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Determination of Early Diagnostic Biomarkers of Renal Dysfunction After Cardiopulmonary Bypass: miR-21 and miR10a Mediated Postoperative Inflammation

Year 2024, Volume: 14 Issue: 1, 245 - 252, 28.03.2024
https://doi.org/10.33808/clinexphealthsci.1222499

Abstract

Objective: Acute renal failure (ARF) prevalence is high among patients who undergo cardiopulmonary bypass (CPB), and this condition can only be diagnosed via serum creatinine level (sCr) conventionally within 48 hours. Therefore, we need early novel diagnosis biomarkers to start preventive treatment of ARF. For that reason, we aimed to analyze if plasma miR-21 derived from heart, correlates with kidney- enriched miR-10a during inflammatory IL-6, IL-1β, and TNF-α response in terms of acute renal failure 30 minutes after CPB.
Methods: Patients (n=46, Female:8 and Male:38), aged 61.08±9.41, who underwent CPB surgery were included. Blood samples were collected during the pre – and post-CPB (30 minutes after CPB). Demographic data of all cases were collected. Quantification of expression levels of miR-21 and miR-10a was done via quantitative PCR (qPCR). Determination of plasma concentration of relevant cytokines, IL-6, IL-1β, and TNF-α was done via ELISA.
Results: The circulating level of miR-21 during post-CPB period (-11.78±6.98) was significantly higher (p≤0.05) than pre-CPB period (-6.55±7.11), but there was no significant change (p>0.05) in the circulating level of miR-10a between pre – (-12.22±3.55) and post-CPB (-11.60±3.36) periods. When we compared the mean ΔΔCt values of miR-21 and miR-10a, downregulation was observed in the expression level of miR-10a (0.62±3.77) whilst the expression level of miR-21 (-5.22±7.25) was upregulated (p≤0.05). The levels of plasma concentration of IL-6 (2.74±2.50 ng/l) and TNF-α (83.63±9.33 ng/l) were increased during post-CPB period (both were ***p<0.0001). Whilst, IL-1β concentration level during pre-CPB period (3.95±0.47 ng/l) was found to be decreased (0.38±2.04 ng/l and *p<0.05) according to post-CPB.
Conclusion: Prospectively, these data suggests that high miR-21 levels is a promising indicator and can be a candidate as an early novel biomarker for diagnosis of acute renal failure 30 minutes after CPB.

