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The Importance of Erythrocyte Deformability in the Physiopathology of Diseases

Year 2023, Issue: 21 - December, 1262 - 1272, 05.01.2024
https://doi.org/10.38079/igusabder.1313165

Abstract

Erythrocytes are cells involved in the exchange of oxygen and carbon dioxide between the tissues and the lungs. They also play a role in protecting the organism against infection, increasing immune adhesion, and strengthening phagocytosis. For erythrocytes to perform these functions, the hemodynamic properties of the blood must be preserved. Deformability ability, one of its most important features, contributes to minimizing resistance to blood flow and adapting the cell shape to variable flow conditions. The deformability ability of erythrocytes prevents cell lysis while maintaining a constant membrane surface area. As a result of the decrease in the deformability of erythrocytes, it clogs the capillaries, obstructing blood flow and reducing tissue oxygenation. There are many factors affecting erythrocyte deformability. It is possible that erythrocyte rigidity changes reversibly with physiological regulation of some effects. While a reversible physiological mechanism is provided in erythrocyte rigidity during exercise, pathological conditions are more likely to cause eryptosis (programmed cell death) in erythrocytes. Various physicochemical properties of the environment determine the ability of erythrocyte deformability and eryptosis formation. It has been suggested that various elements, molecules, and some hormone levels in the bloodstream may affect erythrocyte deformability and eryptosis formation. In addition, the dynamic properties of the erythrocyte membrane are also affected by the content of the cytoplasm. When we examine the literature, many studies show that the deformability ability of erythrocytes is reduced in the physiopathology of various diseases. In this review, we aim to explain the importance of erythrocyte deformability in the physiopathology of diseases.

