Skip to main content
Log in

Wall Shear Stress Measurements in an Arterial Flow Bioreactor

  • Published:
Cardiovascular Engineering and Technology Aims and scope Submit manuscript

Abstract

In vitro arterial flow bioreactor systems are widely used in tissue engineering to investigate response of endothelial cells to shear. However, the assumption that such models reproduce physiological flow has not been experimentally tested. Furthermore, shear stresses experienced by the endothelium are generally calculated using a Poiseuille flow assumption. Understanding the performance of flow bioreactor systems is of great importance, since interpretation of biological responses hinges on the fidelity of such systems and the validity of underlying assumptions. Here we test the physiologic reliability of arterial flow bioreactors and the validity of the Poiseuille assumption for a typical system used in tissue engineering. A particle image velocimetry system was employed to experimentally measure the flow within the vessel with high spatial and temporal resolution. Two types of vessels were considered: first, fluorinated ethylene propylene (FEP) tubing representative of a human artery without cells; and second, FEP tubing with a confluent layer of endothelial cells on the vessel lumen. Instantaneous wall shear stress (WSS), time-averaged WSS, and oscillatory shear index were computed from velocity field measurements and compared between cases. The flow patterns and resulting wall shear were quantitatively determined to not accurately reproduce physiological flow, and that the Poiseuille flow assumption was found to be invalid. This work concludes that analysis of cell response to hemodynamic parameters using such bioreactors should be accompanied by corresponding flow measurements for accurate quantification of fluid stresses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

E :

Tensile modulus

C :

Compliance

Re :

Reynolds number

α :

Womersley number

u avg :

Average flow velocity

D :

Vessel diameter

ν :

Kinematic viscosity

ω :

Pulse frequency

n :

Index of refraction

μ :

Dynamic viscosity

τ w(x,t):

Instantaneous wall shear stress

\( \overline{{\tau_{\text{w}} }} \left( x \right) \) :

Time-averaged wall shear stress

ε:

Measurement uncertainty

OSI:

Oscillatory shear index

N t :

Number of time points

T :

Cycle period

P :

Pressure

Q :

Volumetric flow rate

t i :

Cycle interval

x*:

Nondimensionalized axial position

y*:

Nondimensionalized radial position

R c :

Reverse coefficient

L e :

Entrance length

PIV:

Particle image velocimetry

HMEC:

Human microvascular endothelial cells

FEP:

Fluorinated ethylene propylene

WSS:

Wall shear stress

References

  1. Adrian, R. J. Particle-imaging techniques for experimental fluid-mechanics. Ann. Rev. Fluid Mech. 23:261–304, 1991.

    Article  Google Scholar 

  2. Adrian, R. J. Twenty years of particle image velocimetry. Exp. Fluids 39(2):159–169, 2005.

    Article  Google Scholar 

  3. Atabek, H. B., and C. C. Chang. Oscillatory flow near the entry of a circular tube. Zeitschrift für Angewandte Mathematik und Physik (ZAMP) 12(3):185–201, 1961.

    Article  MathSciNet  MATH  Google Scholar 

  4. Bowlin, G. L., M. J. McClure, S. A. Sell, and D. G. Simpson. Electrospun polydioxanone, elastin, and collagen vascular scaffolds: uniaxial cyclic distension. J. Eng. Fiber. Fabr. 4(2):18–25, 2009.

    Google Scholar 

  5. Califano, J. P., and C. A. Reinhart-King. Exogenous and endogenous force regulation of endothelial cell behavior. J. Biomech. 43(1):79–86, 2010.

    Article  Google Scholar 

  6. Charonko, J. Studies of Stented Arteries and Left Ventricular Diastolic Dysfunction Using Experimental and Clinical Analysis with Data Augmentation. Dissertation, Blacksburg: Virginia Polytechnic Institute and State University, 2009.

  7. Charonko, J., S. Karri, J. Schmieg, S. Prabhu, and P. Vlachos. In vitro, time-resolved PIV comparison of the effect of stent design on wall shear stress. Ann. Biomed. Eng. 37(7):1310–1321, 2009.

    Article  Google Scholar 

  8. Coleman, H. W., and W. G. Steele. Experimentation, Validation, and Uncertainty Analysis for Engineers (3rd ed.). Hoboken, NJ: John Wiley & Sons, 2009.

