The effect of endobronchial coil treatment (EBCT) on hemorheological parameters and oxidative stress: a pilot study
Yıl 2025,
Cilt: 18 Sayı: 2, 5 - 5
Erhan Ugurlu
,
Emine Kılıç Toprak
,
Nazlı Çetin
,
Özgen Kılıç Erkek
,
Nilüfer Yiğit
,
Hilmiye Pakyürek
,
Göksel Altınışık Ergur
,
Z. Melek Küçükatay
Öz
Objective: Chronic Obstructive Pulmonary Disease (COPD) is a common, preventable, curable disease characterized by persistent airflow limitation, respiratory symptoms due to airway and/or alveolar abnormalities caused by severe exposure to harmful particles, gases. During the endobronchial coil treatment (EBCT) process, the volume of the lung parenchyma is reduced by shrinking the elastic recoil. Although there are studies showing worsening of hemorheological parameters in COPD exacerbations, no study investigated whether hemorheological parameters are improved after coil. The aim of this study was to assess the effects of coil therapy on erythrocyte deformability, whole blood viscosity (WBV) measured at autologous, standard (40%) hematocrit and plasma viscosity (PV) in COPD patients.
Material and methods: Venous blood samples were taken once from the healthy control group (n=17) and before and 1 month after the treatment from the COPD patients who had been indicated for coil according to GOLD guidelines (n=20). To assess erythrocyte deformability, shear-dependent erythrocyte elongation was measured at 0.3-3.0 Pa by an ektacytometer (LORCA), while WBV, PV were measured using a rotational viscometer.
Results: Erythrocyte deformability measured at shear stresses between 0.3-5.33 Pa were found to be higher following treatment compared to pre-coil values. EBCT did not have a statistically significant effect on WBV measured at autologous, 40% hematocrit, PV and oxidative stress indices.
Conclusion: Increased erythrocyte deformability determined following EBCT at the shear stresses observed at the pulmonary level is a favourable finding, showing that the procedure may positively affect the hemodynamics of COPD patients as well as causing clinical improvement.
Kaynakça
- 1. Rabe KF, Watz H. Chronic obstructive pulmonary disease. Lancet 2017;389:1931-1940. https://doi.org/10.1016/S0140-6736(17)31222-9
- 2. Mendy A, Salo PM, Cohn RD, Wilkerson J, Zeldin DC, Thorne PS. House dust endotoxin association with chronic bronchitis and emphysema. Environ Health Perspect 2018;126:037007. https://doi.org/10.1289/EHP2452
- 3. Shah PL, Herth FJ, van Geffen WH, Deslee G, Slebos DJ. Lung volume reduction for emphysema. Lancet Respir Med 2017;5:147-156. https://doi.org/10.1016/S2213-2600(16)30221-1
- 4. Toker Ugurlu T, Ugurlu E. Impacts of coil treatment on anxiety and depression in emphysema. Can Respir J 2020;2020:4270826. https://doi.org/10.1155/2020/4270826
- 5. Global Strategy for the Diagnosis, Management and Prevention of COPD, Global Initiative for Chronic Obstructive Lung Disease (GOLD) 2020. Available at: http://goldcopd.org. Accessed October 1, 2021
