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Microbubble moving in blood flow in microchannels: effect on the cell-free layer and cell local concentration

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Abstract

Gas embolisms can hinder blood flow and lead to occlusion of the vessels and ischemia. Bubbles in microvessels circulate as tubular bubbles (Taylor bubbles) and can be trapped, blocking the normal flow of blood. To understand how Taylor bubbles flow in microcirculation, in particular, how bubbles disturb the blood flow at the scale of blood cells, experiments were performed in microchannels at a low Capillary number. Bubbles moving with a stream of in vitro blood were filmed with the help of a high-speed camera. Cell-free layers (CFLs) were observed downstream of the bubble, near the microchannel walls and along the centerline, and their thicknesses were quantified. Upstream to the bubble, the cell concentration is higher and CFLs are less clear. While just upstream of the bubble the maximum RBC concentration happens at positions closest to the wall, downstream the maximum is in an intermediate region between the centerline and the wall. Bubbles within microchannels promote complex spatio-temporal variations of the CFL thickness along the microchannel with significant relevance for local rheology and transport processes. The phenomenon is explained by the flow pattern characteristic of low Capillary number flows. Spatio-temporal variations of blood rheology may have an important role in bubble trapping and dislodging.

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References

  • M. D. Abramoff, P. J. Magalhaes, S. J. Ram, Image processing with ImageJ. Biophoton. Int. 11(7), 36–42 (2004)

    Google Scholar 

  • Y. Abu-Omar, L. Balacumaraswami, D. W. Pigott, P. M. Matthews, D. P. Taggart, Solid and gaseous cerebral microembolization during off-pump, on-pump, and open cardiac surgery procedures. J. Thorac. Cardiovasc. Surg. 127(6), 1759–1765 (2004)

    Article  Google Scholar 

  • P. Angeli, A. Gavriilidis, Hydrodynamics of Taylor flow in small channels: a review. Proc. Inst. Mech. Eng. C J. Mech. Eng. Sci. 222(5), 737–751 (2008)

    Article  Google Scholar 

  • D. A. Bartholomeusz, R. W. Boutte, J. D. Andrade, Xurography: rapid prototyping of microstructures using a cutting plotter. J. Microelectromech. Syst. 14(6), 1364–1374 (2005)

    Article  Google Scholar 

  • M. D. Bischel, B. G. Scoles, J. G. Mohler, Evidence for pulmonary microembolization during hemodialysis. CHEST Journal 67(3), 335–337 (1975)

    Article  Google Scholar 

  • M. A. Borger, C. M. Peniston, R. D. Weisel, M. Vasiliou, R. E. A. Green, C. M. Feindel, Neuropsychologic impairment after coronary bypass surgery: effect of gaseous microemboli during perfusionist interventions. J. Thorac. Cardiovasc. Surg. 121(4), 743–749 (2001)

    Article  Google Scholar 

  • A. B. Branger, D. M. Eckmann, Accelerated arteriolar gas embolism reabsorption by an exogenous surfactant. Anesthesiology 96(4), 971–979 (2002)

    Article  Google Scholar 

  • N. Bumseok, H. L. Leo K. Sangho, Physiological significance of cell-free layer and experimental determination of its width in mi-crocirculatory vessels, in Visualization and simulation of complex flows in biomedical engineering, ed. by R. lima, T. Ishikawa, Y. Imai, M. S. N. Oliveira (Springer, Dordrecht, 2014), pp. 75–87

  • A. J. Calderón, Y. S. Heo, D. Huh, N. Futai, S. Takayama, J. B. Fowlkes, J. L. Bull, Microfluidic model of bubble lodging in microvessel bifurcations, Appl. Phys. Lett. 89(24), 244103–3 (2006)

  • G. Deklunder, M. Roussel, J.-L. Lecroart, A. Prat, C. Gautier, Microemboli in cerebral circulation and alteration of cognitive abilities in patients with mechanical prosthetic heart valves. Stroke 29(9), 1821–1826 (1998)

    Article  Google Scholar 

  • V. Doyeux, T. Podgorski, S. Peponas, M. Ismail, G. Coupier, Spheres in the vicinity of a bifurcation: elucidating the Zweifach–Fung effect. J. Fluid Mech. 674, 359–388 (2011)

    Article  MathSciNet  MATH  Google Scholar 

  • D. C. Duffy, J. C. McDonald, O. J. Schueller, G. M. Whitesides, Rapid prototyping of microfluidic systems in poly (dimethylsiloxane), Anal. Chem. 70(23), 4974–4984 (1998)