    Book  Google Scholar 

  9. Conklin, B. S., S. M. Surowiec, P. H. Lin, and C. Y. Chen. A simple physiologic pulsatile perfusion system for the study of intact vascular tissue. Med. Eng. Phys. 22(6):441–449, 2000.

    Article  Google Scholar 

  10. Dodge, J. T., B. G. Brown, E. L. Bolson, and H. T. Dodge. Lumen diameter of normal human coronary-arteries—influence of age, sex, anatomic variation, and left-ventricular hypertrophy or dilation. Circulation 86(1):232–246, 1992.

    Google Scholar 

  11. DuPont, A. DuPont FEP Fluorocarbon Film. Properties Bulletin, 2010, p. 4.

  12. Durst, F., J. C. F. Pereira, and C. Tropea. The plane symmetrical sudden-expansion flow at low Reynolds-numbers. J. Fluid. Mech. 248:567–581, 1993.

    Article  Google Scholar 

  13. Eckstein, A., and P. P. Vlachos. Digital particle image velocimetry (DPIV) robust phase correlation. Meas. Sci. Technol. 20(5):055401, 2009.

    Google Scholar 

  14. Eckstein, A., and P. P. Vlachos. Assessment of advanced windowing techniques for digital particle image velocimetry (DPIV). Meas. Sci. Technol. 20(7):075402, 2009.

    Google Scholar 

  15. Eckstein, A. C., J. Charonko, and P. Vlachos. Phase correlation processing for DPIV measurements. Exp. Fluids 45(3):485–500, 2008.

    Article  Google Scholar 

  16. Fung, Y. C. Biomechanics: Circulation (2nd ed.). New York: Springer, 1997.

    Google Scholar 

  17. Geddes, L. A., R. Roeder, J. Wolfe, N. Lianakis, T. Hinson, and J. Obermiller. Compliance, elastic modulus, and burst pressure of small-intestine submucosa (SIS), small-diameter vascular grafts. J. Biomed. Mater. Res. 47(1):65–70, 1999.

    Article  Google Scholar 

  18. He, X. Y., and D. N. Ku. Unsteady entrance flow development in a straight tube. J. Biomech. Eng.-T. ASME 116(3):355–360, 1994.

    Article  Google Scholar 

  19. Ikada, Y. Tissue Engineering: Fundamentals and Applications. 1st ed. Interface Science and Technology, Vol. 8. Boston: Academic Press/Elsevier Amsterdam, 2006.

    Google Scholar 

  20. Kadja, M., D. Touzopoulos, and G. Bergeles. Numerical investigation of bifurcation phenomena occurring in flows through planar sudden expansions. Acta Mech. 153(1–2):47–61, 2002.

    Article  MATH  Google Scholar 

  21. Karri, S., J. Charonko, and P. P. Vlachos. Robust wall gradient estimation using radial basis functions and proper orthogonal decomposition (POD) for particle image velocimetry (PIV) measured fields. Meas. Sci. Technol. 20(4):045401, 2009.

    Google Scholar 

  22. Karri, S., and P. P. Vlachos. Time-resolved DPIV investigation of pulsatile flow in symmetric stenotic arteries effects of phase angle. J. Biomech. Eng.-T. ASME 132(3):031010, 2010.

    Google Scholar 

  23. Kleinstreuer, C., S. Hyun, J. R. Buchanan, P. W. Longest, J. P. Archie, and G. A. Truskey. Hemodynamic parameters and early intimal thickening in branching blood vessels. Crit. Rev. Biomed. Eng. 29(1):1–64, 2001.

    Google Scholar 

  24. Ku, D. N. Blood flow in arteries. Ann. Rev. Fluid Mech. 29:399–434, 1997.

    Article  MathSciNet  Google Scholar 

  25. Kumar, V., L. Brewster, J. Caves, and E. Chaikof. Tissue engineering of blood vessels: functional requirements, progress, and future challenges. Cardiovasc. Eng. Technol. 2(3):137–148, 2011.

    Article  Google Scholar 

  26. Lee, S. J., J. Liu, S. H. Oh, S. Soker, A. Atala, and J. J. Yoo. Development of a composite vascular scaffolding system that withstands physiological vascular conditions. Biomaterials 29(19):2891–2898, 2008.