- 6. Ugurlu E, Kilic Toprak E, Can I, Kilic Erkek O, Altinisik G, Bor Kucukatay M. Impaired hemorheology in exacerbations of COPD. Can Respir J 2017;2017:1286263. https://doi.org/10.1155/2017/1286263
- 7. Marchetti N, Kaufman T, Chandra D, et al. Endobronchial coils versus lung volume reduction surgery or medical therapy for treatment of advanced homogenous emphysema. Chronic Obstr Pulm Dis 2018;5:87-96. https://doi.org/10.15326/jcopdf.5.2.2017.0134
- 8. Uğurlu E, Çetin N, Yiğit N, et al. A retrospective evaluation of the pulmonary function tests and quality of life assessment surveys of emphysema patients subject to coil treatment. Tuberk Toraks 2020;68:399-406. https://doi.org/10.5578/tt.70358
- 9. Copley AL. Fluid mechanics and biorheology. Biorheology 1990;27:3-19. https://doi.org/10.3233/bir-1990-27102
10. Baskurt OK, Meiselman HJ. Blood rheology and hemodynamics. Semin Thromb Hemost 2003;29:435-450. https://doi.org/10.1055/s-2003-44551
- 11. Rahman I, MacNee W. Antioxidant pharmacological therapies for COPD. Curr Opin Pharmacol 2012;12:256-265. https://doi.org/10.1016/j.coph.2012.01.015
- 12. Rahman I. Antioxidant therapies in COPD. Int J Chron Obstruct Pulmon Dis 2006;1:15-29. https://doi.org/10.2147/copd.2006.1.1.15
- 13. Aydemir Y, Aydemir Ö, Şengül A, et al. Comparison of oxidant/antioxidant balance in COPD and non-COPD smokers. Heart Lung 2019;48:566‐569. https://doi.org/10.1016/j.hrtlng.2019.07.005
- 14. Fischer BM, Voynow JA, Ghio AJ. COPD: balancing oxidants and antioxidants. Int J Chron Obstruct Pulmon Dis 2015;10:261-276. https://doi.org/10.2147/COPD.S42414
- 15. Ugurlu E, Kilic Toprak E, Altinisik G, et al. Increased erythrocyte aggregation and oxidative stress in patients with idiopathic interstitial pneumonia. Sarcoidosis Vasc Diffuse Lung Dis 2016;33:308-316.
- 16. Gyawali P, Richards RS, Bwititi PT, Nwose EU. Association of abnormal erythrocyte morphology with oxidative stress and inflammation in metabolic syndrome. Blood Cells Mol Dis 2015;54:360-363. https://doi.org/10.1016/j.bcmd.2015.01.005
- 17. Coppola L, Verrazzo G, Esposito G, et al. Hemorheological and cardiovascular effects of exercise training in the rehabilitation of elderly patients with chronic obstructive pulmonary disease. Arch Gerontol Geriatr 1999;28:1-8. https://doi.org/10.1016/s0167-4943(98)00115-0
- 18. Cakmak G, Ates Alkan F, Korkmaz K, et al. Blood viscosity as a forgotten factor and its effect on pulmonary flow. Transl Respir Med 2013;1:3. https://doi.org/10.1186/2213-0802-1-3
- 19. Herth FJF, Slebos DJ, Criner GJ, Shah PL. Endoscopic lung volume reduction: an expert panel recommendation – update 2017. Respiration 2017;94:380-388. https://doi.org/10.1159/000479379
- 20. Baskurt OK, Boynard M, Cokelet GC, et al. New guidelines for hemorheological laboratory techniques. Clin Hemorheol Microcirc 2009;42:75-97. https://doi.org/10.3233/CH-2009-1202
- 21. Hardeman MR, Goedhart P, Shin S. Methods in hemorheology. In: Baskurt OK, Hardeman MR, Rampling MR, Meiselman HJ, editors. Handbook of hemorheology and hemodynamics. Netherlands: IOS Press 2007:242-266.
