Role of soluble fractalkine, GFAP and CD163 in cognitive functions after open heart surgery in diabetic and non-diabetic patients

Arif Ozbay; Sureyya Barun; Aybeniz Civan Kahve; Abdullah Özer; Özlem Gülbahar; Hasan Dağlı; Seçil Özkan; Dilek Erer

doi:10.31067/acusaglik.1124251

Research Article

Year 2022, , 565 - 573, 01.10.2022

Arif Ozbay Sureyya Barun Aybeniz Civan Kahve , Abdullah Özer , Özlem Gülbahar , Hasan Dağlı , Seçil Özkan , Dilek Erer

https://doi.org/10.31067/acusaglik.1124251

Abstract

References

1. Rundshagen I. Postoperative cognitive dysfunction. Dtsch Arztebl Int. 2014;111(8):119-125.
2. Bedford PD. Adverse cerebral effects of anaesthesia on old people. Lancet. 1955;269(6884):259-263.
3. Ramlawi B, Rudolph JL, Mieno S, et al. C-Reactive protein and inflammatory response associated to neurocognitive decline following cardiac surgery. Surgery. 2006;140(2):221-226.
4. Rasmussen LS. Postoperative cognitive dysfunction: incidence and prevention. Best Pract Res Clin Anaesthesiol. 2006;20(2):315-330.
5. Shaw PJ, Bates D, Cartlidge NE, French JM, Heaviside D, Julian DG, Shaw DA. Neurologic and neuropsychological morbidity following major surgery: comparison of coronary artery bypass and peripheral vascular surgery. Stroke. 1987;18(4):700-707.
6. Newman S, Stygall J, Hirani S, Shaefi S, Maze M. Postoperative cognitive dysfunction after noncardiac surgery: a systematic review. Anesthesiology. 2007;106(3):572-590.
7. Gao L, Taha R, Gauvin D, Othmen LB, Wang Y, Blaise G. Postoperative cognitive dysfunction after cardiac surgery. Chest. 2005;128(5):3664-3670.
8. Wang W, Wang Y, Wu H, et al. Postoperative cognitive dysfunction: current developments in mechanism and prevention. Med Sci Monit. 2014;20:1908-1912.
9. Browne SM, Halligan PW, Wade DT, Taggart DP. Postoperative hypoxia is a contributory factor to cognitive impairment after cardiac surgery. J Thorac Cardiovasc Surg. 2003;126(4):1061-1064.
10. Kadoi Y, Goto F. Factors associated with postoperative cognitive dysfunction in patients undergoing cardiac surgery. Surg Today. 2006;36(12):1053-1057.
11. Newman MF, Grocott HP, Mathew JP, et al. Report of the substudy assessing the impact of neurocognitive function on quality of life 5 years after cardiac surgery. Stroke. 2001;32(12):2874-2881.
12. Skvarc DR, Berk M, Byrne LK, et al. Post-Operative Cognitive Dysfunction: An exploration of the inflammatory hypothesis and novel therapies. Neurosci Biobehav Rev. 2018;84:116-133.
13. Glumac S, Kardum G, Sodic L, Supe-Domic D, Karanovic N. Effects of dexamethasone on early cognitive decline after cardiac surgery: A randomised controlled trial. Eur J Anaesthesiol. 2017;34(11):776-784.
14. Barrientos RM, Hein AM, Frank MG, Watkins LR, Maier SF. Intracisternal interleukin-1 receptor antagonist prevents postoperative cognitive decline and neuroinflammatory response in aged rats. J Neurosci. 2012;32(42):14641-14648.
15. Hovens IB, van Leeuwen BL, Mariani MA, Kraneveld AD, Schoemaker RG. Postoperative cognitive dysfunction and neuroinflammation; Cardiac surgery and abdominal surgery are not the same. Brain Behav Immun. 2016;54:178-193.
16. Kodl CT, Seaquist ER. Cognitive dysfunction and diabetes mellitus. Endocr Rev. 2008;29(4):494-511.
17. Yaffe K, Lindquist K, Penninx BW, et al. Inflammatory markers and cognition in well-functioning African-American and white elders. Neurology. 2003;61(1):76-80.
18. Wright CB, Sacco RL, Rundek T, Delman J, Rabbani L, Elkind M. Interleukin-6 is associated with cognitive function: the Northern Manhattan Study. J Stroke Cerebrovasc Dis. 2006;15(1):34-38.
19. Lauro C, Catalano M, Trettel F, Limatola C. Fractalkine in the nervous system: neuroprotective or neurotoxic molecule? Ann N Y Acad Sci. 2015;1351:141-148.
20. Maciejewski-Lenoir D, Chen S, Feng L, Maki R, Bacon KB. Characterization of fractalkine in rat brain cells: migratory and activation signals for CX3CR-1-expressing microglia. J Immunol. 1999;163(3):1628-1635.
21. Suzumura A. Neuron-microglia interaction in neuroinflammation. Curr Protein Pept Sci. 2013;14(1):16-20.
22. Finneran DJ, Nash KR. Neuroinflammation and fractalkine signaling in Alzheimer's disease. J Neuroinflammation. 2019;16(1):30.
23. Kim TS, Lim HK, Lee JY, Kim DJ, Park S, Lee C, Lee CU. Changes in the levels of plasma soluble fractalkine in patients with mild cognitive impairment and Alzheimer's disease. Neurosci Lett. 2008;436(2):196-200.
24. Chang YC, Kim HW, Rapoport SI, Rao JS. Chronic NMDA administration increases neuroinflammatory markers in rat frontal cortex: cross-talk between excitotoxicity and neuroinflammation. Neurochem Res. 2008;33(11):2318-2323.
25. Rappold T, Laflam A, Hori D, et al. Evidence of an association between brain cellular injury and cognitive decline after non-cardiac surgery. Br J Anaesth. 2016;116(1):83-89.
26. Kowal K, Silver R, Slawinska E, Bielecki M, Chyczewski L, Kowal-Bielecka O. CD163 and its role in inflammation. Folia Histochem Cytobiol. 2011;49(3):365-374.
