 Mar 15;77:400-8. PubMed PMID: 26433352.

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