Flow patterns and endothelial cell morphology in a simplified model of an artificial ventricle

Abstract

The aim of this study was to delineate the flow patterns in a non-unidirectional flow field inside a ventricle-shaped cell culture chamber, and examine the resulting morphology and integrity of the endothelium in select regions of the monolayer. The chamber was perfused by pulsatile flow, and the coherent motion of the fluid was studied using flow visualization aided by image analysis. Four distinct flow patterns were discerned and examined: central jet, flow impingement, flow separation, and recirculating eddies. The influence of these patterns on endothelial cell morphology was assessed after 20 h of exposure to flow. There were no signs of damage to the endothelium in the jet region nor was there evidence of cell alignment with the flow. Yet, there were changes in cell morphology and cytoskeletal architecture as compared to control. By contrast, within the eddies where the flow was highly disturbed, there was apparent damage to the endothelium. Thus, exposure of cells to random velocity fluctuations in regions of quasi-static flow compromises the integrity of the monolayer. Identification of such sites and acquisition of the knowledge necessary to protect the cells from denudation will be valuable for the endothelialization efforts of cardiac prostheses.

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References

  1. 1.

    Grasel, T. G. and Cooper, S. L. (1986) Surface properties and blood compatibility of polyurethaneureas.Biomaterials 7, 315–328.

    PubMed  Article  CAS  Google Scholar 

  2. 2.

    Gimbrone, M. A., Jr., (1987) Vascular endothelium: nature's blood-compatible container.Ann. NY Acad. Sci. 516, 5–11.

    PubMed  Article  Google Scholar 

  3. 3.

    Rupnick, M. A., Hubbard, F. A., Pratt, K., Jarrell, B. E., and Williams, S. K. (1991) Endothelialization of vascular prosthetic surfaces after seeding or sodding with human microvascular endothelial cells.J. Vasc. Surg. 9, 788–795.

    Article  Google Scholar 

  4. 4.

    Lelkes, P. I. and Samet, M. M. (1991) Endothelialization of the luminal sac in artificial cardiac prostheses: a challenge for both biologists and engineers.J. Biomech. Eng. 113, 132–142.

    PubMed  CAS  Google Scholar 

  5. 5.

    Wechezak, A. R., Viggers, R. F., Sauvage, L. R., and Mansfield, P. B. (1984) Endothelial cell rounding associated with long-term implantations of left ventricular assist devices.Scan. Elect. Microscopy 3, 1353–1360.

    Google Scholar 

  6. 6.

    Lelkes, P. I., Samet, M. M., Christensen, C. W., and Amrani, D. L. (1992) Factitious angiogenesis: endothelialization of artificial cardiovascular prostheses, inAngiogenesis in Health and Disease (Maragoudakis, M. E., Gullino, P. and Lelkes, P. I., eds.), Plenum, New York, pp. 339–353.

    Google Scholar 

  7. 7.

    Zilla, P., Fasol, R., Grimm, M., Fischlein, T., Eberl, T., Preiss, P., Krupicka, O., von Oppell, U., and Deutsch, M. (1991) Growth properties of cultured human endothelial cells on differently coated artificial heart materials.J. Thorac. Cardiovasc. Surg. 101, 671–680.

    PubMed  CAS  Google Scholar 

  8. 8.

    Flaherty, J. T., Pierce, J. E., Ferrans, V. J., Patel, D. J., Tucker, K., and Fry, D. L. (1972) Endothelial nuclear patterns in the canine arterial tree with particular reference to hemodynamic events.Circ. Res. 30, 23–33.

    PubMed  CAS  Google Scholar 

  9. 9.

    Kim, D. W., Gotlieb, A., and Langille, B. L. (1989) In vivo modulation of endothelial F-actin microfilaments by experimental alterations in shear stress.Arteriosclerosis 9, 439–445.

    PubMed  CAS  Google Scholar 

  10. 10.