  • D. M. Eckmann, J. I. E. Zhang, J. Lampe, P. S. Ayyaswamy, Gas embolism and surfactant-based intervention. Ann. N. Y. Acad. Sci. 1077(1), 256–269 (2006)

    Article  Google Scholar 

  • B. Eshpuniyani, J. B. Fowlkes, J. L. Bull, A bench top experimental model of bubble transport in multiple arteriole bifurcations. Int. J. Heat Fluid Flow 26(6), 865–872 (2005)

    Article  Google Scholar 

  • R. Fåhraeus, The suspension stability of the blood. Physiol. Rev. 9(2), 241–274 (1929)

    Google Scholar 

  • R. Fåhræus, T. Lindqvist, The viscosity of the blood in narrow capillary tubes. Am. J. Phys. 96(3), 562–568 (1931)

    Google Scholar 

  • M. Faivre, M. Abkarian, K. Bickraj, H. A. Stone, Geometrical focusing of cells in a microfluidic device: an approach to separate blood plasma. Biorheology 43(2), 147–159 (2006)

    Google Scholar 

  • V. Faustino, S. O. Catarino, R. Lima, G. Minas, Biomedical microfluidic devices by using low-cost fabrication techniques: a review. J. Biomech. 49(11), 2280–2292 (2016)

    Article  Google Scholar 

  • L. K. Fiddes, N. Raz, S. Srigunapalan, E. Tumarkan, C. A. Simmons, A. R. Wheeler, E. Kumacheva, A circular cross-section PDMS microfluidics system for replication of cardiovascular flow conditions. Biomaterials 31(13), 3459–3464 (2010)

    Article  Google Scholar 

  • P. P. Foster, B. D. Butler, Decompression to altitude: assumptions, experimental evidence, and future directions. J. Appl. Physiol. 106(2), 678–690 (2009)

    Article  Google Scholar 

  • Y.-C. Fung, Stochastic flow in capillary blood vessels. Microvasc. Res. 5(1), 34–48 (1973)

    Article  MathSciNet  Google Scholar 

  • V. Garcia, R. Dias, R. Lima, In vitro blood flow behaviour in microchannels with simple and complex geometries, in Applied Biological Engineering – Principles and Practice, ed. by G. R. Naik (InTech, Rijeka, 2012), pp. 393–416

  • T. Ishikawa, H. Fujiwara, N. Matsuki, T. Yoshimoto, Y. Imai, H. Ueno, T. Yamaguchi, Asymmetry of blood flow and cancer cell adhesion in a microchannel with symmetric bifurcation and confluence. Biomed. Microdevices 13(1), 159–167 (2011)

    Article  Google Scholar 

  • L. L. Karlsson, S. L. Blogg, P. Lindholm, M. Gennser, T. Hemmingsson, D. Linnarsson, Venous gas emboli and exhaled nitric oxide with simulated and actual extravehicular activity. Respir. Physiol. Neurobiol. 169, 315–322 (2009)

    Article  Google Scholar 

  • V. Leble, R. Lima, R. Dias, C. Fernandes, T. Ishikawa, Y. Imai, T. Yamaguchi, Asymmetry of red blood cell motions in a microchannel with a diverging and converging bifurcation, Biomicrofluidics 5(4), 044120–15 (2011)

  • R. Lima, M. Nakamura, T. Omori, T. Ishikawa, S. Wada, T. Yamaguchi, Microscale flow dynamics of red blood cells in microchannels: an experimental and numerical analysis, in Advances in Computational Vision and Medical Image Processing: Methods and Applications, ed. by T. a. Jorge (Springer, Dordrecht, 2009a), pp. 203–220

  • R. Lima, M. S. Oliveira, T. Ishikawa, H. Kaji, S. Tanaka, M. Nishizawa, T. Yamaguchi, Axisymmetric polydimethysiloxane microchannels for in vitro hemodynamic studies, Biofabrication 1(3), 035005 (2009b)

  • N. Maeda, Erythrocyte rheology in microcirculation. The Japanese Journal of Physiology 46(1), 1–14 (1996)

    Article  MathSciNet  Google Scholar 

  • G. Mchedlishvili, N. Maeda, Blood flow structure related to red cell flow: determinant of blood fluidity in narrow microvessels. The Japanese Journal of Physiology 51(1), 19–30 (2001)

    Article  Google Scholar 

  • E. Meijering, O. Dzyubachyk, I. Smal, Methods for cell and particle tracking. Methods Enzymol. 504(9), 183–200 (2012)