27. Sandireddy R, Yerra VG, Areti A, Komirishetty P, Kumar A. Neuroinflammation and oxidative stress in diabetic neuropathy: futuristic strategies based on these targets. Int J Endocrinol. 2014;2014:674987.
28. Singh R, Kishore L, Kaur N. Diabetic peripheral neuropathy: current perspective and future directions. Pharmacol Res. 2014;80:21-35.
29. Yan SD, Schmidt AM, Anderson GM, Zhang J, Brett J, Zou YS, Pinsky D, Stern D. Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem. 1994;269(13):9889-9897.
30. Wada R, Yagihashi S. Role of advanced glycation end products and their receptors in development of diabetic neuropathy. Ann N Y Acad Sci. 2005;1043:598-604.
31. King RH. The role of glycation in the pathogenesis of diabetic polyneuropathy. Mol Pathol. 2001;54(6):400-408.
32. Feinkohl I, Winterer G, Pischon T. Diabetes is associated with risk of postoperative cognitive dysfunction: A meta-analysis. Diabetes Metab Res Rev. 2017;33(5).
33. Rom S, Zuluaga-Ramirez V, Gajghate S, et al. Hyperglycemia-Driven Neuroinflammation Compromises BBB Leading to Memory Loss in Both Diabetes Mellitus (DM) Type 1 and Type 2 Mouse Models. Mol Neurobiol. 2019;56(3):1883-1896.
34. Guo L, Lu X, Wang Y, Bao C, Chen S. Elevated levels of soluble fractalkine and increased expression of CX3CR1 in neuropsychiatric systemic lupus erythematosus. Exp Ther Med. 2017;14(4):3153-3158.
35. Nakayama W, Jinnin M, Makino K, Kajihara I, Makino T, Fukushima S, Inoue Y, Ihn H. Serum levels of soluble CD163 in patients with systemic sclerosis. Rheumatol Int. 2012;32(2):403-407.
36. Benchimol EI, Smeeth L, Guttmann A, et al. The REporting of studies Conducted using Observational Routinely-collected health Data (RECORD) statement. PLoS Med. 2015;12(10):e1001885.
37. McGeer EG, McGeer PL. Neuroinflammation in Alzheimer's disease and mild cognitive impairment: a field in its infancy. J Alzheimers Dis. 2010;19(1):355-361.
38. Tweedie D, Ferguson RA, Fishman K, et al. Tumor necrosis factor-alpha synthesis inhibitor 3,6'-dithiothalidomide attenuates markers of inflammation, Alzheimer pathology and behavioral deficits in animal models of neuroinflammation and Alzheimer's disease. J Neuroinflammation. 2012;9:106.
39. Ju H, Wang Y, Shi Q, Zhou Y, Ma R, Wu P, Fang H. Inhibition of connexin 43 hemichannels improves postoperative cognitive function in aged mice. Am J Transl Res. 2019;11(4):2280-2287.
40. Lu Y, Xu X, Dong R, Sun L, Chen L, Zhang Z, Peng M. MicroRNA-181b-5p attenuates early postoperative cognitive dysfunction by suppressing hippocampal neuroinflammation in mice. Cytokine. 2019;120:41-53.
41. Nishigaki A, Kawano T, Iwata H, et al. Acute and long-term effects of haloperidol on surgery-induced neuroinflammation and cognitive deficits in aged rats. J Anesth. 2019;33(3):416-425.
42. Etzerodt A, Maniecki MB, Moller K, Moller HJ, Moestrup SK. Tumor necrosis factor alpha-converting enzyme (TACE/ADAM17) mediates ectodomain shedding of the scavenger receptor CD163. J Leukoc Biol. 2010;88(6):1201-1205.
43. Hintz KA, Rassias AJ, Wardwell K, et al. Endotoxin induces rapid metalloproteinase-mediated shedding followed by up-regulation of the monocyte hemoglobin scavenger receptor CD163. J Leukoc Biol. 2002;72(4):711-717.
44. Yona S, Jung S. Monocytes: subsets, origins, fates and functions. Curr Opin Hematol. 2010;17(1):53-59.
45. Brahmachari S, Fung YK, Pahan K. Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide. J Neurosci. 2006;26(18):4930-4939.
46. Zhang S, Wu M, Peng C, Zhao G, Gu R. GFAP expression in injured astrocytes in rats. Exp Ther Med. 2017;14(3):1905-1908.
47. Etzerodt A, Moestrup SK. CD163 and inflammation: biological, diagnostic, and therapeutic aspects. Antioxid Redox Signal. 2013;18(17):2352-2363.
48. Akerfeldt T, Helmersson-Karlqvist J, Gordh T, Larsson A. Circulating human fractalkine is decreased post-operatively after orthopedic and coronary bypass surgery. In Vivo. 2014;28(2):185-188.
49. Xu B, Qian Y, Zhao Y, Fang Z, Tang K, Zhou N, Li D, Wang J. Prognostic value of fractalkine/CX3CL1 concentration in patients with acute myocardial infarction treated with primary percutaneous coronary intervention. Cytokine. 2019;113:365-370.
50. Jungwirth B, Zieglgansberger W, Kochs E, Rammes G. Anesthesia and postoperative cognitive dysfunction (POCD). Mini Rev Med Chem. 2009;9(14):1568-1579.
51. Tan AMY, Amoako D. Postoperative cognitive dysfunction after cardiac surgery. Continuing Education in Anaesthesia Critical Care & Pain. 2013;13(6):218-223.
52. van Harten AE, Scheeren TW, Absalom AR. A review of postoperative cognitive dysfunction and neuroinflammation associated with cardiac surgery and anaesthesia. Anaesthesia. 2012;67(3):280-293.
53. Rudolph JL, Schreiber KA, Culley DJ, McGlinchey RE, Crosby G, Levitsky S, Marcantonio ER. Measurement of post-operative cognitive dysfunction after cardiac surgery: a systematic review. Acta Anaesthesiol Scand. 2010;54(6):663-677.

