Abstract
Variations in blood oxygen concentrations are not only part of the normal physiology but they may also indicate various pathological conditions. In the present work, we examined the influence of oxygen concentration on the rheological properties of whole human blood. Blood samples were taken from two healthy donors, a male and a female, with hematocrits 0.47 and 0.42, respectively. In addition to the original samples of normal oxygen concentration (normoxemia), samples of different blood oxygen level were also prepared by using the perfusion cell equipped with a gas supply to induce either hypoxemia by driving out the oxygen saturating blood by nitrogen or hyperoxemia by saturating blood with oxygen. The rheology of the samples was measured using a Physica MCR 301 rheometer equipped with a sensor designed for hemorheology. The rheological results showed that oxygen-depleted blood exhibited lower viscosity and a lower yield stress when fitted to the Herschel-Bulkley constitutive model. Blood flow simulations of the effect of oxygen concentration on the local hemodynamics were also carried out in an idealized axisymmetric 75 % stenosis and in a realistic carotid bifurcation geometry constructed from MRI images obtained from a healthy male volunteer. The modified Herschel-Bulkley model with the Papanastasiou regularization was used to account for both the shear thinning and finite yield stress properties of blood. The results of this work showed that oxygen concentration affects the rheology and flow behavior of blood, suggesting compensatory responses under hypoxic conditions leading to a lower blood viscosity.
Similar content being viewed by others
References
Apostolides AJ, Beris AN (2014) Modeling of the blood rheology in steady-state shear flows. J Rheol 58:607–633
Apostolides AJ, Armstrong MJ, Beris AN (2015) Modeling of human blood rheology in transient shear flows. J Rheol 59:275–298
Apostolides AJ, Beris AN (2016) The effect of cholesterol and triglycerides on the steady state shear rheology of blood. Rheol Acta 55:497–509
Aristokleous N, Seimenis I, Papaharilaou Y, Georgiou G, Brott BC, Anayiotos AS (2011) Effect of posture change on the geometric features of the healthy carotid bifurcation. IEEE Trans Inf Tech Biomed 15:148–154
Aristokleous N, Seimenis I, Georgiou GC, Nicolaides A, Anayiotos AS (2015) The effect of head rotation on the geometry and hemodynamics of healthy vertebral arteries. Ann Biomed Eng 43:1287–1297
Balmforth NJ, Frigaard IA, Ovarlez G (2014) Yielding to stress: recent developments in viscoplastic fluid mechanics. Annu Rev Fluid Mech 46:121–46
Barnes HA (1999) The yield stress—a review or ‘παντα ρει’—everything flows? J Non-Newtonian Fluid Mech 81:133–178
Benderro GF, LaManna JC (2013) Kidney EPO expression during chronic hypoxia in aged mice. Adv Exp Med Biol 765:9–14
Bertoluzzo SM, Bollini A, Rasia M, Raynal A (1999) Kinetic model for erythrocyte aggregation. Blood Cells Mol Dis 25:339–349
Bessonov N, Sequeira A, Simakov S, Vassilevskii Y, Volpert V (2016) Methods of blood flow modelling. Math Model Nat Phenom 11:1–25
Brun JF, Varlet-Marie E, Romain AJ, Guiraudou M, Raynaud de Mauverger E (2013) Exercise hemorheology: moving from old simplistic paradigms to a more complex picture. Clin Hemorheol Microcirc 55:15–27
Brust M, Schaefer C, Doerr R, Pan L, Garcia M, Arratia PE, Wagner C (2013) Rheology of human blood plasma: Viscoelastic versus Newtonian behavior. Phys Rev Lett 110:078305
Butler IB, Schoonen MA, Rickard DT (1994) Removal of dissolved oxygen from water: a comparison of four common techniques. Talanta 41:211–215
Caballero AD, Laín S (2015) Numerical simulation of non-Newtonian blood flow dynamics in human thoracic aorta. Comp Meth Biomech Biomed Eng 18:1200–1216