Project Number

YOK

References

  • 1. Ho TL, Hoang NT, Lee J, Park JH, Kim BK. Determining mean corpuscular volume and red blood cell count using electrochemical collision events. Biosens. Bioelectron. 2018;110:155-159.
  • 2. Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AJ. ATP: the red blood cell link to NO and local control of the pulmonary circulation. Am. J. Physiol. Heart Circ. Physiol. 1996;271(6):H2717-H2722.
  • 3. Fadhel MA, Humaidi AJ, Oleiwi SR. Image processing-based diagnosis of sickle cell anemia in erythrocytes. Annual conference on new trends in information & communications technology applications (NTICT). 2017:203-7
  • 4. Lopes de Almeida JP, Oliveira S, Saldanha C. Erythrocyte as a biological sensor. Clin. Hemorheol. Microcirc. 2012;51(1):1-20.
  • 5. Barshtein G, Arbell D, Yedgar S. Hemodynamic functionality of transfused red blood cells in the microcirculation of blood recipients. Front. Physiol. 2018;9:41.
  • 6. Narla J, Mohandas N. Red cell membrane disorders. Int. J. Lab. Hematol. 2017;39:47-52.
  • 7. Mukherjee R, Chaudhury K, Chakraborty C. Topological features of erythrocytes in thalassemic patients: quantitative characterization by scanning electron and atomic force microscopy. Anal. Quant. Cytol. Histol. 2014;36(2):91-99.
  • 8. Betz T, Bakowsky U, Müller MR, Lehr CM, Bernhardt I. Conformational change of membrane proteins leads to shape changes of red blood cells. Bioelectrochemistry. 2007;70(1):122-126.
  • 9. Diez-Silva M, Dao M, Han J, Lim CT, Suresh S. Shape and biomechanical characteristics of human red blood cells in health and disease. MRS Bull. 2010;35(5):382-388.
  • 10. Mohandas N, Evans E. Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects. Annu. Rev. Bioph. Biom. 1994;23(1):787-818.
  • 11. Matot I, Katz M, Pappo O, et al. Resuscitation with aged blood exacerbates liver injury in a hemorrhagic rat model. Crit. Care Med. 2013;41(3):842-849.
  • 12. Brun JF, Varlet-Marie E, Myzia J, Raynaud de Mauverger E, Pretorius E. Metabolic influences modulating erythrocyte deformability and eryptosis. Metabolites. 2022;12(1):4.
  • 13. Sugie J, Intaglietta M, Sung LA. Water transport and homeostasis as a major function of erythrocytes. Am. J. Physiol. Heart Circ. Physiol. 2018;314(5):H1098-H1107.
  • 14. Broadway-Duren JB, Klaassen H. Anemias. Crit. Care Nurs. Clin. 2013;25(4):411-426.
  • 15. Alaarg A, Schiffelers RM, van Solinge WW, Van Wijk R. Red blood cell vesiculation in hereditary hemolytic anemia. Front. Physiol. 2013;4:365.
  • 16. Salomao M, Zhang X, Yang Y, et al. Protein 4.1 R-dependent multiprotein complex: new insights into the structural organization of the red blood cell membrane. PNAS. 2008;105(23):8026-8031.
  • 17. Siddon AJ, Tormey CA. The chemical and laboratory investigation of hemolysis. Adv. Clin. Chem. 2019;89:215-258.
  • 18. Varo R, Chaccour C, Bassat Q. Update on malaria. Med. Clin. (English Edition). 2020;155(9):395-402.
  • 19. Farrar J, Hotez P, Junghanss T, Kang G, Lalloo D, White NJ. Manson's Tropical Diseases E-Book. Elsevier health sciences; 2013.
  • 20. Jakeman G, Saul A, Hogarth W, Collins W. Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology. 1999;119(2):127-133.
  • 21. Matthews K, Duffy SP, Myrand-Lapierre ME, et al. Microfluidic analysis of red blood cell deformability as a means to assess hemin-induced oxidative stress resulting from Plasmodium falciparum intraerythrocytic parasitism. Integr. Biol. 2017;9(6):519-528.
  • 22. White NJ. Anaemia and malaria. Malar. J. 2018;17(1):1-17.
  • 23. Deng X, Duffy SP, Myrand-Lapierre ME, et al. Reduced deformability of parasitized red blood cells as a biomarker for anti-malarial drug efficacy. Malar. J. 2015;14:1-9.
  • 24. Dugar S, Choudhary C, Duggal A. Sepsis and septic shock: Guideline-based management. Cleve Clin J Med. 2020;87(1):53-64.
  • 25. Minasyan H. Sepsis: mechanisms of bacterial injury to the patient. Scand. J. Trauma, Resusc. Emerg. Med. 2019;27(1):1-22.
  • 26. Chan YL, Han ST, Li CH, Wu CC, Chen KF. Transfusion of red blood cells to patients with sepsis. Int. J. Mol. Sci. 2017;18(9):1946.
  • 27. Vincent JL, De Backer D. Oxygen transport—the oxygen delivery controversy. Intensive Care Med. 2004;30:1990-1996.
