Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-06T07:01:08.679Z Has data issue: false hasContentIssue false
  • English
  • Français

Age-Dependent Acoustic and Microelastic Properties of Red Blood Cells Determined by Vector Contrast Acoustic Microscopy

Published online by Cambridge University Press:  29 May 2012

Esam T. Ahmed Mohamed ,
Albert E. Kamanyi ,
Mieczysław Pluta  and
Wolfgang Grill
Esam T. Ahmed Mohamed*
Affiliation:
Institute of Experimental Physics II, University of Leipzig, Linnéstr. 5, D-04103 Leipzig, Germany
Albert E. Kamanyi
Affiliation:
Institute of Experimental Physics II, University of Leipzig, Linnéstr. 5, D-04103 Leipzig, Germany
Mieczysław Pluta
Affiliation:
Institute of Experimental Physics II, University of Leipzig, Linnéstr. 5, D-04103 Leipzig, Germany
Wolfgang Grill
Affiliation:
Institute of Experimental Physics II, University of Leipzig, Linnéstr. 5, D-04103 Leipzig, Germany
*
Corresponding author. E-mail: [email protected]
Get access

Abstract

Variations of the mechanical properties of red blood cells that occur during their life span have long been an intriguing task for investigations. The research presented is based on noninvasive monitoring of red blood cells of different ages performed by scanning acoustic microscopy with magnitude and phase contrast. The characteristic signature of fixed cells from groups of three different ages fractionated according to mass density is obtained from the acoustic microscope images, with the data represented in polar graphs. The analysis of these data enables the determination of averaged values for the velocities of ultrasound propagating in the cells from the different groups ranging from (1,681 ± 16) m s−1 in the youngest to (1,986 ± 20) m s−1 in the oldest group. The determined bulk modulus varies with age from (3.04 ± 0.05) GPa to (4.34 ± 0.08) GPa. An approach to determine for an age-mixed population of red blood cells, collected from a healthy person, the age of the individual cells and the age dependence of the cell parameters including density, velocity, and attenuation of longitudinal polarized ultrasonic waves traveling in the cells is demonstrated.