- 22. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem 2005;38:1103-1111. https://doi.org/10.1016/j.clinbiochem.2005.08.008
- 23. Erel O. A novel automated method to measure total antioxidant response against potent free radical reactions. Clin Biochem 2004;37:112-119. https://doi.org/10.1016/j.clinbiochem.2003.10.014
- 24. Profita M, Giorgi RD, Sala A, et al. Muscarinic receptors, leukotriene B4 production and neutrophilic inflammation in COPD patients. Allergy 2005;60:1361-1369. https://doi.org/10.1111/j.1398-9995.2005.00892.x
- 25. Tertemiz KC, Ozgen Alpaydin A, Sevinc C, Ellidokuz H, Acara AC, Cimrin A. Could "red cell distribution width" predict COPD severity? Rev Port Pneumol (2006) 2016;22:196-201. https://doi.org/10.1016/j.rppnen.2015.11.006
- 26. Ekin S, Arısoy A, Gunbatar H, et al. The relationships among the levels of oxidative and antioxidative parameters, FEV1 and prolidase activity in COPD. Redox Rep 2017;22:74-77. https://doi.org/10.1080/13510002.2016.1139293
- 27. Ben Anes A, Ben Nasr H, Garrouche A, et al. The Cu/Zn superoxide dismutase +35A/C (rs2234694) variant correlates with altered levels of protein carbonyls and glutathione and associates with severity of COPD in a Tunisian population. Free Radic Res 2019;53:293-303. https://doi.org/10.1080/10715762.2019.1572888
- 28. Reznick AZ, Packer L. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 1994;233:357-563. https://doi.org/10.1016/s0076-6879(94)33041-7
- 29. Donaldson GC, Seemungal TAR, Patel IS, et al. Airway and systemic inflammation and decline in lung function in patients with COPD. Chest 2005;128:1995-2004. https://doi.org/10.1378/chest.128.4.1995
- 30. Kosecik M, Erel O, Sevinc E, Selek S. Increased oxidative stress in children exposed to passive smoking. Int J Cardiol 2005;100:61-64. https://doi.org/10.1016/j.ijcard.2004.05.069
- 31. Barnes PJ. Cellular and molecular mechanisms of asthma and COPD. Clin Sci (Lond) 2017;131:1541-1558. https://doi.org/10.1042/CS20160487
- 32. Salvagno GL, Sanchis Gomar F, Picanza A, Lippi G. Red blood cell distribution width: a simple parameter with multiple clinical applications. Crit Rev Clin Lab Sci 2015;52:86-105. https://doi.org/10.3109/10408363.2014.992064
- 33. Sato K, Inoue S, Ishibashi Y, et al. Association between low mean corpuscular hemoglobin and prognosis in patients with exacerbation of chronic obstructive pulmonary disease. Respir Investig 2021;59:498-504. https://doi.org/10.1016/j.resinv.2021.01.006
- 34. Nickol AH, Frise MC, Cheng HY, et al. A cross-sectional study of the prevalence and associations of iron deficiency in a cohort of patients with chronic obstructive pulmonary disease. BMJ Open 2015;5:e007911. https://doi.org/10.1136/bmjopen-2015-007911
- 35. Horoz M, Bolukbas C, Bolukbas FF, et al. Oxidative stress in hepatitis C infected end-stage renal disease subjects. BMC Infect Dis 2006;6:114. https://doi.org/10.1186/1471-2334-6-114
- 36. Ahmad B, Ferrari N, Montiel G, et al. Influence of amoderate physical activity intervention on red cell deformability in patients suffering from chronic obstructive pulmonary disease (COPD). Wien Med Wochenschr 2013;163:334-339. https://doi.org/10.1007/s10354-013-0183-7
- 37. Simmonds MJ, Meiselman HJ, Baskurt OK. Blood rheology and aging. J Geriatr Cardiol 2013;10:291-301. https://doi.org/10.3969/j.issn.1671-5411.2013.03.010
- 38. Tikhomirova IA, Oslyakova AO, Mikhailova SG. Microcirculation and blood rheology in patients with cerebrovascular disorders. Clin Hemorheol Microcirc 2011;49:295-305. https://doi.org/10.3233/CH-2011-1480
- 39. Barshtein G, Ben Ami R, Yedgar S. Role of red blood cell flow behavior in hemodynamics and hemostasis. Expert Rev Cardiovasc Ther 2007;5:743-752. https://doi.org/10.1586/14779072.5.4.743
- 40. Carr RT, Lacoin M. Nonlinear dynamics of microvascular blood flow. Ann Biomed Eng 2000;28:641-652. https://doi.org/10.1114/1.1306346
- 41. Novák Z, Gyurkovits K. Examination of red blood cell deformability in cystic fibrosis. Acta Univ Carol Med (Praha) 1990;36:68-70.
- 42. Halvani A, Haddad H. Comparison of the factors influencing pulmonary arterial pressure in smoker and non-smoker COPD patients with pulmonary hypertension. Tanaffos 2019;18:41-46.
- 43. Schäfer M, Kheyfets VO, Schroeder JD, et al. Main pulmonary arterial wall shear stress correlates with invasive hemodynamics and stiffness in pulmonary hypertension. Pulm Circ 2016;6:37-45. https://doi.org/10.1086/685024
- 44. Verbitskiĭ ON, Buturov IV, lu Purkh T, Fadi Fanari M, Par¬aska VI. Hemodynamics, blood gas composition and viscosity in pa¬tients with chronic obstructive bronchitis complicated by chronic cor pulmonale. Probl Tuberk Bolezn Legk 2004;7:42-45.