  • 28. Moutzouri AG, Skoutelis AT, Gogos CA, Missirlis YF, Athanassiou GM. Red blood cell deformability in patients with sepsis: a marker for prognosis and monitoring of severity. Clin. Hemorheol. Microcirc. 2007;36(4):291-299.
  • 29. Luepker RV, Lakshminarayan K. Cardiovascular and cerebrovascular diseases. Oxford Textbook of Public Health, Volume 3: the practice of public health. 2009;(Ed. 5):971-996.
  • 30. Li N, Zhou H, Tang Q. Red blood cell distribution width: a novel predictive indicator for cardiovascular and cerebrovascular diseases. Dis. Markers. 2017;2017:7089493.
  • 31. Strömberg S, Nordanstig A, Bentzel T, Österberg K, Bergström G. Risk of early recurrent stroke in symptomatic carotid stenosis. Eur. J. Vasc. Endovasc. Surg. 2015;49(2):137-144.
  • 32. Kara H, Degirmenci S, Bayir A, et al. Red cell distribution width and neurological scoring systems in acute stroke patients. Neuropsychiatr. Dis. Treat. 2015;733-739.
  • 33. Boisseau M, Freyburger G, Lorient-Roudaut M. Changes in blood filterability in cerebrovascular accidents. Wien. Med. Wochenschr. 1986;136:44-46.
  • 34. Groen K, Maltby VE, Sanders KA, Scott RJ, Tajouri L, Lechner-Scott J. Erythrocytes in multiple sclerosis–forgotten contributors to the pathophysiology? Mult. Scler. J. Exp. Transl. Clin. 2016;2:2055217316649981.
  • 35. Ljubisavljevic S, Stojanovic I, Cvetkovic T, et al. Erythrocytes' antioxidative capacity as a potential marker of oxidative stress intensity in neuroinflammation. Neurol. Sci. 2014;337(1-2):8-13.
  • 36. Simpson LO, Shand BI, Olds RJ, Larking PW, Arnott MJ. Red cell and hemorheological changes in multiple sclerosis. Pathology. 1987;19(1):51-55.
  • 37. Wang Y, Yang P, Yan Z, et al. The relationship between erythrocytes and diabetes mellitus. J. Diabetes Res. 2021;2021.
  • 38. Lee S, Lee MY, Nam JS, et al. Hemorheological approach for early detection of chronic kidney disease and diabetic nephropathy in type 2 diabetes. Diabetes Technol. Ther. 2015;17(11):808-815.
  • 39. Babu N, Singh M. Influence of hyperglycemia on aggregation, deformability and shape parameters of erythrocytes. Clin. Hemorheol. Microcirc. 2004;31(4):273-280.
  • 40. Levi E, Başkurt O, Kahdemir N, Aidaç S, Kutman M, Üçer O. Changes in erythrocyte deformability during experimental hyperthyroidism. Clin. Hemorheol. Microcirc. 1989;9(4):577-581.
  • 41. Davidson R, Cumming A, Leel V, How J, Bewsher P, Khir A. A search for the mechanism underlying the altered MCV in thyroid dysfunction: a study of serum and red cell membrane lipids. Scand. J. Haematol. 1984;32(1):19-24.
  • 42. Sütterlin U, Gless KH, Schaz K, Hüfner M, Schütz V, Hunstein W. Peripheral effects of thyroid hormones: alteration of intracellular Na-concentration, ouabain-sensitive Na-transport, and Na-Li countertransport in human red blood cells. Klin. Wochenschr. 1984;62(12):598-601.
  • 43. Xiao T, Cai Y, Chen B. HIV-1 entry and membrane fusion inhibitors. Viruses. 2021;13(5):735.
  • 44. Geene D, Sudre P, Anwar D, Goehring C, Saaidia A, Hirschel B. Causes of macrocytosis in HIV-infected patients not treated with zidovudine. Swiss HIV Cohort Study. J. Infect. 2000;40(2):160-163.
  • 45. Baskurt OK, Meiselman HJ. Activated polymorphonuclear leukocytes affect red blood cell aggregability. J. Leukoc. Biol. 1998;63(1):89-93.
  • 46. Kim A, Dadgostar H, Holland GN, et al. Hemorheologic abnormalities associated with HIV infection: altered erythrocyte aggregation and deformability. Invest. Ophthalmol. Vis. Sci. 2006;47(9):3927-3932.
  • 47. Prudinnik DS, Sinauridze EI, Shakhidzhanov SS, et al. Filterability of erythrocytes in Patients with COVID-19. Biomolecules. 2022;12(6):782.
  • 48. Renoux C, Fort R, Nader E, et al. Impact of COVID-19 on red blood cell rheology. Br. J. Haematol. 2021;192(4):e108-e111.
  • 49. Baskurt O, Boynard M, Cokelet G, et al. New guidelines for hemorheological laboratory techniques. Clin. Hemorheol. Microcirc. 2009;42(2):75-97.
  • 50. Kubánková M, Hohberger B, Hoffmanns J, et al. Physical phenotype of blood cells is altered in COVID-19. Biophys. J. 2021;120(14):2838-2847.
  • 51. Ulrich H, Pillat MM. CD147 as a target for COVID-19 treatment: suggested effects of azithromycin and stem cell engagement. Stem Cell Rev. Rep. 2020;16(3):434-440.

