SerumPro-Oxidant-Antioxidant Balance, Advanced Oxidized Protein Products (AOPP) and Protein Carbonyl in PatientsWith Stroke

Authors

1 Department of Biochemistry, Faculty of Medicine,Mashhad University of Medical Sciences,Mashhad, IR Iran

2 Surgical Oncology Research Center, ImamReza Hospital, Faculty of Medicine,Mashhad University of Medical Sciences,Mashhad, IR Iran

3 Department of Neurology, GhaemHospital,Mashhad University of Medical Sciences,Mashhad, IR Iran

4 Biochemistry of Nutrition Research Center,Mashhad University of Medical Sciences,Mashhad, IR Iran

5 Department of Biochemistry, Biochemistry and Nutrition Research Center, Faculty of Medicine,Mashhad University of Medical Sciences,Mashhad, IR Iran

Abstract

 Background: Stroke is the second cause of death and disability in the world, and oxidative stress which could be considered as a prognostic factor in patients for prevention, follow up and determination of stroke’s severity has a conceivable role in neural damage.
 
Objectives: The aim of our study was to explain the association between oxidant/antioxidant imbalance as a prognostic factor in patients with stroke.
 
Methods: Pro-oxidant-antioxidant balance (PAB), advanced oxidized protein products (AOPP) and protein carbonyl were measured in patients with ischemic stroke and hemorrhagic stroke as well as healthy group. Sera were collected from 18 is- chemic and 23 hemorrhagic stroke patients, and 34 healthy volunteers. The PAB assay, routine biochemical parameters, lipid profile and total protein concentration were assessed in patients and healthy group.
 
Results: The level of AOPP (P < 0.007), protein carbonyl (P < 0.001) and PAB (P < 0.01) were significantly higher in stroke patients than the healthy group.
 
Conclusions: There are increased level of protein carbonyl, AOPP and PAB in patients with stroke. Measuring these factors may be beneficial as prognostic factors in treatment and follow up of the patients with both hemorrhagic and ischemic strokes. More investigations withmore cases and longer follow up are needed to approve that these factors play an important role in prognosis of stroke.

Keywords


Open Access Policy: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/

1. Hankey GJ, Warlow CP. Treatment and secondary prevention of stroke: evidence, costs, and effects on individuals and populations. Lancet. 1999;354(9188):1457-63. [PubMed: 10543686].
https://doi.org/10.1016/S0140-6736(99)04407-4
PMid:10543686
 
2. Sarti C, Rastenyte D, Cepaitis Z, Tuomilehto J. International trends in mortality from stroke, 1968 to 1994. Stroke. 2000;31(7):1588-601. [PubMed: 10884459].
https://doi.org/10.1161/01.STR.31.7.1588
PMid:10884459
 
3. Rathore SS, Hinn AR, Cooper LS, Tyroler HA, Rosamond WD. Characterization of incident stroke signs and symptoms: findings from the atherosclerosis risk in communities study. Stroke. 2002;33(11):2718-21. [PubMed: 12411667].
https://doi.org/10.1161/01.STR.0000035286.87503.31
PMid:12411667
 
4. Kothari R, Sauerbeck L, Jauch E, Broderick J, Brott T, Khoury J, et al. Patients' awareness of stroke signs, symptoms, and risk factors. Stroke. 1997;28(10):1871-5. [PubMed: 9341687].
https://doi.org/10.1161/01.STR.28.10.1871
PMid:9341687
 
5. Goszcz K, Deakin SJ, Duthie GG, Stewart D, Leslie SJ, Megson IL. Antioxidants in Cardiovascular Therapy: Panacea or False Hope?. Front Cardiovasc Med. 2015;2:29. [PubMed: 26664900].
https://doi.org/10.3389/fcvm.2015.00029
PMid:26664900 PMCid:PMC4671344
 