Role of soluble fractalkine, GFAP and CD163 in cognitive functions after open heart surgery in diabetic and non-diabetic patients

Year 2022, , 565 - 573, 01.10.2022

Arif Ozbay Sureyya Barun Aybeniz Civan Kahve , Abdullah Özer , Özlem Gülbahar , Hasan Dağlı , Seçil Özkan , Dilek Erer

https://doi.org/10.31067/acusaglik.1124251

Abstract

Purpose: In this study, the relationship between postoperative cognitive functions and serum fractalkine, Glial Fibrillar Acidic Protein (GFAP) and Cluster of differentiation 163 (CD163) levels in diabetic and non-diabetic patients after open heart surgery was evaluated.
Methods and Materials: This research was planned prospectively as observational clinical study. Cognitive functions, fractalkine, GFAP and CD163 levels were evaluated with preoperative day 1 and postoperative day 7 in 44 patients. Minimental test (MM) was used to evaluate cognitive functions.
Results: A positive correlation was found between preoperative CD163 concentrations and postoperative MM test scores in non-diabetic patients (r=0.536, p=0.010). There was also a positive correlation between postoperative CD163 concentrations and postoperative MM Test scores in non-diabetics (r=0.461, p=0.031). In diabetic patients, a positive correlation was found between preoperative and postoperative GFAP concentrations (r=0.792, p<0.001).
Conclusion: The underlying mechanisms of Postoperative cognitive dysfunction (POCD) are thought to be different in non-diabetic and diabetic patients. Evidence suggesting that preoperative serum CD163 levels may be a candidate for biomarkers directly related to postoperative cognitive performance in non-diabetic patients. In order to prevent POCD, which is associated with mortality, it is important to determine the predictors before surgery and to select the surgical method and anesthetics according to the risk assessment.