Hastalıkların Fizyopatolojisinde Eritrosit Deformabilitesinin Önemi

Year 2023, Issue: 21 - December, 1262 - 1272, 05.01.2024
https://doi.org/10.38079/igusabder.1313165

Abstract

Eritrositler, dokular ile akciğerler arasında oksijen ve karbondioksit alışverişinde rol alan hücrelerdir. Organizmayı enfeksiyona karşı korunmasında, immün adezyonun arttırılmasında, fagositozun güçlendirilmesinde de görev alırlar. Eritrositlerin bu görevlerini yerine getirebilmesi için kanın hemodinamik özelliklerinin korunması gerekmektedir. En önemli özelliklerinden biri olan deformabilite yeteneği, kan akımına karşı direnci en aza indirmeye ve hücre şeklini değişken akış koşullarına adapte edebilmeye katkı sağlamaktadır. Eritrositlerin deformabilite yeteneği, sabit bir membran yüzey alanını korurken, hücre parçalanmasını da engellemektedir. Eritrositlerin deformabilite yeteneğinin azalması sonucu kılcal damarları tıkayarak kan akımını engellemekte ve doku oksijenlenmesini azaltmaktadır. Eritrosit deformabilitesini etkileyen çok sayıda faktör bulunmaktadır. Bazı etkilerin fizyolojik regülasyonu ile eritrosit rijiditesinin reversibl olarak değişmesi olasıdır. Egzersiz esnasında eritrosit rijiditesinde reversibl olarak bir fizyolojik mekanizma sağlanıyorken, patolojik koşulların eritrositlerde eriptoza (eritrositlerde programlanmış ölüme) yol açma olasılığı daha yüksektir. Eritrosit deformabilite yeteneğini ve eriptoz oluşumunu ortamın çeşitli fizikokimyasal özellikleri belirlemektedir. Kan dolaşımındaki çeşitli elementlerin, moleküllerin ve bazı hormon düzeylerinin eritrosit deformabilite yeteneği ve eriptoz oluşumunu etkileyebildiği ileri sürülmektedir. Ayrıca eritrosit membranının dinamik özellikleri sitoplazma içeriğinden de etkilenmektedir. Literatürü incelediğimizde, çok sayıda yapılan çalışmada çeşitli hastalıkların fizyopatolojisinde eritrositlerin deformabilite yeteneğinin azaldığı görülmektedir. Bu derlememizde, hastalıkların fizyopatolojisinde eritrosit deformabilite yeteneğinin önemini açıklamayı amaçlanmaktadır.