References

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  • Khreba NA, Abdelsalam M, Wahab AM, Sanad M, Elhelaly R, Adel M, El-Kannishy G. Kidney Injury Molecule 1 (KIM-1) as an early predictor for acute kidney injury in post-cardiopulmonary bypass (cpb) in open heart surgery patients. International Journal of Nephrology 2019;2019:6265307. DOI: 10.1155/2019/6265307
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  • Aghabozorgi AS, Ahangari N, Eftekhaari TE, Torbati PN, Bahiraee A, Ebrahimi R, Pasdar A. Circulating exosomal miRNAs in cardiovascular disease pathogenesis: New emerging hopes. Journal of Cellular Physiology 2019; 234(12):21796-21809. DOI: 10.1002/jcp.28942
  • Li YF, Jing Y, Hao J, Frankfort NC, Zhou X, Shen B, Liu X, Wang L, Li R. MicroRNA-21 in the pathogenesis of acute kidney injury. Protein & Cell 2013;4(11):813-819. DOI:10.1007/s13238-013-3085-y
  • Lin Q, Geng Y, Zhao M, Lin S, Zhu Q, Tian Z. MiR-21 Regulates TNF-alpha-Induced CD40 expression via the sirt1-nf-kappab pathway in renal inner medullary collecting duct cells. Cellular Physiology and Biochemistry 2017;41(1):124-136. DOI: 10.1159/000455981
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  • Pesonen E, Passov A, Andersson S, Suojaranta R, Niemi T, Raivio P, Salmenpera M, Schramko A. Glycocalyx degradation and inflammation in cardiac surgery. Journal of Cardiothoracic and Vascular Anesthesia 2019;33(2):341-345. DOI: 10.1053/j.jvca.2018.04.007
  • Altan-Bonnet G, Mukherjee R. Cytokine-mediated communication: A quantitative appraisal of immune complexity. Nature Reviews Immunology 2019;19:205-217. DOI: 10.1038/s41577-019-0131-x
  • Hu SL, Chang AC, Huang CC, Tsai CH, Lin CC, Tang CH. Myostatin Promotes interleukin-1beta expression in rheumatoid arthritis synovial fibroblasts through inhibition of miR-21-5p. Frontiers in Immunology 2017;8:1747. DOI: 10.3389/fimmu.2017.01747
  • Ding H, Li J, Li Y, Yang M, Nie S, Zhou M, Zhou Z, Yang X, Liu Y, Hou FF. MicroRNA-10 negatively regulates inflammation in diabetic kidney via targeting activation of the NLRP3 inflammasome. Molecular Therapy 2021;29(7):2308-2320. DOI: 10.1016/j.ymthe.2021.03.012
  • Zheng G, Qiu G, Ge M, Meng J, Zhang G, Wang J, Huang R, Shu Q, Xu J. miR-10a in Peripheral blood mononuclear cells is a biomarker for sepsis and has anti-inflammatory function. Mediators of Inflammation 2020;2020:4370983. DOI: 10.1155/2020/4370983
  • Yang L, Sun HF, Guo LQ, Cao HB. MiR-10a-5p: A promising biomarker for early diagnosis and prognosis evaluation of bladder cancer. Cancer Management and Research 2021;13:7841-7850. DOI: 10.2147/CMAR.S326732
  • Wang J, Liu Y, Li Y, Zheng X, Gan J, Wan Z, Zhang J, Liu Y, Wang Y, Hu W, Li Y, Liu Y. Exosomal‑miR‑10a derived from colorectal cancer cells suppresses migration of human lung fibroblasts, and expression of IL‑6, IL‑8 and IL‑1β. Molecular Medicine Reports 2021;23(1):84. DOI: 10.3892/mmr.2020.11723