Keywords

cognitive functions, inflammation, CD163, fractalkine, GFAP, heart surgery

References

1. Rundshagen I. Postoperative cognitive dysfunction. Dtsch Arztebl Int. 2014;111(8):119-125.
2. Bedford PD. Adverse cerebral effects of anaesthesia on old people. Lancet. 1955;269(6884):259-263.
3. Ramlawi B, Rudolph JL, Mieno S, et al. C-Reactive protein and inflammatory response associated to neurocognitive decline following cardiac surgery. Surgery. 2006;140(2):221-226.
4. Rasmussen LS. Postoperative cognitive dysfunction: incidence and prevention. Best Pract Res Clin Anaesthesiol. 2006;20(2):315-330.
5. Shaw PJ, Bates D, Cartlidge NE, French JM, Heaviside D, Julian DG, Shaw DA. Neurologic and neuropsychological morbidity following major surgery: comparison of coronary artery bypass and peripheral vascular surgery. Stroke. 1987;18(4):700-707.
6. Newman S, Stygall J, Hirani S, Shaefi S, Maze M. Postoperative cognitive dysfunction after noncardiac surgery: a systematic review. Anesthesiology. 2007;106(3):572-590.
7. Gao L, Taha R, Gauvin D, Othmen LB, Wang Y, Blaise G. Postoperative cognitive dysfunction after cardiac surgery. Chest. 2005;128(5):3664-3670.
8. Wang W, Wang Y, Wu H, et al. Postoperative cognitive dysfunction: current developments in mechanism and prevention. Med Sci Monit. 2014;20:1908-1912.
9. Browne SM, Halligan PW, Wade DT, Taggart DP. Postoperative hypoxia is a contributory factor to cognitive impairment after cardiac surgery. J Thorac Cardiovasc Surg. 2003;126(4):1061-1064.
10. Kadoi Y, Goto F. Factors associated with postoperative cognitive dysfunction in patients undergoing cardiac surgery. Surg Today. 2006;36(12):1053-1057.
11. Newman MF, Grocott HP, Mathew JP, et al. Report of the substudy assessing the impact of neurocognitive function on quality of life 5 years after cardiac surgery. Stroke. 2001;32(12):2874-2881.
12. Skvarc DR, Berk M, Byrne LK, et al. Post-Operative Cognitive Dysfunction: An exploration of the inflammatory hypothesis and novel therapies. Neurosci Biobehav Rev. 2018;84:116-133.
13. Glumac S, Kardum G, Sodic L, Supe-Domic D, Karanovic N. Effects of dexamethasone on early cognitive decline after cardiac surgery: A randomised controlled trial. Eur J Anaesthesiol. 2017;34(11):776-784.
14. Barrientos RM, Hein AM, Frank MG, Watkins LR, Maier SF. Intracisternal interleukin-1 receptor antagonist prevents postoperative cognitive decline and neuroinflammatory response in aged rats. J Neurosci. 2012;32(42):14641-14648.
15. Hovens IB, van Leeuwen BL, Mariani MA, Kraneveld AD, Schoemaker RG. Postoperative cognitive dysfunction and neuroinflammation; Cardiac surgery and abdominal surgery are not the same. Brain Behav Immun. 2016;54:178-193.
16. Kodl CT, Seaquist ER. Cognitive dysfunction and diabetes mellitus. Endocr Rev. 2008;29(4):494-511.
17. Yaffe K, Lindquist K, Penninx BW, et al. Inflammatory markers and cognition in well-functioning African-American and white elders. Neurology. 2003;61(1):76-80.
18. Wright CB, Sacco RL, Rundek T, Delman J, Rabbani L, Elkind M. Interleukin-6 is associated with cognitive function: the Northern Manhattan Study. J Stroke Cerebrovasc Dis. 2006;15(1):34-38.
19. Lauro C, Catalano M, Trettel F, Limatola C. Fractalkine in the nervous system: neuroprotective or neurotoxic molecule? Ann N Y Acad Sci. 2015;1351:141-148.
20. Maciejewski-Lenoir D, Chen S, Feng L, Maki R, Bacon KB. Characterization of fractalkine in rat brain cells: migratory and activation signals for CX3CR-1-expressing microglia. J Immunol. 1999;163(3):1628-1635.