Project Number

YOK

References

  • 1. Ho TL, Hoang NT, Lee J, Park JH, Kim BK. Determining mean corpuscular volume and red blood cell count using electrochemical collision events. Biosens. Bioelectron. 2018;110:155-159.
  • 2. Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AJ. ATP: the red blood cell link to NO and local control of the pulmonary circulation. Am. J. Physiol. Heart Circ. Physiol. 1996;271(6):H2717-H2722.
  • 3. Fadhel MA, Humaidi AJ, Oleiwi SR. Image processing-based diagnosis of sickle cell anemia in erythrocytes. Annual conference on new trends in information & communications technology applications (NTICT). 2017:203-7
  • 4. Lopes de Almeida JP, Oliveira S, Saldanha C. Erythrocyte as a biological sensor. Clin. Hemorheol. Microcirc. 2012;51(1):1-20.
  • 5. Barshtein G, Arbell D, Yedgar S. Hemodynamic functionality of transfused red blood cells in the microcirculation of blood recipients. Front. Physiol. 2018;9:41.
  • 6. Narla J, Mohandas N. Red cell membrane disorders. Int. J. Lab. Hematol. 2017;39:47-52.
  • 7. Mukherjee R, Chaudhury K, Chakraborty C. Topological features of erythrocytes in thalassemic patients: quantitative characterization by scanning electron and atomic force microscopy. Anal. Quant. Cytol. Histol. 2014;36(2):91-99.
  • 8. Betz T, Bakowsky U, Müller MR, Lehr CM, Bernhardt I. Conformational change of membrane proteins leads to shape changes of red blood cells. Bioelectrochemistry. 2007;70(1):122-126.
  • 9. Diez-Silva M, Dao M, Han J, Lim CT, Suresh S. Shape and biomechanical characteristics of human red blood cells in health and disease. MRS Bull. 2010;35(5):382-388.
  • 10. Mohandas N, Evans E. Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects. Annu. Rev. Bioph. Biom. 1994;23(1):787-818.
  • 11. Matot I, Katz M, Pappo O, et al. Resuscitation with aged blood exacerbates liver injury in a hemorrhagic rat model. Crit. Care Med. 2013;41(3):842-849.
  • 12. Brun JF, Varlet-Marie E, Myzia J, Raynaud de Mauverger E, Pretorius E. Metabolic influences modulating erythrocyte deformability and eryptosis. Metabolites. 2022;12(1):4.
  • 13. Sugie J, Intaglietta M, Sung LA. Water transport and homeostasis as a major function of erythrocytes. Am. J. Physiol. Heart Circ. Physiol. 2018;314(5):H1098-H1107.
  • 14. Broadway-Duren JB, Klaassen H. Anemias. Crit. Care Nurs. Clin. 2013;25(4):411-426.
  • 15. Alaarg A, Schiffelers RM, van Solinge WW, Van Wijk R. Red blood cell vesiculation in hereditary hemolytic anemia. Front. Physiol. 2013;4:365.
  • 16. Salomao M, Zhang X, Yang Y, et al. Protein 4.1 R-dependent multiprotein complex: new insights into the structural organization of the red blood cell membrane. PNAS. 2008;105(23):8026-8031.
  • 17. Siddon AJ, Tormey CA. The chemical and laboratory investigation of hemolysis. Adv. Clin. Chem. 2019;89:215-258.
  • 18. Varo R, Chaccour C, Bassat Q. Update on malaria. Med. Clin. (English Edition). 2020;155(9):395-402.
  • 19. Farrar J, Hotez P, Junghanss T, Kang G, Lalloo D, White NJ. Manson's Tropical Diseases E-Book. Elsevier health sciences; 2013.
  • 20. Jakeman G, Saul A, Hogarth W, Collins W. Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology. 1999;119(2):127-133.
  • 21. Matthews K, Duffy SP, Myrand-Lapierre ME, et al. Microfluidic analysis of red blood cell deformability as a means to assess hemin-induced oxidative stress resulting from Plasmodium falciparum intraerythrocytic parasitism. Integr. Biol. 2017;9(6):519-528.
  • 22. White NJ. Anaemia and malaria. Malar. J. 2018;17(1):1-17.
  • 23. Deng X, Duffy SP, Myrand-Lapierre ME, et al. Reduced deformability of parasitized red blood cells as a biomarker for anti-malarial drug efficacy. Malar. J. 2015;14:1-9.
  • 24. Dugar S, Choudhary C, Duggal A. Sepsis and septic shock: Guideline-based management. Cleve Clin J Med. 2020;87(1):53-64.
  • 25. Minasyan H. Sepsis: mechanisms of bacterial injury to the patient. Scand. J. Trauma, Resusc. Emerg. Med. 2019;27(1):1-22.
  • 26. Chan YL, Han ST, Li CH, Wu CC, Chen KF. Transfusion of red blood cells to patients with sepsis. Int. J. Mol. Sci. 2017;18(9):1946.
  • 27. Vincent JL, De Backer D. Oxygen transport—the oxygen delivery controversy. Intensive Care Med. 2004;30:1990-1996.
