Swinging of Red Blood Cells under Shear Flow

Abkarian, Manouk; Faivre, Magalie; Viallat, Annie

doi:10.1103/physrevlett.98.188302

Cited by 315 publications

(470 citation statements)

References 21 publications

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“…The length variation of the long cell axis is less than 10% for the entire studied range of shear stresses. This behavior was not highlighted in previous experimental studies, but previously published pictures already suggested it (7,18). We show it clearly by visualizing on the same sequence the rotation of a small bead attached to the membrane and the presence of a dimple on the shape.…”

Section: Resultsmentioning

confidence: 50%

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confidence: 99%

“…The Keller and Skalak (KS) analytical model (21), which describes an RBC as a viscous ellipsoid of fixed shape, qualitatively recovers (T), (TT) as a function of λ. However, recent experiments revealed new dynamic states specifically due to the shear elasticity and the shape memory of the red cell membrane (7,8): (i) swinging superimposed to tank-treading, in which the cell's inclination angle changes periodically relative to the direction of flow (S); (ii) intermittency, in which the cell alternately Ts and TTs when it undergoes a TT-to-T transition driven by the shear rate, _ γ; and (iii) chaotic motion in a time-periodic flow (8). The KS model modified to account for membrane elasticity and shape memory, developed by Abkarian et al (AFV) (7) and by Skotheim and Secomb (SS) (14), semiquantitatively recovers these dynamic states and their transition.…”

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Full dynamics of a red blood cell in shear flow

Dupire

Socol

Viallat

2012

Proc. Natl. Acad. Sci. U.S.A.

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263

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At the cellular scale, blood fluidity and mass transport depend on the dynamics of red blood cells in blood flow, specifically on their deformation and orientation. These dynamics are governed by cellular rheological properties, such as internal viscosity and cytoskeleton elasticity. In diseases in which cell rheology is altered genetically or by parasitic invasion or by changes in the microenvironment, blood flow may be severely impaired. The nonlinear interplay between cell rheology and flow may generate complex dynamics, which remain largely unexplored experimentally. Under simple shear flow, only two motions, "tumbling" and "tank-treading," have been described experimentally and relate to cell mechanics. Here, we elucidate the full dynamics of red blood cells in shear flow by coupling two videomicroscopy approaches providing multidirectional pictures of cells, and we analyze the mechanical origin of the observed dynamics. We show that contrary to common belief, when red blood cells flip into the flow, their orientation is determined by the shear rate. We discuss the "rolling" motion, similar to a rolling wheel. This motion, which permits the cells to avoid energetically costly deformations, is a true signature of the cytoskeleton elasticity. We highlight a hysteresis cycle and two transient dynamics driven by the shear rate: an intermittent regime during the "tank-treading-to-flipping" transition and a Frisbee-like "spinning" regime during the "rolling-to-tank-treading" transition. Finally, we reveal that the biconcave red cell shape is highly stable under moderate shear stresses, and we interpret this result in terms of stress-free shape and elastic buckling. . Its fluidity strongly depends on its behavior in flow, which is a key factor of proper tissue perfusion. At the cellular scale, blood flow behavior is affected primarily by the RBC response to the hydrodynamic stress in terms of cell orientation relative to the flow direction and of cell deformation. For example, on one hand, at low shear rates, similar cell orientations may favor the formation of stacks (rouleaux) (1) of RBCs, like rolls of coins, which increases blood viscosity. On the other hand, at high shear rates, the individualization of RBCs, their alignment, and their stretching in the flow (2) decrease blood viscosity (3). The orientation and the deformation in flow of RBCs are governed by their rheological properties. They result from the viscoelastic contributions of all components of the cell composite structure. Moreover, RBC rheological properties also depend on the microenvironment and on metabolic functionality (4). Both local and systemic disturbances of homeostasis (in diabetes mellitus, hypertension) have the potential to induce RBC rheological alterations and consequently to impair blood circulation. It therefore is crucial to understand the relationships between the rheological properties of RBCs and their orientation and deformation in flow. This question is far from trivial because even in a simple shear flow, RBCs present a v...