  • Azzawi M, Hasleton P. Tumour necrosis factor alpha and the cardiovascular system: its role in cardiac allograft rejection and heart disease. Cardiovascular Research 1999;43(4):850-859. DOI: 10.1016/S0008-6363(99)00138-8
  • Huang RL, Yuan Y, Tu J, Zou GM, Li Q. Opposing TNF-alpha/IL-1beta- and BMP-2-activated MAPK signaling pathways converge on Runx2 to regulate BMP-2-induced osteoblastic differentiation. Cell Death&Disease 2014;5(4):e1187. DOI: 10.1038/cddis.2014.101
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  • Nandate K, Vuylsteke A, Crosbie AE, Messahel S, Oduro-Dominah A, Menon DK. Cerebrovascular cytokine responses during coronary artery bypass surgery: Specific production of interleukin-8 and its attenuation by hypothermic cardiopulmonary bypass. Anesthesia&Analgesia 1999; 89(4):823. DOI: 10.1213/00000539-199910000-00003
  • Naruka V, Salmasi MY, Arjomandi Rad A, Marczin N, Lazopoulos G, Moscarelli M, Casula R, Athanasiou T. Use of cytokine filters during cardiopulmonary bypass: systematic review and meta-analysis. Heart, Lung and Circulation 2022;31(11):1493-1503. DOI: 10.1016/j.hlc.2022.07.015
  • Shi J. Considering Exosomal mir-21 as a biomarker for cancer. Journal of Clinical Medicine 2016; 5(4):42. DOI: 10.3390/jcm5040042
  • Sheedy FJ. Turning 21: Induction of miR-21 as a key switch in the inflammatory response. Frontiers in Immunology 2015;6:19. DOI: 0.3389/fimmu.2015.00019
  • Xu X, Kriegel AJ, Liu Y, Usa K, Mladinov D, Liu H, Fang Y, Ding X, Liang M. Delayed ischemic preconditioning contributes to renal protection by upregulation of miR-21. Kidney International 2012;82(11):1167-1175. DOI: 10.1038/ki.2012.241
  • Zhou TB, Jiang ZP. Role of miR-21 and its signaling pathways in renal diseases. Journal of Receptors and Signal Transduction 2014;34(5):335-337. DOI: 10.3109/10799893.2014.896382
  • Lange T, Artelt N, Kindt F, Stracke S, Rettig R, Lendeckel U, Chadjichristos CE, Kavvadas P, Chatziantoniou C, Endlich K, Endlich N. MiR-21 is up-regulated in urinary exosomes of chronic kidney disease patients and after glomerular injury. Journal of Cellular and Molecular Medicine 2019;23(7):4839-4843. DOI: 10.1111/jcmm.14317
  • Ronco C, Haapio M, House AA, Anavekar N, Bellomo R. Cardiorenal syndrome. Journal of The American College of Cardiology 2008;52(19):1527-1539. DOI: 10.1016/j.jacc.2008.07.051
  • Huang CK, Bar C, Thum T. miR-21, Mediator, and Potential Therapeutic Target in the Cardiorenal Syndrome. Frontiers in Pharmacology 2020;11:726. DOI: 10.3389/fphar.2020.00726
  • Glowacki F, Savary G, Gnemmi V, Buob D, Van der Hauwaert C, Lo-Guidice JM, Bouye S, Hazzan M, Pottier N, Perrais M, Aubert S, Cauffiez C. Increased circulating miR-21 levels are associated with kidney fibrosis. PLoS One 2013;8(2):e58014. DOI: 10.1371/journal.pone.0058014
Year 2024, Volume: 14 Issue: 1, 245 - 252, 28.03.2024
https://doi.org/10.33808/clinexphealthsci.1222499