    Article  Google Scholar 

  • S. Milo, E. Rambod, C. Gutfinger, M. Gharib, Mitral mechanical heart valves: in vitro studies of their closure, vortex and microbubble formation with possible medical implications. Eur. J. Cardiothorac. Surg. 24(3), 364–370 (2003)

    Article  Google Scholar 

  • C. M. Muth, E. S. Shank, Gas embolism. N. Engl. J. Med. 342, ‘ (2000)

    Article  Google Scholar 

  • V. Papadopoulou, R. J. Eckersley, C. Balestra, T. D. Karapantsios, M.-X. Tang, A critical review of physiological bubble formation in hyperbaric decompression. Adv. Colloid Interf. Sci. 191–192, 22–30 (2013)

  • V. Papadopoulou, M. X. Tang, C. Balestra, R. J. Eckersley, T. D. Karapantsios, Circulatory bubble dynamics: from physical to biological aspects. Adv. Colloid Interf. Sci. 206, 239–249 (2014)

  • D. Pinho, T. Yaginuma, R. Lima, A microfluidic device for partial cell separation and deformability assessment. Biochip Journal 7(4), 367–374 (2013)

    Article  Google Scholar 

  • E. Pinto, V. Faustino, R. Rodrigues, D. Pinho, V. Garcia, J. Miranda, R. Lima, A rapid and low-cost Nonlithographic method to fabricate biomedical microdevices for blood flow analysis. Micromachines 6(1), 121–135 (2015)

    Article  Google Scholar 

  • S. Samuel, A. Duprey, M. L. Fabiilli, J. L. Bull, J. Brian Fowlkes, In Vivo microscopy of targeted vessel occlusion employing acoustic droplet vaporization. Microcirculation 19(6), 501–509 (2012)

    Article  Google Scholar 

  • E. Sollier, M. Cubizolles, Y. Fouillet, J.-L. Achard, Fast and continuous plasma extraction from whole human blood based on expanding cell-free layer devices. Biomed. Microdevices 12(3), 485–497 (2010)

    Article  Google Scholar 

  • A. Suzuki, S. C. Armstead, D. M. Eckmann, Surfactant reduction in embolism bubble adhesion and endothelial damage. Anesthesiology 101(1), 97–103 (2004)

    Article  Google Scholar 

  • K. Svanes, B. W. Zweifach, Variations in small blood vessel hematocrits produced in hypothermic rats by micro-occlusion. Microvasc. Res. 1(2), 210–220 (1968)

    Article  Google Scholar 

  • T. Taha, Z. Cui, Hydrodynamics of slug flow inside capillaries. Chem. Eng. Sci. 59(6), 1181–1190 (2004)

    Article  Google Scholar 

  • T. Taha, Z. F. Cui, CFD modelling of slug flow inside square capillaries. Chem. Eng. Sci. 61(2), 665–675 (2006)

    Article  Google Scholar 

  • V. Talimi, Y. Muzychka, S. Kocabiyik, A review on numerical studies of slug flow hydrodynamics and heat transfer in microtubes and microchannels. Int. J. Multiphase Flow 39, 88–104 (2012)

    Article  Google Scholar 

  • T. Thulasidas, M. Abraham, R. Cerro, Flow patterns in liquid slugs during bubble-train flow inside capillaries. Chem. Eng. Sci. 52(17), 2947–2962 (1997)

    Article  Google Scholar 

  • D. Valassis, R. Dodde, B. Esphuniyani, J. B. Fowlkes, J. Bull, Microbubble transport through a bifurcating vessel network with pulsatile flow. Biomed. Microdevices 14(1), 131–143 (2012)

    Article  Google Scholar 

  • T. Yaginuma, M. S. Oliveira, R. Lima, T. Ishikawa, T. Yamaguchi, Human red blood cell behavior under homogeneous extensional flow in a hyperbolic-shaped microchannel. Biomicrofluidics 7(5), 054110–14 (2013)

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Acknowledgements

The authors acknowledge the financial support provided by PTDC/SAU-BEB/105650/2008, PTDC/SAU-ENB/116929/2010, EXPL/EMS-SIS/2215/2013 and PTDC/QEQ-FTT/4287/2014 from FCT (Science and Technology Foundation), COMPETE, QREN and European Union (FEDER).

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Correspondence to João M. Miranda.

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David Bento and Lúcia Sousa contributed equally to the manuscript.

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Bento, D., Sousa, L., Yaginuma, T. et al. Microbubble moving in blood flow in microchannels: effect on the cell-free layer and cell local concentration. Biomed Microdevices 19, 6 (2017). https://doi.org/10.1007/s10544-016-0138-z

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