  • 28. Moutzouri AG, Skoutelis AT, Gogos CA, Missirlis YF, Athanassiou GM. Red blood cell deformability in patients with sepsis: a marker for prognosis and monitoring of severity. Clin. Hemorheol. Microcirc. 2007;36(4):291-299.
  • 29. Luepker RV, Lakshminarayan K. Cardiovascular and cerebrovascular diseases. Oxford Textbook of Public Health, Volume 3: the practice of public health. 2009;(Ed. 5):971-996.
  • 30. Li N, Zhou H, Tang Q. Red blood cell distribution width: a novel predictive indicator for cardiovascular and cerebrovascular diseases. Dis. Markers. 2017;2017:7089493.
  • 31. Strömberg S, Nordanstig A, Bentzel T, Österberg K, Bergström G. Risk of early recurrent stroke in symptomatic carotid stenosis. Eur. J. Vasc. Endovasc. Surg. 2015;49(2):137-144.
  • 32. Kara H, Degirmenci S, Bayir A, et al. Red cell distribution width and neurological scoring systems in acute stroke patients. Neuropsychiatr. Dis. Treat. 2015;733-739.
  • 33. Boisseau M, Freyburger G, Lorient-Roudaut M. Changes in blood filterability in cerebrovascular accidents. Wien. Med. Wochenschr. 1986;136:44-46.
  • 34. Groen K, Maltby VE, Sanders KA, Scott RJ, Tajouri L, Lechner-Scott J. Erythrocytes in multiple sclerosis–forgotten contributors to the pathophysiology? Mult. Scler. J. Exp. Transl. Clin. 2016;2:2055217316649981.
  • 35. Ljubisavljevic S, Stojanovic I, Cvetkovic T, et al. Erythrocytes' antioxidative capacity as a potential marker of oxidative stress intensity in neuroinflammation. Neurol. Sci. 2014;337(1-2):8-13.
  • 36. Simpson LO, Shand BI, Olds RJ, Larking PW, Arnott MJ. Red cell and hemorheological changes in multiple sclerosis. Pathology. 1987;19(1):51-55.
  • 37. Wang Y, Yang P, Yan Z, et al. The relationship between erythrocytes and diabetes mellitus. J. Diabetes Res. 2021;2021.
  • 38. Lee S, Lee MY, Nam JS, et al. Hemorheological approach for early detection of chronic kidney disease and diabetic nephropathy in type 2 diabetes. Diabetes Technol. Ther. 2015;17(11):808-815.
  • 39. Babu N, Singh M. Influence of hyperglycemia on aggregation, deformability and shape parameters of erythrocytes. Clin. Hemorheol. Microcirc. 2004;31(4):273-280.
  • 40. Levi E, Başkurt O, Kahdemir N, Aidaç S, Kutman M, Üçer O. Changes in erythrocyte deformability during experimental hyperthyroidism. Clin. Hemorheol. Microcirc. 1989;9(4):577-581.
  • 41. Davidson R, Cumming A, Leel V, How J, Bewsher P, Khir A. A search for the mechanism underlying the altered MCV in thyroid dysfunction: a study of serum and red cell membrane lipids. Scand. J. Haematol. 1984;32(1):19-24.
  • 42. Sütterlin U, Gless KH, Schaz K, Hüfner M, Schütz V, Hunstein W. Peripheral effects of thyroid hormones: alteration of intracellular Na-concentration, ouabain-sensitive Na-transport, and Na-Li countertransport in human red blood cells. Klin. Wochenschr. 1984;62(12):598-601.
  • 43. Xiao T, Cai Y, Chen B. HIV-1 entry and membrane fusion inhibitors. Viruses. 2021;13(5):735.
  • 44. Geene D, Sudre P, Anwar D, Goehring C, Saaidia A, Hirschel B. Causes of macrocytosis in HIV-infected patients not treated with zidovudine. Swiss HIV Cohort Study. J. Infect. 2000;40(2):160-163.
  • 45. Baskurt OK, Meiselman HJ. Activated polymorphonuclear leukocytes affect red blood cell aggregability. J. Leukoc. Biol. 1998;63(1):89-93.
  • 46. Kim A, Dadgostar H, Holland GN, et al. Hemorheologic abnormalities associated with HIV infection: altered erythrocyte aggregation and deformability. Invest. Ophthalmol. Vis. Sci. 2006;47(9):3927-3932.
  • 47. Prudinnik DS, Sinauridze EI, Shakhidzhanov SS, et al. Filterability of erythrocytes in Patients with COVID-19. Biomolecules. 2022;12(6):782.
  • 48. Renoux C, Fort R, Nader E, et al. Impact of COVID-19 on red blood cell rheology. Br. J. Haematol. 2021;192(4):e108-e111.
  • 49. Baskurt O, Boynard M, Cokelet G, et al. New guidelines for hemorheological laboratory techniques. Clin. Hemorheol. Microcirc. 2009;42(2):75-97.
  • 50. Kubánková M, Hohberger B, Hoffmanns J, et al. Physical phenotype of blood cells is altered in COVID-19. Biophys. J. 2021;120(14):2838-2847.
  • 51. Ulrich H, Pillat MM. CD147 as a target for COVID-19 treatment: suggested effects of azithromycin and stem cell engagement. Stem Cell Rev. Rep. 2020;16(3):434-440.
There are 51 citations in total.