Abstract

References

  • Gill N, Nally Jr JV, Fatica RA. Renal failure secondary to acute tubular necrosis: Epidemiology, diagnosis, and management. Chest 2005;128(4):2847-2863. DOI: 10.1378/chest.128.4.2847
  • Ristikankare A, Kuitunen T, Kuitunen A, Uotila L, Vento A, Suojaranta-Ylinen R, Salmenpera M, Poyhia R. Lack of renoprotective effect of i.v. N-acetylcysteine in patients with chronic renal failure undergoing cardiac surgery. British Journal of Anaesthesia 2006;97(5):611-616. DOI: 10.1093/bja/ael224
  • Ma Y, Cai F, Li Y, Chen J, Han F, Lin W. A review of the application of nanoparticles in the diagnosis and treatment of chronic kidney disease. Bioactive Materials 2020;5(3):732-743. DOI: 10.1016/j.bioactmat.2020.05.002
  • Khreba NA, Abdelsalam M, Wahab AM, Sanad M, Elhelaly R, Adel M, El-Kannishy G. Kidney Injury Molecule 1 (KIM-1) as an early predictor for acute kidney injury in post-cardiopulmonary bypass (cpb) in open heart surgery patients. International Journal of Nephrology 2019;2019:6265307. DOI: 10.1155/2019/6265307
  • Oh DJ. A long journey for acute kidney injury biomarkers. Renal Failure 2020;42(1):154-165. DOI: 10.1080/0886022X.2020.1721300
  • Legrand M, Bell S, Forni L, Joannidis M, Koyner JL, Liu K, Cantaluppi V. Pathophysiology of COVID-19-associated acute kidney injury. Nature Reviews Nephrology 2021;17:751-764. DOI: 10.1038/s41581-021-00452-0
  • Ekdahl KN, Fromell K, Mannes M, Grinnemo KH, Huber-Lang M, Teramura Y, Nilsson B. Therapeutic regulation of complement activation in extracorporeal circuits and intravascular treatments with special reference to the alternative pathway amplification loop. Immunological Reviews 2022;313(1):91-103. DOI: 10.1111/imr.13148
  • Presta P, Bolignano D, Coppolino G, Serraino F, Mastroroberto P, Andreucci M, Fuiano G. Antecedent ACE-inhibition, inflammatory response, and cardiac surgery associated acute kidney injury. Reviews in Cardiovascular Medicine 2021;22(1):207-213. DOI: 10.31083/j.rcm.2021.01.288
  • Xu X, Kriegel AJ, Jiao X, Liu H, Bai X, Olson J, Liang M, Ding X. miR-21 in ischemia/reperfusion injury: A double-edged sword? Physiological Genomics 2014;46(21)789-797. DOI:10.1152/physiolgenomics.00020.2014
  • Larrue R, Fellah S, Van der Hauwaert C, Hennino MF, Perrais M, Lionet A, Glowacki F, Pottier N, Cauffiez C. The versatile role of mir-21 in renal homeostasis and diseases. Cells 2022;11(21):3525. DOI: 10.3390/cells11213525
  • Mu N, Gu J, Huang T, Zhang C, Shu Z, Li M, Hao Q, Li W, Zhang W, Zhao J, Zhang Y, Huang L, Wang S, Jin X, Xue X, Zhang W, Zhang Y. A novel NF-kappaB/YY1/microRNA-10a regulatory circuit in fibroblast-like synoviocytes regulates inflammation in rheumatoid arthritis. Scientific Reports 2016;6:20059. DOI: 10.1038/srep20059
  • Tahamtan A, Teymoori-Rad M, Nakstad B, Salimi V. Anti-inflammatory micrornas and their potential for inflammatory diseases treatment. Frontiers in Immunology 2018;9:1377. DOI: 10.3389/fimmu.2018.01377
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Metods 2001;25(4): 402-408. DOI: 10.1006/meth.2001.1262
  • Axtell AL, Fiedler AG, Melnitchouk S, D'Alessandro DA, Villavicencio MA, Jassar AS, Sundt TM, 3rd. Correlation of cardiopulmonary bypass duration with acute renal failure after cardiac surgery. The Journal of Thoracic and Cardiovascular Surgery 2020;159(1):170-178. DOI: 10.1016/j.jtcvs.2019.01.072