Caillaud C, Connes P, Bouix D, Mercier J (2002) Does haemorheology explain the paradox of hypoxemia during exercise in elite athletes or thoroughbred horses? Clin Hemorheol Microcirc 26:175–181
Chien S, Usami S, Dellenback RJ, Gregersen MI (1967) Blood viscosity: influence of erythrocyte aggregation. Science 157:827–829
Cokelet G, Merrill EW, Gilliland ER, Shin H, Britten A, Wells RE (1963) The rheology of human blood—measurement near and at zero shear rate. Trans Soc Rheol 7:303–317
Copley AI, Huang CR, King RG (1973) Rheogoniometric studies of whole human blood at shear rates from 1000 to 0.0009 sec-1. I. Experimental findings. Biogeosciences 10:17–22
De Cort SC, Innes JA, Barstow TJ, Guz A (1991) Cardiac output, oxygen consumption, and arteriovenous oxygen difference following a sudden rise in exercise level in humans. J Physiol 441:501–512
Diaw M, Samb A, Diop S, Sall ND, Ba A, Cissé F, Connes P (2014) Effects of hydration and water deprivation on blood viscosity during a soccer game in sickle cell trait carriers. Br J Sports Med 48:326–331
Dimakopoulos Y, Kelesidis G, Tsouka S, Georgiou GC, Tsamopoulos J (2015) Hemodynamics in stenotic microvessels under steady state conditions. Part I: the non-homogeneous model. J Biorheol 52:183–210
Dintenfass L (1962) Thixotropy of blood and proneness to thrombus formation. Circ Res 11:233–239
Dintenfass L (1971) Blood Microrheology—Viscosity Factors in Blood Flow, Ischaemia and Thrombosis, Butterworth
Esteva S, Panisello P, Torrella JR, Pages T, Viscor G (2009) Blood rheology adjustments in rats after a program of intermittent exposure to hypobaric hypoxia. High Alt Med Biol 10:275–281
Farquhar H, Weatherall M, Wijesinghe M, Perrin K, Ranchord A, Simmonds M, Beasley R (2009) Systematic review of studies of the effect of hyperoxia on coronary blood flow. Am Heart J 158:371–377
Fedosov DA, Pan W, Caswell B, Gompper G, Karniadakis GE (2011) Predicting human blood viscosity in silico. PNAS 108:11772–11777
Guner I, Uzun DD, Yaman MO, Genc H, Geligsen R, Korkmaz GG, Hallac M, Yelmen N, Sahin G, Karter Y, Simsek G (2013) The effect of chronic long-term intermittent hypobaric hypoxia on bone mineral density in rats: role of nitric oxide. Biol Trace Elem Res 154:262–267
Jia Y, Li P, Dziennis S, Wang RK (2011) Responses of peripheral blood flow to acute hypoxia and hyperoxia as measured by optical microangiography. PLoS One 6:e26802
Kang J, Li Y, Hu K, Lu W, Zhou X, Yu S, Xu L (2016) Chronic intermittent hypoxia versus continuous hypoxia: same effects on hemorheology? Clin Hemorheol Microcirc. doi:10.3233/CH-151973
Kim S, Namgung B, Ong PK, Cho YI, Chun KJ, Lim D (2009) Determination of rheological properties of whole blood with a scanning capillary-tube rheometer using constitutive models. J Mech Sci Technol 23:1718–1726
King MW (2015) Hemoglobin and Myoglobin. http://themedicalbiochemistrypage.org/hemoglobin-myoglobin.php#myoglobin
Kohl ZF, Crossley DA II, Tazawa H, Burggren WW (2015) Dynamics of blood viscosity regulation during hypoxic challenges in the chicken embryo (Gallus gallus domesticus). Comp Biochem Physiol A Mol Integr Physiol 190:1–8
Longo V, D’Alessandro A, Zolla L (2014) Deoxygenation of leucofiltered erythrocyte concentrates preserves proteome stability during storage in the blood bank. Blood Transfus 12:599–604
Lykov K, Li X, Lei H, Pivkin IV, Karniadakis GE (2015) Inflow/outflow boundary conditions for particle-based blood flow simulations: application to arterial bifurcations and trees. PLoS Comput Biol 11:e1004410
Merrill EW, Cheng CS, Pelletier GA (1969) Yield stress of normal human blood as a function of endogenous fibrinogen. J Appl Physiol 26:1–3