- 45. Brun JF, Varlet Marie E, Romain AJ, Guiraudou M, Raynaud de Mauver E. Exercise hemorheology: moving from old simplistic paradigmstoamore complex picture. Clin Hemorheol Microcirc 2013;55:15-27. https://doi.org/10.3233/CH-131686
- 46. Clivati A, Marazzini L, Agosti R, Gatto R, Longhini E. Effect of hematocrit on the blood viscosity of patients with chronic respiratory failure and secondary polycythemia. Respiration 1980;40:201-207. https://doi.org/10.1159/000194285
- 47. Cheng AL, Takao CM, Wenby RB, Meiselman HJ, Wood JC, Detterich JA. Elevated low-shear blood viscosity is associated with decreased pulmonary blood flow in children with univentricular heart defects. Pediatr Cardiol 2016;37:789-801. https://doi.org/10.1007/s00246-016-1352-4
- 48. Almarshad HA, Hassan FM. Alterations in blood coagulation and viscosity among young male cigarette smokers of al-jouf region in Saudi Arabia. Clin Appl Thromb Hemost 2016;22:386-389. https://doi.org/10.1177/1076029614561319
- 49. Lowe GD, Drummond MM, Forbes CD, Barbenel JC. The effects of age and cigarette-smoking on blood and plasma viscosity in men. Scottish Med J 1980;25:13-17. https://doi.org/10.1177/003693308002500103
Endobronşiyal koil tedavisinin (EBCT) hemoreolojik parametreler ve oksidatif stres üzerine etkisi: pilot çalışma
Yıl 2025,
Cilt: 18 Sayı: 2, 5 - 5
Erhan Ugurlu
,
Emine Kılıç Toprak
,
Nazlı Çetin
,
Özgen Kılıç Erkek
,
Nilüfer Yiğit
,
Hilmiye Pakyürek
,
Göksel Altınışık Ergur
,
Z. Melek Küçükatay
Öz
Amaç: Kronik Obstrüktif Akciğer Hastalığı (KOAH), zararlı partiküllere, gazlara şiddetli maruziyetin neden olduğu hava yolu ve/veya alveolar anormalliklere bağlı kalıcı hava akımı kısıtlılığı, solunum semptomları ile karakterize yaygın, önlenebilir, tedavi edilebilir bir hastalıktır. Endobronşiyal koil tedavisi (EBCT) işlemi sırasında elastik geri tepme küçültülerek akciğer parankiminin hacmi azaltılır. KOAH alevlenmelerinde hemoreolojik parametrelerin kötüleştiğini gösteren çalışmalar olmasına rağmen, koil sonrası hemoreolojik parametrelerin iyileşip iyileşmediğini araştıran bir çalışma yoktur. Bu çalışmanın amacı, KOAH hastalarında koil tedavisinin eritrosit deformabilitesi, otolog, standart (%40) hematokritte ölçülen tam kan viskozitesi (WBV) ve plazma viskozitesi (PV) üzerindeki etkilerini değerlendirmektir.
Gereç ve yöntem: Sağlıklı kontrol grubundan (n=17) ve GOLD yönergelerine göre coil için endikasyon konulmuş olan KOAH hastalarından (n=20) tedaviden önce ve 1 ay sonra venöz kan örnekleri alındı. Eritrosit deformabilitesini değerlendirmek için, kaymaya bağlı eritrosit uzaması 0,3-3,0 Pa'da bir ektasitometre (LORCA) ile ölçülürken, WBV, PV rotasyonel bir viskozimetre kullanılarak ölçüldü.
Bulgular: Eritrosit deformabilitesi 0,3-5,33 Pa arasındaki kayma streslerinde ölçülmüş ve tedavi sonrasında coil öncesi değerlere kıyasla daha yüksek bulunmuştur. EBCT'nin otolog, %40 hematokrit, PV ve oksidatif stres indekslerinde ölçülen WBV üzerinde istatistiksel olarak anlamlı bir etkisi olmamıştır.