6. Goldstein LB, Amarenco P, Szarek M, Callahan A3, Hennerici M, Sillesen H, et al. Hemorrhagic stroke in the Stroke Prevention by Aggressive Reduction in Cholesterol Levels study. Neurology. 2008;70(24 Pt 2):2364-70. [PubMed: 18077795].
https://doi.org/10.1212/01.wnl.0000296277.63350.77
PMid:18077795
 
7. Yano K, Reed DM, MacLean CJ. Serum cholesterol and hemorrhagic stroke in the Honolulu Heart Program. Stroke. 1989;20(11):1460-5. [PubMed: 2815179].
https://doi.org/10.1161/01.STR.20.11.1460
PMid:2815179
 
8. Gibbons GH. Collaborative partnership model results in new cardiovascular disease prevention guidelines. NHLBI; 2013.
 
9. El Kossi MM, Zakhary MM. Oxidative stress in the context of acute cerebrovascular stroke. Stroke. 2000;31(8):1889-92. [PubMed: 10926952].
https://doi.org/10.1161/01.STR.31.8.1889
PMid:10926952
 
10. Parizadeh MR, Azarpazhooh MR, Mobarra N, Nematy M, Alamdari DH, Tavalaie S, et al. Prooxidant-antioxidant balance in stroke patients and 6-month prognosis. Clin Lab. 2011;57(3-4):183-91. [PubMed: 21500725].
 
11. Lucivero V, Prontera M, Mezzapesa DM, Petruzzellis M, Sancilio M, Tinelli A, et al. Different roles of matrix metalloproteinases-2 and - 9 after human ischaemic stroke. Neurol Sci. 2007;28(4):165-70. [PubMed: 17690845].
https://doi.org/10.1007/s10072-007-0814-0
PMid:17690845
 
12. Polidori MC, Frei B, Cherubini A, Nelles G, Rordorf G, Keaney JJ, et al. Increased plasma levels of lipid hydroperoxides in patients with ischemic stroke. Free Radic Biol Med. 1998;25(4-5):561-7. [PubMed: 9741593].
https://doi.org/10.1016/S0891-5849(98)00085-9
PMid:9741593
 
13. Dominguez C, Delgado P, Vilches A, Martin-Gallan P, Ribo M, Santamarina E, et al. Oxidative stress after thrombolysis-induced reperfusion in human stroke. Stroke. 2010;41(4):653-60. [PubMed: 20185784].
https://doi.org/10.1161/STROKEAHA.109.571935
PMid:20185784
 
14. Betteridge DJ. What is oxidative stress?. Metabolism. 2000;49(2 Suppl 1):3-8. [PubMed: 10693912].
https://doi.org/10.1016/S0026-0495(00)80077-3
PMid:10693912
 
15. Yorek MA. The role of oxidative stress in diabetic vascular and neural disease. Free Radic Res. 2003;37(5):471-80. [PubMed: 12797466].
https://doi.org/10.1080/1071576031000083161
PMid:12797466
 
16. Piantadosi CA, Zhang J. Mitochondrial generation of reactive oxygen species after brain ischemia in the rat. Stroke. 1996;27(2):327-31. [PubMed: 8571432] discussion 32.
https://doi.org/10.1161/01.STR.27.2.327
PMid:8571432
 
17. Halliwell B. Oxidative stress and cancer: have we moved forward?. Biochem J. 2007;401(1):1-11. [PubMed: 17150040].
https://doi.org/10.1042/BJ20061131
PMid:17150040
 
18. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis. 2007;12(5):913-22. [PubMed: 17453160].
https://doi.org/10.1007/s10495-007-0756-2
PMid:17453160
 
19. Paschen W. Endoplasmic reticulum dysfunction in brain pathology: critical role of protein synthesis. Curr Neurovasc Res. 2004;1(2):173-81. [PubMed: 16185192].
https://doi.org/10.2174/1567202043480125
PMid:16185192
 