21. Suzumura A. Neuron-microglia interaction in neuroinflammation. Curr Protein Pept Sci. 2013;14(1):16-20.
22. Finneran DJ, Nash KR. Neuroinflammation and fractalkine signaling in Alzheimer's disease. J Neuroinflammation. 2019;16(1):30.
23. Kim TS, Lim HK, Lee JY, Kim DJ, Park S, Lee C, Lee CU. Changes in the levels of plasma soluble fractalkine in patients with mild cognitive impairment and Alzheimer's disease. Neurosci Lett. 2008;436(2):196-200.
24. Chang YC, Kim HW, Rapoport SI, Rao JS. Chronic NMDA administration increases neuroinflammatory markers in rat frontal cortex: cross-talk between excitotoxicity and neuroinflammation. Neurochem Res. 2008;33(11):2318-2323.
25. Rappold T, Laflam A, Hori D, et al. Evidence of an association between brain cellular injury and cognitive decline after non-cardiac surgery. Br J Anaesth. 2016;116(1):83-89.
26. Kowal K, Silver R, Slawinska E, Bielecki M, Chyczewski L, Kowal-Bielecka O. CD163 and its role in inflammation. Folia Histochem Cytobiol. 2011;49(3):365-374.
27. Sandireddy R, Yerra VG, Areti A, Komirishetty P, Kumar A. Neuroinflammation and oxidative stress in diabetic neuropathy: futuristic strategies based on these targets. Int J Endocrinol. 2014;2014:674987.
28. Singh R, Kishore L, Kaur N. Diabetic peripheral neuropathy: current perspective and future directions. Pharmacol Res. 2014;80:21-35.
29. Yan SD, Schmidt AM, Anderson GM, Zhang J, Brett J, Zou YS, Pinsky D, Stern D. Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem. 1994;269(13):9889-9897.
30. Wada R, Yagihashi S. Role of advanced glycation end products and their receptors in development of diabetic neuropathy. Ann N Y Acad Sci. 2005;1043:598-604.
31. King RH. The role of glycation in the pathogenesis of diabetic polyneuropathy. Mol Pathol. 2001;54(6):400-408.
32. Feinkohl I, Winterer G, Pischon T. Diabetes is associated with risk of postoperative cognitive dysfunction: A meta-analysis. Diabetes Metab Res Rev. 2017;33(5).
33. Rom S, Zuluaga-Ramirez V, Gajghate S, et al. Hyperglycemia-Driven Neuroinflammation Compromises BBB Leading to Memory Loss in Both Diabetes Mellitus (DM) Type 1 and Type 2 Mouse Models. Mol Neurobiol. 2019;56(3):1883-1896.
34. Guo L, Lu X, Wang Y, Bao C, Chen S. Elevated levels of soluble fractalkine and increased expression of CX3CR1 in neuropsychiatric systemic lupus erythematosus. Exp Ther Med. 2017;14(4):3153-3158.
35. Nakayama W, Jinnin M, Makino K, Kajihara I, Makino T, Fukushima S, Inoue Y, Ihn H. Serum levels of soluble CD163 in patients with systemic sclerosis. Rheumatol Int. 2012;32(2):403-407.
36. Benchimol EI, Smeeth L, Guttmann A, et al. The REporting of studies Conducted using Observational Routinely-collected health Data (RECORD) statement. PLoS Med. 2015;12(10):e1001885.
37. McGeer EG, McGeer PL. Neuroinflammation in Alzheimer's disease and mild cognitive impairment: a field in its infancy. J Alzheimers Dis. 2010;19(1):355-361.
38. Tweedie D, Ferguson RA, Fishman K, et al. Tumor necrosis factor-alpha synthesis inhibitor 3,6'-dithiothalidomide attenuates markers of inflammation, Alzheimer pathology and behavioral deficits in animal models of neuroinflammation and Alzheimer's disease. J Neuroinflammation. 2012;9:106.
39. Ju H, Wang Y, Shi Q, Zhou Y, Ma R, Wu P, Fang H. Inhibition of connexin 43 hemichannels improves postoperative cognitive function in aged mice. Am J Transl Res. 2019;11(4):2280-2287.