Keywords

SAMPSAMelastic properties of red blood cellsred blood cell age monitoring
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 18 , Issue 3 , June 2012 , pp. 436 - 444
Copyright
Copyright © Microscopy Society of America 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmed Mohamed, E.T., Kamanyi, A., von Butllar, M., Wannemacher, R., Hillmann, K., Ngwa, W. & Grill, W. (2008). Determination of mechanical properties of layered materials with vector-contrast scanning acoustic microscopy by polar diagram image representation. In Health Monitoring of Structural and Biological Systems II, Volume 6935, Kundu, T. (Ed.), pp. 69351Z–69658Z. Bellingham, WA: SPIE.Google Scholar
Ahmed Mohamed, E.T., Kamanyi, A., von Butllar, M., Wannemacher, R., Hillmann, K., Ngwa, W. & Grill, W. (2011). Ultra-high resolution thin film thickness delineation using reflection phase-sensitive acoustic microscopy. In Acoustical Imaging Volume 30, André, M.P., Jones, J.P. & Lee, H. (Eds.), pp. 125–134. New York: Springer.CrossRefGoogle Scholar
Ainslie, M.A. & McColm, J.G. (1998). A simplified formula for viscous and chemical absorption in sea water. J Acoust Soc Am 103, 1671–1672.CrossRefGoogle Scholar
Amjad, U., Ndop, J., Twerdowski, E. & Grill, W. (2008). Determination of the velocity of sound with high resolution by ultrasonic imaging of wedge shaped objects in transmission with vector contrast. In Health Monitoring of Structural and Biological Systems II, Volume 6935, Kundu, T. (Ed.), pp. 69351C–69358C. Bellingham, WA: SPIE.Google Scholar
Antonelou, A.H., Kriebardis, A.G. & Papassideri, I.S. (2010). Aging and death signaling in mature red cells: From basic science to transfusion practice. Blood Transfus 8, s39–s47.Google ScholarPubMed
Bartosz, G. (1991). Erythrocyte aging: Physical and chemical membrane changes. Gerontology 37, 33–67.CrossRefGoogle ScholarPubMed
Bereiter-Hahn, J. & Blasé, C. (2004). Ultrasonic characterization of biological cells. In Ultrasonic Non-Destructive Evaluation, Kundu, T. (Ed.), pp. 725–760. Boca Raton, FL: CRC Press.Google Scholar
Bereiter-Hahn, J., Blase, C., Kundu, T. & Wagner, O. (2002). Cells as seen with the acoustic microscope. In Acoustical Imaging Volume 26, Maev, R.G. (Ed.), pp. 83–90. Berlin: Springer.CrossRefGoogle Scholar
Borun, E.R., Figueroa, W.G. & Perry, S.M. (1957). The distribution of Fe59 tagged human erythrocytes in centrifuged specimens as a function of cell age. J Clin Invest 36, 676–679.CrossRefGoogle ScholarPubMed
Brekhovskikh, L.M. (1980). Waves in Layered Media. New York: Academic Press.Google Scholar
Briggs, A. & Kolosov, O. (2009). Acoustic Microscopy. New York: Oxford University Press.CrossRefGoogle Scholar
Briggs, G.A., Wang, J. & Gundle, R. (1993). Quantitative acoustic microscopy of individual living human cells. J Microsc 172, 3–12.CrossRefGoogle ScholarPubMed
Chandraratna, P.A.N., Choudhary, S. & Jones, J.P. (1992). Visualization of myocardial cellular architecture using acoustic microscopy. Am Heart 124, 1358–1364.CrossRefGoogle ScholarPubMed
Cordero, J.F., Rodriguez, P.J. & Romero, P.J. (2004). Differences in intramembrane particle distribution in young and old human erythrocytes. Cell Biol Int 28, 423–431.CrossRefGoogle Scholar
Corrons Vives, J., Albarède, S., Flandrin, G., Heller, S., Horvath, K., Houwen, B., Sarkani, E., Skitek, M., Van Blerk, M. & Libeer, J.C. (2004). Guidelines for blood smear preparation and staining procedure for setting up an external quality assessment scheme for blood smear interpretation. Part 1: Control material. Clin Chem Lab Med 42, 922–926.Google Scholar
Costa, M., Ghiran, I., Peng, C.K., Nicholson-Weller, A. & Goldberger, A.L. (2008). Complex dynamics of human red blood cell flickering: Alterations with in vivo aging. Phys Rev E 78, 020901–020904.CrossRefGoogle ScholarPubMed