  • Engelman DT, Crisafi C, Germain M, Greco B, Nathanson BH, Engelman RM, Schwann TA. Using urinary biomarkers to reduce acute kidney injury following cardiac surgery. The Journal of Thoracic and Cardiovascular Surgery 2020;160(5):1235-1246. DOI: 10.1016/j.jtcvs.2019.10.034
  • Ostermann M, Zarbock A, Goldstein S, Kashani K, Macedo E, Murugan R, Bell M, Forni L, Guzzi L, Joannidis M, Kane-Gill SL, Legrand M, Mehta R, Murray PT, Pickkers P, Plebani M, Prowle J, Ricci Z, Rimmele T, Rosner M, Shaw AD, Kellum JA, Ronco C. Recommendations on acute kidney injury biomarkers from the acute disease quality initiative consensus conference: a consensus statement. JAMA Netw Open 2020;3(10):e2019209. DOI: 10.1001/jamanetworkopen.2020.19209
  • Poon KS, Palanisamy K, Chang SS, Sun KT, Chen KB, Li PC, Lin TC, Li CY. Plasma exosomal miR-223 expression regulates inflammatory responses during cardiac surgery with cardiopulmonary bypass. Sci Rep 2017;7(1):10807. DOI: 10.1038/s41598-017-09709-w
  • Aghabozorgi AS, Ahangari N, Eftekhaari TE, Torbati PN, Bahiraee A, Ebrahimi R, Pasdar A. Circulating exosomal miRNAs in cardiovascular disease pathogenesis: New emerging hopes. Journal of Cellular Physiology 2019; 234(12):21796-21809. DOI: 10.1002/jcp.28942
  • Li YF, Jing Y, Hao J, Frankfort NC, Zhou X, Shen B, Liu X, Wang L, Li R. MicroRNA-21 in the pathogenesis of acute kidney injury. Protein & Cell 2013;4(11):813-819. DOI:10.1007/s13238-013-3085-y
  • Lin Q, Geng Y, Zhao M, Lin S, Zhu Q, Tian Z. MiR-21 Regulates TNF-alpha-Induced CD40 expression via the sirt1-nf-kappab pathway in renal inner medullary collecting duct cells. Cellular Physiology and Biochemistry 2017;41(1):124-136. DOI: 10.1159/000455981
  • Giacinto O, Satriano U, Nenna A, Spadaccio C, Lusini M, Mastroianni C, Nappi F, Chello M. Inflammatory response and endothelial dysfunction following cardiopulmonary bypass: pathophysiology and pharmacological targets. Recent Patents on Inflammation&Allergy Drug Discovery 2019;13(2):158-173. DOI: 10.2174/1872213X13666190724112644
  • Pesonen E, Passov A, Andersson S, Suojaranta R, Niemi T, Raivio P, Salmenpera M, Schramko A. Glycocalyx degradation and inflammation in cardiac surgery. Journal of Cardiothoracic and Vascular Anesthesia 2019;33(2):341-345. DOI: 10.1053/j.jvca.2018.04.007
  • Altan-Bonnet G, Mukherjee R. Cytokine-mediated communication: A quantitative appraisal of immune complexity. Nature Reviews Immunology 2019;19:205-217. DOI: 10.1038/s41577-019-0131-x
  • Hu SL, Chang AC, Huang CC, Tsai CH, Lin CC, Tang CH. Myostatin Promotes interleukin-1beta expression in rheumatoid arthritis synovial fibroblasts through inhibition of miR-21-5p. Frontiers in Immunology 2017;8:1747. DOI: 10.3389/fimmu.2017.01747
  • Ding H, Li J, Li Y, Yang M, Nie S, Zhou M, Zhou Z, Yang X, Liu Y, Hou FF. MicroRNA-10 negatively regulates inflammation in diabetic kidney via targeting activation of the NLRP3 inflammasome. Molecular Therapy 2021;29(7):2308-2320. DOI: 10.1016/j.ymthe.2021.03.012
  • Zheng G, Qiu G, Ge M, Meng J, Zhang G, Wang J, Huang R, Shu Q, Xu J. miR-10a in Peripheral blood mononuclear cells is a biomarker for sepsis and has anti-inflammatory function. Mediators of Inflammation 2020;2020:4370983. DOI: 10.1155/2020/4370983
  • Yang L, Sun HF, Guo LQ, Cao HB. MiR-10a-5p: A promising biomarker for early diagnosis and prognosis evaluation of bladder cancer. Cancer Management and Research 2021;13:7841-7850. DOI: 10.2147/CMAR.S326732