    Nerem, R. M., Levesque, M. J., and Sato, M. (1986) Vascular dynamics and the endothelium, inFrontiers in Biomechanics. (Schmid-Schonbein, G. W., Woo, S. L.-Y., and Zweifach, B. W., eds.), Springer-Verlag, New York, pp. 324–341.

    Google Scholar 

  11. 11.

    Davies, P. F., Remuzzi, A., Gordon, E. J., Dewey, C. F., Jr., and Gimbrone, M. A., Jr. (1986) Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro.Proc. Natl. Acad. Sci. USA 83, 2114–2117.

    PubMed  Article  CAS  Google Scholar 

  12. 12.

    Helmlinger, G., Geiger, R. V., Schreck, S., and Nerem, R. M. (1991) Effects of pulsatile flow on cultured vascular endothelial cell morphology.J. Biomech. Eng. 113, 123–131.

    PubMed  CAS  Google Scholar 

  13. 13.

    Diamond, S. L., Eskin, S. G., and McIntire, L. V. (1989) Fluid flow stimulates tissue plasminogen activator secretion by cultured human endothelial cells.Science 243, 1483–1485.

    PubMed  Article  CAS  Google Scholar 

  14. 14.

    Macoviak, J. A., Dasse, K. A., and Poirier, V. L. (1986) Mechanical cardiac assistance and replacement.Cardiology Clinics 8, 39–53.

    Google Scholar 

  15. 15.

    Ku, D. N. and Zhu, C. (1993) The mechanical environment of the artery, inHemodynamic Forces and Vascular Cell Biology, 2nd Ed. (Sumpio, B. E., ed.), Landes, Austin, TX, pp. 1–23.

    Google Scholar 

  16. 16.

    Samet, M. M. and Lelkes, P. I. (1994) Pulsatile flow and endothelial cell morphology in a cell culture chamber model of an artificial cardiac ventricle.J. Biomech. Eng. (in press).

  17. 17.

    Townsend, A. A. (1976)The Structure of Turbulent Shear Flow, 2nd Ed., Cambridge University Press, UK.

    Google Scholar 

  18. 18.

    Bendat, J. S. and Piersol, A. G. (1986)Random Data: Analysis and Measurement Procedures, 2nd Ed., Wiley-Interscience, New York, pp. 48–108.

    Google Scholar 

  19. 19.

    Molloy, N. A. and Taylor, P. L. (1969) Oscillatory flow of a jet into a blind cavity.Nature 224, 1192–1194.

    Article  Google Scholar 

  20. 20.

    Tritton, D. J. (1988)Physical Fluid Dynamics. Clarendon, Oxford, UK.

    Google Scholar 

  21. 21.

    Christensen, C. W., Samet, M. M., Chick, D. M., and Lelkes, P. I. (1992) Experimental studies of pulsatile flow and endothelial-cell adaptation in ventricle-shaped cell culture chambers.ASAIO J. 38, M501-M506.

    PubMed  Article  CAS  Google Scholar 

  22. 22.

    Lundback, S. (1986)Cardiac Pumping and Function of the Ventricular Septum. Videomagica, Sweden.

    Google Scholar 

  23. 23.

    Taylor, D. E. M. and Wade, J. D. (1973) Pattern of blood flow within the heart: a stable system.Cardiovasc. Res. 7, 14–21.

    PubMed  Article  Google Scholar 

  24. 24.

    Kamiya, A. and Togawa, T. (1980) Adaptive regulation of wall shear stress to flow change in the canine carotid artery.Am. J. Physiol. 239, H14-H21.

    PubMed  CAS  Google Scholar 

  25. 25.

    Baldwin, J. T., Tarbell, J. M., Deutsch, S., Geselowitz, D. B., and Rosenberg, G. (1988) Hot-film wall shear probe measurements inside a ventricular assist device.J. Biomech. Eng. 110, 326–333.

    PubMed  CAS  Google Scholar 

  26. 26.

    Fry, D. L. (1969) Certain histological and chemical responses of the vascular interface to acutely induced mechanical stress in the aorta of the dog.Circ. Res. 24, 93–108.

    PubMed  CAS  Google Scholar 

  27. 27.