Deplaine, G., Safeukui, I., Jeddi, F., Lacoste, F., Brousse, V., Perrot, S., Biligui, S., Guillotte, M., Guitton, C., Dokmak, S., Aussilhou, B., Sauvanet, A., Hatem, D.C., Paye, F., Thellier, M., Geneviève, D.M., Mohandas, N., Mercereau-Puijalon, O., David, P.H. & Buffet, P.A. (2011). The sensing of poorly deformable red blood cells by the human spleen can be mimicked in vitro. Blood 117, e88–e95.CrossRefGoogle ScholarPubMed
Dukhin, A.S. & Goetz, P.J. (2002). Acoustic parameters. In Ultrasound for Characterizing Colloids Particle Sizing, Zeta Potential, Rheology, Möbius, D. & Miller, R (Eds.), pp. 22–32. Amsterdam: Elsevier.Google Scholar
Dukhin, A.S. & Goetz, P.J. (2009). Bulk viscosity and compressibility measurement using acoustic spectroscopy. J Chem Phys 130, 124519-1–13.CrossRefGoogle ScholarPubMed
Dukhin, A.S., Goetz, P.J. & Van de Ven, T.G.M. (2006). Ultrasonic characterization of proteins and blood cells. Colloids Surf B 53, 121–126.CrossRefGoogle ScholarPubMed
Embree, P.M., Tervola, M.U., Foster, S.G. & O'Brien, W.D. (1985). Spatial distribution of the speed of sound in biological materials with the scanning laser acoustic microscope. IEEE Trans Soni Ultrason 32, 341–350.CrossRefGoogle Scholar
Every, A.G., Hillmann, K., Würz, K.U., Hasselmann, H. & Grill, W. (1996). Singularities in surface acoustic microscopy phase images. Physica B (Amsterdam) 219–220, 714–716.CrossRefGoogle Scholar
Föller, M., Huber, S.M. & Lang, F. (2008). Erythrocyte programmed cell death. IUBMB Life 60, 661–668.CrossRefGoogle ScholarPubMed
Fornaini, G., Magnani, M., Fazi, A., Accorsi, A., Stocchi, V. & Daachà, M. (1985). Regulatory properties of human erythrocyte hexokinase during cell ageing. Arch Biochem Biophys 239, 352–358.CrossRefGoogle ScholarPubMed
Fortier, N., Snyder, L.M., Garver, F., Kiefer, C., McKenney, J. & Mohandas, N. (1988). The relationship between in vivo generated hemoglobin skeletal protein complex and increased red cell membrane rigidity. Blood 71, 1427–1431.CrossRefGoogle ScholarPubMed
Gaczyńska, M. & Bartosz, G. (1986). Crosslinking of membrane proteins during erythrocyte ageing. Int J Biochem 18, 377–382.CrossRefGoogle ScholarPubMed
Gratzer, W.B. (1981). The red cell membrane and its cytoskeleton. Biochem J 198, 1–8.CrossRefGoogle ScholarPubMed
Grill, W., Hillmann, K., Kim, T.J., Lenkeit, O., Ndop, J. & Schubert, M. (1999). Scanning acoustic microscopy with vector contrast. Physica B 263–264, 553–558.CrossRefGoogle Scholar
Grill, W., Hillmann, K., Würz, K.U. & Wesner, J. (1996). Scanning ultrasonic microscopy with phase contrast. In Advances in Acoustic Microscopy, Briggs, A. & Arnold, A. (Eds.), pp. 167–216. New York: Plenum Press.CrossRefGoogle Scholar
Hildebrandt, J.A., Rugar, D., Johnston, R.N. & Quate, C.F. (1981). Acoustic microscopy of living cells. Proc Natl Acad Sci USA 78, 1656–1660.CrossRefGoogle Scholar
Hillmann, K., Grill, W. & Bereiter-Hahn, J. (1994). Determination of ultrasonic attenuation in small samples of solid material by scanning acoustic microscopy with phase contrast. J Alloy Compd 211–212, 625–627.CrossRefGoogle Scholar
Jain, S.K. & Hochstein, P. (1980). Polymerization of membrane components in aging red blood cells. Biochem Biophys Res Commun 92, 247–254.CrossRefGoogle ScholarPubMed
Johnston, R.N., Atalar, A., Heiserman, J., Jipson, V. & Quate, C.F. (1979). Acoustic microscopy: Resolution of subcellular detail. Proc Natl Acad Sci USA 76, 3325–3329.CrossRefGoogle ScholarPubMed
Jürgens, K.D., Baumann, R. & Röbbel, H. (1980). Ligand l linked changes of ultrasound absorption of hemoglobin. Eur J Biochem 103, 331–338.CrossRefGoogle Scholar