  • Wang J, Liu Y, Li Y, Zheng X, Gan J, Wan Z, Zhang J, Liu Y, Wang Y, Hu W, Li Y, Liu Y. Exosomal‑miR‑10a derived from colorectal cancer cells suppresses migration of human lung fibroblasts, and expression of IL‑6, IL‑8 and IL‑1β. Molecular Medicine Reports 2021;23(1):84. DOI: 10.3892/mmr.2020.11723
  • Azzawi M, Hasleton P. Tumour necrosis factor alpha and the cardiovascular system: its role in cardiac allograft rejection and heart disease. Cardiovascular Research 1999;43(4):850-859. DOI: 10.1016/S0008-6363(99)00138-8
  • Huang RL, Yuan Y, Tu J, Zou GM, Li Q. Opposing TNF-alpha/IL-1beta- and BMP-2-activated MAPK signaling pathways converge on Runx2 to regulate BMP-2-induced osteoblastic differentiation. Cell Death&Disease 2014;5(4):e1187. DOI: 10.1038/cddis.2014.101
  • Allan CK, Newburger JW, McGrath E, Elder J, Psoinos C, Laussen PC, del Nido PJ, Wypij D, McGowan FX. The relationship between inflammatory activation and clinical outcome after infant cardiopulmonary bypass. Anesthesia&Analgesia 2010;111(5):1244-1251. DOI: 10.1213/ANE.0b013e3181f333aa
  • Nandate K, Vuylsteke A, Crosbie AE, Messahel S, Oduro-Dominah A, Menon DK. Cerebrovascular cytokine responses during coronary artery bypass surgery: Specific production of interleukin-8 and its attenuation by hypothermic cardiopulmonary bypass. Anesthesia&Analgesia 1999; 89(4):823. DOI: 10.1213/00000539-199910000-00003
  • Naruka V, Salmasi MY, Arjomandi Rad A, Marczin N, Lazopoulos G, Moscarelli M, Casula R, Athanasiou T. Use of cytokine filters during cardiopulmonary bypass: systematic review and meta-analysis. Heart, Lung and Circulation 2022;31(11):1493-1503. DOI: 10.1016/j.hlc.2022.07.015
  • Shi J. Considering Exosomal mir-21 as a biomarker for cancer. Journal of Clinical Medicine 2016; 5(4):42. DOI: 10.3390/jcm5040042
  • Sheedy FJ. Turning 21: Induction of miR-21 as a key switch in the inflammatory response. Frontiers in Immunology 2015;6:19. DOI: 0.3389/fimmu.2015.00019
  • Xu X, Kriegel AJ, Liu Y, Usa K, Mladinov D, Liu H, Fang Y, Ding X, Liang M. Delayed ischemic preconditioning contributes to renal protection by upregulation of miR-21. Kidney International 2012;82(11):1167-1175. DOI: 10.1038/ki.2012.241
  • Zhou TB, Jiang ZP. Role of miR-21 and its signaling pathways in renal diseases. Journal of Receptors and Signal Transduction 2014;34(5):335-337. DOI: 10.3109/10799893.2014.896382
  • Lange T, Artelt N, Kindt F, Stracke S, Rettig R, Lendeckel U, Chadjichristos CE, Kavvadas P, Chatziantoniou C, Endlich K, Endlich N. MiR-21 is up-regulated in urinary exosomes of chronic kidney disease patients and after glomerular injury. Journal of Cellular and Molecular Medicine 2019;23(7):4839-4843. DOI: 10.1111/jcmm.14317
  • Ronco C, Haapio M, House AA, Anavekar N, Bellomo R. Cardiorenal syndrome. Journal of The American College of Cardiology 2008;52(19):1527-1539. DOI: 10.1016/j.jacc.2008.07.051
  • Huang CK, Bar C, Thum T. miR-21, Mediator, and Potential Therapeutic Target in the Cardiorenal Syndrome. Frontiers in Pharmacology 2020;11:726. DOI: 10.3389/fphar.2020.00726
  • Glowacki F, Savary G, Gnemmi V, Buob D, Van der Hauwaert C, Lo-Guidice JM, Bouye S, Hazzan M, Pottier N, Perrais M, Aubert S, Cauffiez C. Increased circulating miR-21 levels are associated with kidney fibrosis. PLoS One 2013;8(2):e58014. DOI: 10.1371/journal.pone.0058014
There are 41 citations in total.