20. Murakami K, Kondo T, Kawase M, Li Y, Sato S, Chen SF, et al. Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency. J Neurosci. 1998;18(1):205-13. [PubMed: 9412501].
https://doi.org/10.1523/JNEUROSCI.18-01-00205.1998
PMid:9412501 PMCid:PMC6793388
 
21. Kannan K, Jain SK. Oxidative stress and apoptosis. Pathophysiology. 2000;7(3):153-63. [PubMed: 10996508].
https://doi.org/10.1016/S0928-4680(00)00053-5
PMid:10996508
 
22. Kong SY, Goodman M, Judd S, Bostick RM, Flanders WD, McClellan W. Oxidative balance score as predictor of all-cause, cancer, and noncancer mortality in a biracial US cohort. Ann Epidemiol. 2015;25(4):256-62 e1. [PubMed: 25682727].
https://doi.org/10.1016/j.annepidem.2015.01.004
PMid:25682727 PMCid:PMC4369443
 
23. Amer J, Ghoti H, Rachmilewitz E, Koren A, Levin C, Fibach E. Red blood cells, platelets and polymorphonuclear neutrophils of patients with sickle cell disease exhibit oxidative stress that can be ameliorated by antioxidants. Br J Haematol. 2006;132(1):108-13. [PubMed: 16371026].
https://doi.org/10.1111/j.1365-2141.2005.05834.x
PMid:16371026
 
24. Asmat U, Abad K, Ismail K. Diabetes mellitus and oxidative stress-A concise review. Saudi Pharm J. 2015 doi: 10.1016/j.jsps.2015.03.013.
https://doi.org/10.1016/j.jsps.2015.03.013
PMid:27752226 PMCid:PMC5059829
 
25. Bonomini F, Tengattini S, Fabiano A, Bianchi R, Rezzani R. Atherosclerosis and oxidative stress. Histol Histopathol. 2008;23(3):381-90. [PubMed: 18072094].
 
26. Pohanka M. Alzheimer s disease and oxidative stress: a review. Curr Med Chem. 2014;21(3):356-64. [PubMed: 24059239].
https://doi.org/10.2174/09298673113206660258
PMid:24059239
 
27. Tsutsui H, Kinugawa S, Matsushima S. Oxidative stress and heart failure. Am J Physiol Heart Circ Physiol. 2011;301(6):H2181-90. [PubMed: 21949114]. Razavi Int J Med. 2016; 4(2):e38203. 5 Toloue Pouya V et al.
https://doi.org/10.1152/ajpheart.00554.2011
PMid:21949114
 
28. Dhalla NS, Temsah RM, Netticadan T. Role of oxidative stress in cardiovascular diseases. J Hypertens. 2000;18(6):655-73. [PubMed: 10872549].
https://doi.org/10.1097/00004872-200018060-00002
PMid:10872549
 
29. James SJ, Cutler P, Melnyk S, Jernigan S, Janak L, Gaylor DW, et al. Metabolic biomarkers of increased oxidative stress and impaired methylation capacity in children with autism. Am J Clin Nutr. 2004;80(6):1611-7. [PubMed: 15585776].
https://doi.org/10.1093/ajcn/80.6.1611
PMid:15585776
 
30. Pilch W, Szygula Z, Tyka AK, Palka T, Tyka A, Cison T, et al. Disturbances in pro-oxidant-antioxidant balance after passive body overheating and after exercise in elevated ambient temperatures in athletes and untrained men. PLoS One. 2014;9(1):ee85320. [PubMed: 24465535].
https://doi.org/10.1371/journal.pone.0085320
PMid:24465535 PMCid:PMC3896384
 
31. Schauenstein E, Esterbauer H. Formation and properties of reactive aldehydes. Ciba Found Symp. 1979;67:225-44.
https://doi.org/10.1002/9780470720493.ch15
PMid:159812
 
32. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med. 1991;11(1):81-128. [PubMed: 1937131].
https://doi.org/10.1016/0891-5849(91)90192-6
PMid:1937131
 
33. Levine RL, Williams JA, Stadtman ER, Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 1994;233:346-57. [PubMed: 8015469].
https://doi.org/10.1016/S0076-6879(94)33040-9
PMid:8015469
 
34. Alamdari DH, Ghayour-Mobarhan M, Tavallaie S, Parizadeh MR, Moohebati M, Ghafoori F, et al. Prooxidant-antioxidant balance as a new risk factor in patients with angiographically defined coronary artery disease. Clin Biochem. 2008;41(6):375-80. [PubMed: 18191639].
https://doi.org/10.1016/j.clinbiochem.2007.12.008
PMid:18191639
 
35. Capeillere-Blandin C, Gausson V, Descamps-Latscha B, Witko-Sarsat V. Biochemical and spectrophotometric significance of advanced oxidized protein products. Biochim Biophys Acta. 2004;1689(2):91-102. [PubMed: 15196590].
https://doi.org/10.1016/j.bbadis.2004.02.008
PMid:15196590
 
36. Eghwrudjakpor PO, Allison AB. Oxidative stress following traumatic brain injury: enhancement of endogenous antioxidant defense systems and the promise of improved outcome. Niger J Med. 2010;19(1):14-21. [PubMed: 20232751].
https://doi.org/10.4314/njm.v19i1.52466
PMid:20232751
 
37. Malhotra R, Lin Z, Vincenz C, Brosius F3. Hypoxia induces apoptosis via two independent pathways in Jurkat cells: differential regulation by glucose. Am J Physiol Cell Physiol. 2001;281(5):C1596-603. [PubMed: 11600423].
https://doi.org/10.1152/ajpcell.2001.281.5.C1596
PMid:11600423
 
38. Weilinger NL, Maslieieva V, Bialecki J, Sridharan SS, Tang PL, Thompson RJ. Ionotropic receptors and ion channels in ischemic neuronal death and dysfunction. Acta Pharmacol Sin. 2013;34(1):39-48. [PubMed: 22864302].
https://doi.org/10.1038/aps.2012.95
PMid:22864302 PMCid:PMC4086487
 
39. Stys PK. Anoxic and ischemic injury of myelinated axons in CNS white matter: from mechanistic concepts to therapeutics. J Cereb Blood Flow Metab. 1998;18(1):2-25. [PubMed: 9428302].
https://doi.org/10.1097/00004647-199801000-00002
PMid:9428302
 
40. Cao XL, Du J, Zhang Y, Yan JT, Hu XM. Hyperlipidemia exacerbates cerebral injury through oxidative stress, inflammation and neuronal apoptosis in MCAO/reperfusion rats. Exp Brain Res. 2015;233(10):2753- 65. [PubMed: 26238404].
https://doi.org/10.1007/s00221-015-4269-x
PMid:26238404
 
41. Crack PJ, Taylor JM. Reactive oxygen species and the modulation of stroke. Free Radic Biol Med. 2005;38(11):1433-44. [PubMed: 15890617].
https://doi.org/10.1016/j.freeradbiomed.2005.01.019
PMid:15890617
 
42. Simao AN, Lehmann MF, Alfieri DF, Meloni MZ, Flauzino T, Scavuzzi BM, et al. Metabolic syndrome increases oxidative stress but does not influence disability and short-time outcome in acute ischemic stroke patients. Metab Brain Dis. 2015;30(6):1409-16. [PubMed: 26342606].
https://doi.org/10.1007/s11011-015-9720-y
PMid:26342606
 
43. Nilsson GE, Lutz PL. Anoxia tolerant brains. J Cereb Blood Flow Metab. 2004;24(5):475-86. [PubMed: 15129179].
https://doi.org/10.1097/00004647-200405000-00001
PMid:15129179
 