    Guyton, A. C. (1991)Textbook of Medical Physiology, 7th Ed., Saunders, Philadelphia, PA.

    Google Scholar 

  28. 28.

    Dewey, C. F., Jr. (1979) Fluid mechanics of arterial flow.Adv. Exp. Med. Biol. 115, 55–103.

    Google Scholar 

  29. 29.

    Nerem, R. M. (1981) Arterial fluid dynamics and interactions with the vessel walls, inStructure and Function of the Circulation. (Schwartz, C. J., Werthessen, N. T., and Wolf, S., eds.), Plenum, New York, pp. 719–835.

    Google Scholar 

  30. 30.

    Jones, R. T. (1972) Fluid dynamics of heart assist devices, inBiomechanics: Its Foundations and Objectives. (Fung, Y. C., Perrone, N., and Anliker, M., eds.), Prentice-Hall, Englewood Cliffs, NJ, pp. 549–565.

    Google Scholar 

  31. 31.

    Phillips, W. M., Furkay, S. S., and Pierce, W. S. (1979) Laser Doppler anemometer studies in unsteady ventricular flows.Trans. Am. Soc. Artif. Intern. Organs 25, 56–60.

    PubMed  CAS  Google Scholar 

  32. 32.

    Mussivand, T. V. (1988)Artifcial Heart Fluid Dynamics. PhD dissertation, University of Akron, Akron, OH.

    Google Scholar 

  33. 33.

    Nitta, S., Katahira, Y., Yambe, T., Tanaka, M., Kagawa, Y., Hongo, T., Sato, N., and Miura, M. (1988) Experimental and clinical evaluation of a sack-type ventricular assist device and drive system, inArtificial Heart 2: Proceedings of the 2nd International Symposium on Artificial Heart and Assist Device. (Akutsu, T., ed.), Springer-Verlag, Tokyo, Japan, pp. 131–139.

    Google Scholar 

  34. 34.

    Christensen, C. W., Smith, L. M., Gao, H., Grenier, R. P., and Schmidt, D. H. (1991) Application of a new nuclear scintigraphy camera to evaluate flow and mechanical pumping of artificial hearts.ASAIO J. 37, M503-M505.

    CAS  Google Scholar 

  35. 35.

    Nose, Y. (1990) My life with the National Institutes of Health Artificial Heart Program,Int. J. Artif. Organs 14, 174–190.

    CAS  Google Scholar 

  36. 36.

    Dewey, C. F., Jr., Bussolari, S. R., Gimbrone, M. A., Jr., and Davies, P. F. (1981) The dynamic response of vascular endothelial cells to fluid shear stress.J. Biomech. Eng. 103, 177–185.

    PubMed  Google Scholar 

  37. 37.

    Olesen, S.-P., Clapham, D. E., and Davies, P. F. (1988) Haemodynamic shear stress activates a K+ current in vascular endothelial cells.Nature 331, 168–170.

    PubMed  Article  CAS  Google Scholar 

  38. 38.

    Shen, J., Luscinskas, F. W., Connolly, A., Dewey, F. C., Jr., and Gimbrone, M. A., Jr. (1992) Fluid shear stress modulates cytosolic free calcium in vascular endothelial cells.Am. J. Physiol. 262, C384-C390.

    PubMed  CAS  Google Scholar 

  39. 39.

    Masuda, M. and Fujiwara, K. (1992) Three distinct types of flow-induced morphological and motile responses of cultured endothelial cells.5th International Congress on Cell Biology, Palacio de Congresos, Madrid, Spain, p. 249. (Abstract).

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Correspondence to Peter I. Lelkes.

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Samet, M.M., Lelkes, P.I. Flow patterns and endothelial cell morphology in a simplified model of an artificial ventricle. Cell Biophysics 23, 139–163 (1993). https://doi.org/10.1007/BF02796510

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Index Entries

  • Artificial ventricle
  • pulsatile flow
  • flow patterns
  • flow visualization
  • shear stress
  • endothelial cells
  • cell morphology
  • cytoskeleton
  • microfilaments