    Article  Google Scholar 

  27. Levesque, M. J., R. M. Nerem, and E. A. Sprague. Vascular endothelial-cell proliferation in culture and the influence of flow. Biomaterials 11(9):702–707, 1990.

    Article  Google Scholar 

  28. Lin, P. H., C. Y. Chen, S. M. Surowiec, B. Conklin, R. L. Bush, E. L. Chaikof, et al. A porcine model of carotid artery thrombosis for thrombolytic therapy and angioplasty: Application of PTFE graft-induced stenosis. J. Endovasc. Ther. 7(3):227–235, 2000.

    Article  Google Scholar 

  29. Mironov, V., V. Kasyanov, K. McAllister, S. Oliver, J. Sistino, and R. Markwald. Perfusion bioreactor for vascular tissue engineering with capacities for longitudinal stretch. J. Craniofac. Surg. 14(3):340–347, 2003.

    Article  Google Scholar 

  30. Poelma, C., P. Vennemann, R. Lindken, and J. Westerweel. In vivo blood flow and wall shear stress measurements in the vitelline network. Exp. Fluids 45(4):703–713, 2008.

    Article  Google Scholar 

  31. Raffel, M. Particle Image Velocimetry: A Practical Guide (2nd ed.). Heidelberg: Springer, 2007.

    Google Scholar 

  32. Reneman, R. S., T. Arts, and A. P. G. Hoeks. Wall shear stress—an important determinant of endothelial cell function and structure—in the arterial system in vivo. J. Vasc. Res. 43(3):251–269, 2006.

    Article  Google Scholar 

  33. Roy, S., P. Silacci, and N. Stergiopulos. Biomechanical proprieties of decellularized porcine common carotid arteries. Am. J. Physiol. Heart Circ. Physiol. 289(4):H1567–H1576, 2005.

    Article  Google Scholar 

  34. Takizawa, K., C. Moorman, S. Wright, J. Christopher, and T. E. Tezduyar. Wall shear stress calculations in space-time finite element computation of arterial fluid-structure interactions. Comput. Mech. 46(1):31–41, 2010.

    Article  MathSciNet  MATH  Google Scholar 

  35. Westerweel, J. Fundamentals of digital particle image velocimetry. Meas. Sci. Technol. 8(12):1379–1392, 1997.

    Article  Google Scholar 

  36. Westerweel, J., D. Dabiri, and M. Gharib. The effect of a discrete window offset on the accuracy of cross-correlation analysis of digital PIV recordings. Exp. Fluids 23(1):20–28, 1997.

    Article  Google Scholar 

  37. Westerweel, J., and F. Scarano. Universal outlier detection for PIV data. Exp. Fluids 39(6):1096–1100, 2005.

    Article  Google Scholar 

  38. Yazdani, S., and J. Berry. Development of an in vitro system to assess stent-induced smooth muscle cell proliferation: a feasibility study. J. Vasc. Interv. Radiol. 20:101–106, 2009.

    Article  Google Scholar 

  39. Yazdani, S. K., B. W. Tillman, J. L. Berry, S. Soker, and R. L. Geary. The fate of an endothelium layer after preconditioning. J. Vasc. Surg. 51(1):174–183, 2010.

    Article  Google Scholar 

Download references

Acknowledgments

Funding for this project was provided by the Clare Boothe Luce Graduate Fellowship (EEV), Virginia Space Grant Consortium Graduate STEM Research Fellowship (EEV), National Institutes of Health/National Heart, Lung, and Blood Institute R01HL098912 (MNR), National Science Foundation CAREER Award CBET 0955072 (MNR), and National Science Foundation CAREER Award CBET 0547434 (PPV).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pavlos P. Vlachos.

Additional information

Associate Editor Ajit P. Yoganathan oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Voigt, E.E., Buchanan, C.F., Nichole Rylander, M. et al. Wall Shear Stress Measurements in an Arterial Flow Bioreactor. Cardiovasc Eng Tech 3, 101–111 (2012). https://doi.org/10.1007/s13239-011-0076-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13239-011-0076-0

Keywords

Navigation