Mitsoulis E (2007) Flows of viscoplastic materials: models and computation. Rheol Reviews 2007:135–178
Núñez-Espinosa C, Douziech A, Ríos-Kristjánsson JG, Rizo D, Torrella JR, Pagè T, Viscor G (2014) Effect of intermittent hypoxia and exercise on blood rheology and oxygen transport in trained rats. Respir Physiol Neurobiol 192:112–117
Papanastasiou TC (1987) Flow of materials with yield. J Rheol 31:385–404
Picart C, Piau JM, Galliard H, Carpentier P (1998) Blood low shear rate rheometry: influence of fibrinogen level and hematocrit on slip and migrational effects. Biorheology 35:335–353
Picart C, Carpentier PH, Galliard H, Piau JM (1999) Blood yield stress in systemic sclerosis. Am J Physiol Heart Circ Physiol 276:771–777
Popel AS, Johnson PC (2005) Microcirculation and hemorheology. Annu Rev Fluid Mech 37:43–69
Rand PW, Lacombe E, Hunt HE, Auston WH (1964) Viscosity of normal; human blood under normothermic and hypothermic conditions. J Appl Physiol 19:117–122
Smith MM, Lucas AR, Hamlin RL, Devor ST (2015) Associations among hemorheological factors and maximal oxygen consumption. Is there a role for blood viscosity in explaining athletic performance? Clin Hemorheol Microcirc 60:347–362
Sousa PC, Pinho FT, Alves MA, Oliveira MSN (2016) A review of hemorheology: measuring techniques and recent advances. Korea-Australia Rheol J 28:1–22
Tada S (2010) Numerical study of oxygen transport in a carotid bifurcation. Phys Med Biol 55:3993–4010
Thurston GB (1996) Viscoelastic properties of blood and blood analogs. Adv Hemodynamics Hemorheol 1:1–30
Tu C, Deville M (1996) Pulsatile flow of non-Newtonian fluids through arterial stenoses. J Biomech 29:899–908
Valant AZ, Ziberna L, Papaharilaou Y, Anayiotos A, Georgiou GC (2011) The influence of temperature on rheological properties of blood mixtures with different volume expanders—implications in numerical arterial hemodynamics simulations. Rheol Acta 50:389–402
Vlastos G, Lerche D, Koch B, Samba O, Pohl M (1997) The effect of parallel combined steady and oscillatory shear flows on blood and polymer solutions. Rheol Acta 36:160–172
Yelmen N, Ozdemir S, Guner I, Toplan S, Sahin G, Yaman OM, Sipahi S (2011) The effects of chronic long-term intermittent hypobaric hypoxia on blood rheology parameters. Gen Physiol Biophys 30:389–395
Yeow YL, Wickramasinghe SR, Leong YK, Han B (2002) Model independent relationships between hematocrit, blood viscosity, and yield stress derived from Couette viscometry data. Biotechnol Prog 18:1068–1075
Zhang M, Li XM, Feng J, Xu GJ, Liu XB, Jiang H, Niu CY, Zhao ZG (2012) Changes of blood viscosity and erythrocyte rheology in acute hypoxic hypoxia mices. Chin J Appl Physiol 28:454–457
Zolla L, D’Alessandro A (2013) An efficient apparatus for rapid deoxygenation of erythrocyte concentrates for alternative banking strategies. J Blood Transfusion 2013:896537
Acknowledgments
We are grateful to the two referees for their constructive comments and criticism. This work was partially funded by a bilateral Cyprus–Slovenia grant from the Cyprus Research Promotion Foundation and the Slovenia Research Agency under the program “DESMI 2009–2010” (Title: The fluidity of blood at different levels of oxygen content; Project: DIAKRATIKES/KY-SLO/0411/02) of the framework program “for research, technological development and innovation 2009–2010” co-funded by the Republic of Cyprus and the European Regional Development Fund.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Valant, A.Z., Ziberna, L., Papaharilaou, Y. et al. The influence of oxygen concentration on the rheological properties and flow of whole human blood. Rheol Acta 55, 921–933 (2016). https://doi.org/10.1007/s00397-016-0967-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00397-016-0967-y