Sonuç: EBCT sonrasında pulmoner düzeyde gözlenen kayma gerilimlerinde belirlenen artmış eritrosit deformabilitesi, işlemin KOAH hastalarının hemodinamiğini olumlu yönde etkileyebileceğini ve klinik iyileşmeye neden olabileceğini gösteren olumlu bir bulgudur.
Kaynakça
- 1. Rabe KF, Watz H. Chronic obstructive pulmonary disease. Lancet 2017;389:1931-1940. https://doi.org/10.1016/S0140-6736(17)31222-9
- 2. Mendy A, Salo PM, Cohn RD, Wilkerson J, Zeldin DC, Thorne PS. House dust endotoxin association with chronic bronchitis and emphysema. Environ Health Perspect 2018;126:037007. https://doi.org/10.1289/EHP2452
- 3. Shah PL, Herth FJ, van Geffen WH, Deslee G, Slebos DJ. Lung volume reduction for emphysema. Lancet Respir Med 2017;5:147-156. https://doi.org/10.1016/S2213-2600(16)30221-1
- 4. Toker Ugurlu T, Ugurlu E. Impacts of coil treatment on anxiety and depression in emphysema. Can Respir J 2020;2020:4270826. https://doi.org/10.1155/2020/4270826
- 5. Global Strategy for the Diagnosis, Management and Prevention of COPD, Global Initiative for Chronic Obstructive Lung Disease (GOLD) 2020. Available at: http://goldcopd.org. Accessed October 1, 2021
- 6. Ugurlu E, Kilic Toprak E, Can I, Kilic Erkek O, Altinisik G, Bor Kucukatay M. Impaired hemorheology in exacerbations of COPD. Can Respir J 2017;2017:1286263. https://doi.org/10.1155/2017/1286263
- 7. Marchetti N, Kaufman T, Chandra D, et al. Endobronchial coils versus lung volume reduction surgery or medical therapy for treatment of advanced homogenous emphysema. Chronic Obstr Pulm Dis 2018;5:87-96. https://doi.org/10.15326/jcopdf.5.2.2017.0134
- 8. Uğurlu E, Çetin N, Yiğit N, et al. A retrospective evaluation of the pulmonary function tests and quality of life assessment surveys of emphysema patients subject to coil treatment. Tuberk Toraks 2020;68:399-406. https://doi.org/10.5578/tt.70358
- 9. Copley AL. Fluid mechanics and biorheology. Biorheology 1990;27:3-19. https://doi.org/10.3233/bir-1990-27102
10. Baskurt OK, Meiselman HJ. Blood rheology and hemodynamics. Semin Thromb Hemost 2003;29:435-450. https://doi.org/10.1055/s-2003-44551
- 11. Rahman I, MacNee W. Antioxidant pharmacological therapies for COPD. Curr Opin Pharmacol 2012;12:256-265. https://doi.org/10.1016/j.coph.2012.01.015
- 12. Rahman I. Antioxidant therapies in COPD. Int J Chron Obstruct Pulmon Dis 2006;1:15-29. https://doi.org/10.2147/copd.2006.1.1.15
- 13. Aydemir Y, Aydemir Ö, Şengül A, et al. Comparison of oxidant/antioxidant balance in COPD and non-COPD smokers. Heart Lung 2019;48:566‐569. https://doi.org/10.1016/j.hrtlng.2019.07.005
- 14. Fischer BM, Voynow JA, Ghio AJ. COPD: balancing oxidants and antioxidants. Int J Chron Obstruct Pulmon Dis 2015;10:261-276. https://doi.org/10.2147/COPD.S42414
- 15. Ugurlu E, Kilic Toprak E, Altinisik G, et al. Increased erythrocyte aggregation and oxidative stress in patients with idiopathic interstitial pneumonia. Sarcoidosis Vasc Diffuse Lung Dis 2016;33:308-316.