44. Arslan C, Altan H, Besirli K, Aydemir B, Kiziler AR, Denli S. The role of oxidative stress and antioxidant defenses in Buerger disease and atherosclerotic peripheral arterial occlusive disease. Ann Vasc Surg. 2010;24(4):455-60. [PubMed: 19128930].
https://doi.org/10.1016/j.avsg.2008.11.006
PMid:19128930
 
45. Cherubini A, Ruggiero C, Polidori MC, Mecocci P. Potential markers of oxidative stress in stroke. Free Radic Biol Med. 2005;39(7):841-52. [PubMed: 16140205].
https://doi.org/10.1016/j.freeradbiomed.2005.06.025
PMid:16140205
 
46. Uno M, Kitazato KT, Nishi K, Itabe H, Nagahiro S. Raised plasma oxidised LDL in acute cerebral infarction. J Neurol Neurosurg Psychiatry. 2003;74(3):312-6. [PubMed: 12588914].
https://doi.org/10.1136/jnnp.74.3.312
PMid:12588914 PMCid:PMC1738343
 
47. Re G, Azzimondi G, Lanzarini C, Bassein L, Vaona I, Guarnieri C. Plasma lipoperoxidative markers in ischaemic stroke suggest brain embolism. Eur J Emerg Med. 1997;4(1):5-9. [PubMed: 9152688].
https://doi.org/10.1097/00063110-199803000-00004
PMid:10406412
 
48. Belch J, McLaren M, Hanslip J, Hill A, Davidson D. The white blood cell and plasma fibrinogen in thrombotic stroke. A significant correlation. Int Angiol. 1998;17(2):120-4. [PubMed: 9754901].
 
49. Pena-Sanchez M, Riveron-Forment G, Zaldivar-Vaillant T, SotoLavastida A, Borrero-Sanchez J, Lara-Fernandez G, et al. Association of status redox with demographic, clinical and imaging parameters in patients with Huntington's disease. Clin Biochem. 2015;48(18):1258-63. [PubMed: 26210848].
https://doi.org/10.1016/j.clinbiochem.2015.06.014
PMid:26210848
 
50. Siciliano G, Piazza S, Carlesi C, Del Corona A, Franzini M, Pompella A, et al. Antioxidant capacity and protein oxidation in cerebrospinal fluid of amyotrophic lateral sclerosis. J Neurol. 2007;254(5):575-80. [PubMed: 17426914].
https://doi.org/10.1007/s00415-006-0301-1
PMid:17426914
 
51. Kaneda H, Taguchi J, Ogasawara K, Aizawa T, Ohno M. Increased level of advanced oxidation protein products in patients with coronary artery disease. Atherosclerosis. 2002;162(1):221-5. [PubMed: 11947918].
https://doi.org/10.1016/S0021-9150(01)00706-7
PMid:11947918
 
52. Kalousova M, Zima T, Tesar V, Sulkova S, Fialova L. Relationship between advanced glycoxidation end products, inflammatory markers/acute-phase reactants, and some autoantibodies in chronic hemodialysis patients. Kidney Int Suppl. 2003(84):S62-4. [PubMed: 12694311].
https://doi.org/10.1046/j.1523-1755.63.s84.19.x
PMid:12694311
 
53. Cichon N, Bijak M, Miller E, Niwald M, Saluk J. Poststroke depression as a factor adversely affecting the level of oxidative damage to plasma proteins during a brain stroke. Oxid Med Cell Longev. 2015;2015:408745. [PubMed: 25838867].
https://doi.org/10.1155/2015/408745
PMid:25838867 PMCid:PMC4370103
 
54. Moon GJ, Kim SJ, Cho YH, Ryoo S, Bang OY. Antioxidant effects of statins in patients with atherosclerotic cerebrovascular disease. J Clin Neurol. 2014;10(2):140-7. [PubMed: 24829600].
https://doi.org/10.3988/jcn.2014.10.2.140
PMid:24829600 PMCid:PMC4017017