Details

Primary Language Turkish
Subjects Clinical Sciences (Other)
Journal Section Articles
Authors

Fadime Köse 0000-0002-6822-6263

Nurten Bahtiyar 0000-0003-2420-8415

Fatma Behice Cinemre 0000-0002-1972-1575

Birsen Aydemir 0000-0003-1406-864X

Project Number YOK
Early Pub Date January 8, 2024
Publication Date January 5, 2024
Acceptance Date December 11, 2023
Published in Issue Year 2023 Issue: 21 - December

Cite

APA Köse, F., Bahtiyar, N., Cinemre, F. B., Aydemir, B. (2024). Hastalıkların Fizyopatolojisinde Eritrosit Deformabilitesinin Önemi. İstanbul Gelişim Üniversitesi Sağlık Bilimleri Dergisi(21), 1262-1272. https://doi.org/10.38079/igusabder.1313165
AMA Köse F, Bahtiyar N, Cinemre FB, Aydemir B. Hastalıkların Fizyopatolojisinde Eritrosit Deformabilitesinin Önemi. IGUSABDER. January 2024;(21):1262-1272. doi:10.38079/igusabder.1313165
Chicago Köse, Fadime, Nurten Bahtiyar, Fatma Behice Cinemre, and Birsen Aydemir. “Hastalıkların Fizyopatolojisinde Eritrosit Deformabilitesinin Önemi”. İstanbul Gelişim Üniversitesi Sağlık Bilimleri Dergisi, no. 21 (January 2024): 1262-72. https://doi.org/10.38079/igusabder.1313165.
EndNote Köse F, Bahtiyar N, Cinemre FB, Aydemir B (January 1, 2024) Hastalıkların Fizyopatolojisinde Eritrosit Deformabilitesinin Önemi. İstanbul Gelişim Üniversitesi Sağlık Bilimleri Dergisi 21 1262–1272.
IEEE F. Köse, N. Bahtiyar, F. B. Cinemre, and B. Aydemir, “Hastalıkların Fizyopatolojisinde Eritrosit Deformabilitesinin Önemi”, IGUSABDER, no. 21, pp. 1262–1272, January 2024, doi: 10.38079/igusabder.1313165.
ISNAD Köse, Fadime et al. “Hastalıkların Fizyopatolojisinde Eritrosit Deformabilitesinin Önemi”. İstanbul Gelişim Üniversitesi Sağlık Bilimleri Dergisi 21 (January 2024), 1262-1272. https://doi.org/10.38079/igusabder.1313165.
JAMA Köse F, Bahtiyar N, Cinemre FB, Aydemir B. Hastalıkların Fizyopatolojisinde Eritrosit Deformabilitesinin Önemi. IGUSABDER. 2024;:1262–1272.
MLA Köse, Fadime et al. “Hastalıkların Fizyopatolojisinde Eritrosit Deformabilitesinin Önemi”. İstanbul Gelişim Üniversitesi Sağlık Bilimleri Dergisi, no. 21, 2024, pp. 1262-7, doi:10.38079/igusabder.1313165.
Vancouver Köse F, Bahtiyar N, Cinemre FB, Aydemir B. Hastalıkların Fizyopatolojisinde Eritrosit Deformabilitesinin Önemi. IGUSABDER. 2024(21):1262-7.

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