- 16. Gyawali P, Richards RS, Bwititi PT, Nwose EU. Association of abnormal erythrocyte morphology with oxidative stress and inflammation in metabolic syndrome. Blood Cells Mol Dis 2015;54:360-363. https://doi.org/10.1016/j.bcmd.2015.01.005
- 17. Coppola L, Verrazzo G, Esposito G, et al. Hemorheological and cardiovascular effects of exercise training in the rehabilitation of elderly patients with chronic obstructive pulmonary disease. Arch Gerontol Geriatr 1999;28:1-8. https://doi.org/10.1016/s0167-4943(98)00115-0
- 18. Cakmak G, Ates Alkan F, Korkmaz K, et al. Blood viscosity as a forgotten factor and its effect on pulmonary flow. Transl Respir Med 2013;1:3. https://doi.org/10.1186/2213-0802-1-3
- 19. Herth FJF, Slebos DJ, Criner GJ, Shah PL. Endoscopic lung volume reduction: an expert panel recommendation – update 2017. Respiration 2017;94:380-388. https://doi.org/10.1159/000479379
- 20. Baskurt OK, Boynard M, Cokelet GC, et al. New guidelines for hemorheological laboratory techniques. Clin Hemorheol Microcirc 2009;42:75-97. https://doi.org/10.3233/CH-2009-1202
- 21. Hardeman MR, Goedhart P, Shin S. Methods in hemorheology. In: Baskurt OK, Hardeman MR, Rampling MR, Meiselman HJ, editors. Handbook of hemorheology and hemodynamics. Netherlands: IOS Press 2007:242-266.
- 22. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem 2005;38:1103-1111. https://doi.org/10.1016/j.clinbiochem.2005.08.008
- 23. Erel O. A novel automated method to measure total antioxidant response against potent free radical reactions. Clin Biochem 2004;37:112-119. https://doi.org/10.1016/j.clinbiochem.2003.10.014
- 24. Profita M, Giorgi RD, Sala A, et al. Muscarinic receptors, leukotriene B4 production and neutrophilic inflammation in COPD patients. Allergy 2005;60:1361-1369. https://doi.org/10.1111/j.1398-9995.2005.00892.x
- 25. Tertemiz KC, Ozgen Alpaydin A, Sevinc C, Ellidokuz H, Acara AC, Cimrin A. Could "red cell distribution width" predict COPD severity? Rev Port Pneumol (2006) 2016;22:196-201. https://doi.org/10.1016/j.rppnen.2015.11.006
- 26. Ekin S, Arısoy A, Gunbatar H, et al. The relationships among the levels of oxidative and antioxidative parameters, FEV1 and prolidase activity in COPD. Redox Rep 2017;22:74-77. https://doi.org/10.1080/13510002.2016.1139293
- 27. Ben Anes A, Ben Nasr H, Garrouche A, et al. The Cu/Zn superoxide dismutase +35A/C (rs2234694) variant correlates with altered levels of protein carbonyls and glutathione and associates with severity of COPD in a Tunisian population. Free Radic Res 2019;53:293-303. https://doi.org/10.1080/10715762.2019.1572888
- 28. Reznick AZ, Packer L. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 1994;233:357-563. https://doi.org/10.1016/s0076-6879(94)33041-7
- 29. Donaldson GC, Seemungal TAR, Patel IS, et al. Airway and systemic inflammation and decline in lung function in patients with COPD. Chest 2005;128:1995-2004. https://doi.org/10.1378/chest.128.4.1995
- 30. Kosecik M, Erel O, Sevinc E, Selek S. Increased oxidative stress in children exposed to passive smoking. Int J Cardiol 2005;100:61-64. https://doi.org/10.1016/j.ijcard.2004.05.069
- 31. Barnes PJ. Cellular and molecular mechanisms of asthma and COPD. Clin Sci (Lond) 2017;131:1541-1558. https://doi.org/10.1042/CS20160487
- 32. Salvagno GL, Sanchis Gomar F, Picanza A, Lippi G. Red blood cell distribution width: a simple parameter with multiple clinical applications. Crit Rev Clin Lab Sci 2015;52:86-105. https://doi.org/10.3109/10408363.2014.992064