Details

Primary Language English
Subjects Pharmaceutical Biochemistry
Journal Section Articles
Authors

Fatma Zehra Çağıl 0000-0002-8669-0449

Koray Ak 0000-0002-8608-5951

Ab. Matteen Rafiqi This is me 0000-0002-5682-1727

Ayten Saraçoğlu 0000-0002-1186-0933

Gamze Nur Öter 0000-0002-7063-3984

Şermin Tetik 0000-0001-7157-9142

Early Pub Date March 23, 2024
Publication Date March 28, 2024
Submission Date December 22, 2022
Published in Issue Year 2024 Volume: 14 Issue: 1

Cite

APA Çağıl, F. Z., Ak, K., Rafiqi, A. M., Saraçoğlu, A., et al. (2024). Determination of Early Diagnostic Biomarkers of Renal Dysfunction After Cardiopulmonary Bypass: miR-21 and miR10a Mediated Postoperative Inflammation. Clinical and Experimental Health Sciences, 14(1), 245-252. https://doi.org/10.33808/clinexphealthsci.1222499
AMA Çağıl FZ, Ak K, Rafiqi AM, Saraçoğlu A, Öter GN, Tetik Ş. Determination of Early Diagnostic Biomarkers of Renal Dysfunction After Cardiopulmonary Bypass: miR-21 and miR10a Mediated Postoperative Inflammation. Clinical and Experimental Health Sciences. March 2024;14(1):245-252. doi:10.33808/clinexphealthsci.1222499
Chicago Çağıl, Fatma Zehra, Koray Ak, Ab. Matteen Rafiqi, Ayten Saraçoğlu, Gamze Nur Öter, and Şermin Tetik. “Determination of Early Diagnostic Biomarkers of Renal Dysfunction After Cardiopulmonary Bypass: MiR-21 and miR10a Mediated Postoperative Inflammation”. Clinical and Experimental Health Sciences 14, no. 1 (March 2024): 245-52. https://doi.org/10.33808/clinexphealthsci.1222499.
EndNote Çağıl FZ, Ak K, Rafiqi AM, Saraçoğlu A, Öter GN, Tetik Ş (March 1, 2024) Determination of Early Diagnostic Biomarkers of Renal Dysfunction After Cardiopulmonary Bypass: miR-21 and miR10a Mediated Postoperative Inflammation. Clinical and Experimental Health Sciences 14 1 245–252.
IEEE F. Z. Çağıl, K. Ak, A. M. Rafiqi, A. Saraçoğlu, G. N. Öter, and Ş. Tetik, “Determination of Early Diagnostic Biomarkers of Renal Dysfunction After Cardiopulmonary Bypass: miR-21 and miR10a Mediated Postoperative Inflammation”, Clinical and Experimental Health Sciences, vol. 14, no. 1, pp. 245–252, 2024, doi: 10.33808/clinexphealthsci.1222499.
ISNAD Çağıl, Fatma Zehra et al. “Determination of Early Diagnostic Biomarkers of Renal Dysfunction After Cardiopulmonary Bypass: MiR-21 and miR10a Mediated Postoperative Inflammation”. Clinical and Experimental Health Sciences 14/1 (March 2024), 245-252. https://doi.org/10.33808/clinexphealthsci.1222499.
JAMA Çağıl FZ, Ak K, Rafiqi AM, Saraçoğlu A, Öter GN, Tetik Ş. Determination of Early Diagnostic Biomarkers of Renal Dysfunction After Cardiopulmonary Bypass: miR-21 and miR10a Mediated Postoperative Inflammation. Clinical and Experimental Health Sciences. 2024;14:245–252.
MLA Çağıl, Fatma Zehra et al. “Determination of Early Diagnostic Biomarkers of Renal Dysfunction After Cardiopulmonary Bypass: MiR-21 and miR10a Mediated Postoperative Inflammation”. Clinical and Experimental Health Sciences, vol. 14, no. 1, 2024, pp. 245-52, doi:10.33808/clinexphealthsci.1222499.
Vancouver Çağıl FZ, Ak K, Rafiqi AM, Saraçoğlu A, Öter GN, Tetik Ş. Determination of Early Diagnostic Biomarkers of Renal Dysfunction After Cardiopulmonary Bypass: miR-21 and miR10a Mediated Postoperative Inflammation. Clinical and Experimental Health Sciences. 2024;14(1):245-52.

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