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Section: Resultsmentioning

confidence: 50%

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confidence: 99%

mentioning

confidence: 99%

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Full dynamics of a red blood cell in shear flow

Dupire

Socol

Viallat

2012

Proc. Natl. Acad. Sci. U.S.A.

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263

266

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“…Observations of RBC dynamics in microtubes (12) and rheoscopes (13) realized during the 1970s and 1980s have led to the foundation of the current paradigm for shear thinning, supporting an emulsion analogy for blood rheology inherited from the 1960s (1, 2). Although at low shear stresses (less than about 0.05 Pa) single RBCs flip like a coin, they reach a steady orientation for increasing flow strength (13,14) allowed by a tank-tread-like circulation of their membrane (13). Such dropletlike behavior should effectively assist the flow by minimizing disturbances to streamlines and has been successfully used to deduce some mechanical properties of RBC membrane in dilute conditions (15,16).…”

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Red cells’ dynamic morphologies govern blood shear thinning under microcirculatory flow conditions

Lanotte

Mauer

Mendez

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Blood viscosity decreases with shear stress, a property essential for an efficient perfusion of the vascular tree. Shear thinning is intimately related to the dynamics and mutual interactions of RBCs, the major component of blood. Because of the lack of knowledge about the behavior of RBCs under physiological conditions, the link between RBC dynamics and blood rheology remains unsettled. We performed experiments and simulations in microcirculatory flow conditions of viscosity, shear rates, and volume fractions, and our study reveals rich RBC dynamics that govern shear thinning. In contrast to the current paradigm, which assumes that RBCs align steadily around the flow direction while their membranes and cytoplasm circulate, we show that RBCs successively tumble, roll, deform into rolling stomatocytes, and, finally, adopt highly deformed polylobed shapes for increasing shear stresses, even for semidilute volume fractions of the microcirculation. Our results suggest that any pathological change in plasma composition, RBC cytosol viscosity, or membrane mechanical properties will affect the onset of these morphological transitions and should play a central role in pathological blood rheology and flow behavior.

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“…For example, motion of red blood cells (RBCs) under viscous shear flow is characterized by the "tank-treading motion": It is steady membrane rotation with constant shape and inclination angle, and tumbling motion is observed as a rotational oscillation of the entire cell accompanied by tank treading motion. 3 The rotational motion, which is principally due to the cell membrane and occurs around the cell axis, has very low frequencies, f L of about 1 -5 Hz. 4 Another type of motion is the electro-rotation: When a colloidal (or bio-colloidal) solution is subjected to an external ac-electric field, the micro-particles will rotate by electro-rotation mechanism.…”

Section: Introductionmentioning

confidence: 99%

Effect of erythrocytes oscillations on dielectric properties of human diabetic-blood

Abdalla

2011

AIP Advances

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It has been demonstrated that the erythrocytes (RBCs) oscillate during their tank-treading motion with high-frequency oscillations. This oscillatory motion drastically affects the dielectric and electrical properties of RBCs. Moreover, the glucose level in blood affects the electrical and dielectric properties of blood. It has been, also, shown that the frequency of these oscillations exponentially decrease from 1.2 MHz down to 0.85 MHz with variation of glucose level from 85 mg/dL up to 346.1 mg/dL. It is expected that these oscillations strongly affect the general physiological properties of blood and would stimulate the curiosity of scientists and bioengineers to present new, more efficient, rapid, safe and viable diagnostic and/or therapeutic methods for blood disorders; in particular diabetes

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Swinging of Red Blood Cells under Shear Flow

Cited by 315 publications

References 21 publications

Full dynamics of a red blood cell in shear flow

Full dynamics of a red blood cell in shear flow

Red cells’ dynamic morphologies govern blood shear thinning under microcirculatory flow conditions

Effect of erythrocytes oscillations on dielectric properties of human diabetic-blood

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