- 33. Sato K, Inoue S, Ishibashi Y, et al. Association between low mean corpuscular hemoglobin and prognosis in patients with exacerbation of chronic obstructive pulmonary disease. Respir Investig 2021;59:498-504. https://doi.org/10.1016/j.resinv.2021.01.006
- 34. Nickol AH, Frise MC, Cheng HY, et al. A cross-sectional study of the prevalence and associations of iron deficiency in a cohort of patients with chronic obstructive pulmonary disease. BMJ Open 2015;5:e007911. https://doi.org/10.1136/bmjopen-2015-007911
- 35. Horoz M, Bolukbas C, Bolukbas FF, et al. Oxidative stress in hepatitis C infected end-stage renal disease subjects. BMC Infect Dis 2006;6:114. https://doi.org/10.1186/1471-2334-6-114
- 36. Ahmad B, Ferrari N, Montiel G, et al. Influence of amoderate physical activity intervention on red cell deformability in patients suffering from chronic obstructive pulmonary disease (COPD). Wien Med Wochenschr 2013;163:334-339. https://doi.org/10.1007/s10354-013-0183-7
- 37. Simmonds MJ, Meiselman HJ, Baskurt OK. Blood rheology and aging. J Geriatr Cardiol 2013;10:291-301. https://doi.org/10.3969/j.issn.1671-5411.2013.03.010
- 38. Tikhomirova IA, Oslyakova AO, Mikhailova SG. Microcirculation and blood rheology in patients with cerebrovascular disorders. Clin Hemorheol Microcirc 2011;49:295-305. https://doi.org/10.3233/CH-2011-1480
- 39. Barshtein G, Ben Ami R, Yedgar S. Role of red blood cell flow behavior in hemodynamics and hemostasis. Expert Rev Cardiovasc Ther 2007;5:743-752. https://doi.org/10.1586/14779072.5.4.743
- 40. Carr RT, Lacoin M. Nonlinear dynamics of microvascular blood flow. Ann Biomed Eng 2000;28:641-652. https://doi.org/10.1114/1.1306346
- 41. Novák Z, Gyurkovits K. Examination of red blood cell deformability in cystic fibrosis. Acta Univ Carol Med (Praha) 1990;36:68-70.
- 42. Halvani A, Haddad H. Comparison of the factors influencing pulmonary arterial pressure in smoker and non-smoker COPD patients with pulmonary hypertension. Tanaffos 2019;18:41-46.
- 43. Schäfer M, Kheyfets VO, Schroeder JD, et al. Main pulmonary arterial wall shear stress correlates with invasive hemodynamics and stiffness in pulmonary hypertension. Pulm Circ 2016;6:37-45. https://doi.org/10.1086/685024
- 44. Verbitskiĭ ON, Buturov IV, lu Purkh T, Fadi Fanari M, Par¬aska VI. Hemodynamics, blood gas composition and viscosity in pa¬tients with chronic obstructive bronchitis complicated by chronic cor pulmonale. Probl Tuberk Bolezn Legk 2004;7:42-45.
- 45. Brun JF, Varlet Marie E, Romain AJ, Guiraudou M, Raynaud de Mauver E. Exercise hemorheology: moving from old simplistic paradigmstoamore complex picture. Clin Hemorheol Microcirc 2013;55:15-27. https://doi.org/10.3233/CH-131686
- 46. Clivati A, Marazzini L, Agosti R, Gatto R, Longhini E. Effect of hematocrit on the blood viscosity of patients with chronic respiratory failure and secondary polycythemia. Respiration 1980;40:201-207. https://doi.org/10.1159/000194285
- 47. Cheng AL, Takao CM, Wenby RB, Meiselman HJ, Wood JC, Detterich JA. Elevated low-shear blood viscosity is associated with decreased pulmonary blood flow in children with univentricular heart defects. Pediatr Cardiol 2016;37:789-801. https://doi.org/10.1007/s00246-016-1352-4
- 48. Almarshad HA, Hassan FM. Alterations in blood coagulation and viscosity among young male cigarette smokers of al-jouf region in Saudi Arabia. Clin Appl Thromb Hemost 2016;22:386-389. https://doi.org/10.1177/1076029614561319
- 49. Lowe GD, Drummond MM, Forbes CD, Barbenel JC. The effects of age and cigarette-smoking on blood and plasma viscosity in men. Scottish Med J 1980;25:13-17. https://doi.org/10.1177/003693308002500103