40. Lu Y, Xu X, Dong R, Sun L, Chen L, Zhang Z, Peng M. MicroRNA-181b-5p attenuates early postoperative cognitive dysfunction by suppressing hippocampal neuroinflammation in mice. Cytokine. 2019;120:41-53.
41. Nishigaki A, Kawano T, Iwata H, et al. Acute and long-term effects of haloperidol on surgery-induced neuroinflammation and cognitive deficits in aged rats. J Anesth. 2019;33(3):416-425.
42. Etzerodt A, Maniecki MB, Moller K, Moller HJ, Moestrup SK. Tumor necrosis factor alpha-converting enzyme (TACE/ADAM17) mediates ectodomain shedding of the scavenger receptor CD163. J Leukoc Biol. 2010;88(6):1201-1205.
43. Hintz KA, Rassias AJ, Wardwell K, et al. Endotoxin induces rapid metalloproteinase-mediated shedding followed by up-regulation of the monocyte hemoglobin scavenger receptor CD163. J Leukoc Biol. 2002;72(4):711-717.
44. Yona S, Jung S. Monocytes: subsets, origins, fates and functions. Curr Opin Hematol. 2010;17(1):53-59.
45. Brahmachari S, Fung YK, Pahan K. Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide. J Neurosci. 2006;26(18):4930-4939.
46. Zhang S, Wu M, Peng C, Zhao G, Gu R. GFAP expression in injured astrocytes in rats. Exp Ther Med. 2017;14(3):1905-1908.
47. Etzerodt A, Moestrup SK. CD163 and inflammation: biological, diagnostic, and therapeutic aspects. Antioxid Redox Signal. 2013;18(17):2352-2363.
48. Akerfeldt T, Helmersson-Karlqvist J, Gordh T, Larsson A. Circulating human fractalkine is decreased post-operatively after orthopedic and coronary bypass surgery. In Vivo. 2014;28(2):185-188.
49. Xu B, Qian Y, Zhao Y, Fang Z, Tang K, Zhou N, Li D, Wang J. Prognostic value of fractalkine/CX3CL1 concentration in patients with acute myocardial infarction treated with primary percutaneous coronary intervention. Cytokine. 2019;113:365-370.
50. Jungwirth B, Zieglgansberger W, Kochs E, Rammes G. Anesthesia and postoperative cognitive dysfunction (POCD). Mini Rev Med Chem. 2009;9(14):1568-1579.
51. Tan AMY, Amoako D. Postoperative cognitive dysfunction after cardiac surgery. Continuing Education in Anaesthesia Critical Care & Pain. 2013;13(6):218-223.
52. van Harten AE, Scheeren TW, Absalom AR. A review of postoperative cognitive dysfunction and neuroinflammation associated with cardiac surgery and anaesthesia. Anaesthesia. 2012;67(3):280-293.
53. Rudolph JL, Schreiber KA, Culley DJ, McGlinchey RE, Crosby G, Levitsky S, Marcantonio ER. Measurement of post-operative cognitive dysfunction after cardiac surgery: a systematic review. Acta Anaesthesiol Scand. 2010;54(6):663-677.

There are 53 citations in total.

Details

Primary Language	English
Subjects	Psychiatry
Journal Section	Research Article
Authors	Arif Ozbay 0000-0002-1075-9999 Sureyya Barun 0000-0003-3726-8177 Aybeniz Civan Kahve 0000-0002-0683-5207 Abdullah Özer 0000-0003-0925-7323 Özlem Gülbahar 0000-0003-0450-4305 Hasan Dağlı 0000-0003-2756-6277 Seçil Özkan 0000-0003-1572-8777 Dilek Erer 0000-0003-1926-720X
Publication Date	October 1, 2022
Submission Date	June 1, 2022
Published in Issue	Year 2022

Cite

EndNote	Ozbay A, Barun S, Civan Kahve A, Özer A, Gülbahar Ö, Dağlı H, Özkan S, Erer D (October 1, 2022) Role of soluble fractalkine, GFAP and CD163 in cognitive functions after open heart surgery in diabetic and non-diabetic patients. Acıbadem Üniversitesi Sağlık Bilimleri Dergisi 13 4 565–573.

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