Kameneva, M.V., Garrett, K.O., Watach, M.J. & Borovetz, H.S. (1998). Red blood cell aging and risk of cardiovascular diseases. Clin Hemorheol Microcirc 18, 67–74.Google ScholarPubMed
Kremkau, F.W., Carstensen, E.L. & Aldridge, W.G. (1973). Macromolecular interactions in the absorption of ultrasound in fixed red blood cells. J Acoust Soc Am 53, 1448–1451.CrossRefGoogle Scholar
Kruse, A., Uehlinger, D.E., Gotch, F., Kotanko, P. & Levin, N.W. (2008). Red blood cell life span, erythropoiesis and hemoglobin control. Contrib Nephrol 161, 247–254.CrossRefGoogle Scholar
Kuettner, J.F., Dreher, K.L., Rao, G.H., Eaton, J.W., Blackshear, P.L. & White, J.G. (1977). Influence of the ionophore A23187 on the plastic behavior of normal erythrocytes. Am J Pathol 88, 81–94.Google ScholarPubMed
Kundu, T., Bereiter-Hahn, J. & Karl, I. (2000). Cell property determination from the acoustic microscope generated voltage versus frequency curves. Biophys J 78, 2270–2279.CrossRefGoogle ScholarPubMed
Lee, P., Kirk, R.G. & Hoffman, J.F. (1984). Interrelations among Na and K content, cell volume, and buoyant density in human red blood cell populations. J Membr Biol 79, 119–126.CrossRefGoogle Scholar
Lemons, R.A. & Quate, C.F. (1974). Acoustic microscope-scanning version. Appl Phys Lett 24, 163–165.CrossRefGoogle Scholar
Liang, K.K., Bennett, S.D., Khuri-Yakub, B.T. & Kino, G.S. (1985). Precise phase measurements with the acoustic microscope. IEEE Trans Sonics Ultrason 32, 266–273.CrossRefGoogle Scholar
Litniewski, J. & Bereiter-Hahn, J. (1990). Measurements of cells in culture by scanning acoustic microscopy. J Microsc 158, 95–107.CrossRefGoogle ScholarPubMed
Lorand, L., Weissmann, L.B., Epel, D.L. & Bruner-Lorand, J. (1976). Role of the intrinsic transglutaminase in the Ca2+-mediated crosslinking of erythrocyte proteins. Proc Natl Acad Sci USA 73, 4479–4481.CrossRefGoogle ScholarPubMed
Nash, G.B. & Gratzer, W.B. (1993). Structural determinants of the rigidity of the red cell membrane. Biorheology 30, 397–407.CrossRefGoogle ScholarPubMed
Nguyen, D. (2010). Phosphatidylserine exposure in red blood cells: A suggestion for the active role of red blood cells in blood clot formation. PhD thesis. University of Saarland, Germany.Google Scholar
Park, Y., Best, C.A., Badizadegan, K., Dasari, R.R., Feld, M.S., Kuriabova, T., Henle, M.L., Levine, A.J. & Popescu, G. (2010). Measurement of red blood cell mechanics during morphological changes. Proc Natl Acad Sci USA 15, 6731–6736.CrossRefGoogle Scholar
Parker, K.J. (1983). Ultrasonic attenuation and absorption in liver tissue ultrasound. Med Biol 9, 363–369.Google Scholar
Pfafferott, C., Nashj, G.B. & Meiselman, H.J. (1985). Red blood cell deformation in shear flow: Effects of internal and external phase viscosity and of in vivo aging. Biophys J 74, 695–704.CrossRefGoogle Scholar
Pierce, A. (1989). The Doppler effect. In Acoustics: An Introduction to Its Physical Principles and Applications, Pierce, A. (Ed.), pp. 451–460. New York: Acoustical Society of America.Google Scholar
Piomelli, S. & Seaman, C. (1993). Mechanism of red blood cell aging: Relationship of cell density and cell age. Am J Hematol 42, 46–52.CrossRefGoogle ScholarPubMed
Racca, A., Biondi, C., Cotorruelo, C., Galizzi, S., Rasia, R.J., Stoltz, J-F. & Valverde, J. (1999). Senescent erythrocytes: Modifications of rheologic properties, antigenic expression and interaction with monocytes. Medicina (B Aires) 59, 33–37.Google ScholarPubMed
Reinholdtsen, P.A., Chou, C.H. & Khuri-Yakub, B.T. (1987). Quantitative acoustic microscopy using amplitude and phase imaging. In IEEE 1987 Ultrasonic Symposium, McAvoy, B.R. (Eds.), pp. 807–811. New York: IEEE Ultrasonics, Ferroelectrics, and Frequency Control Society.CrossRefGoogle Scholar
Rennie, C.M., Thompson, S., Parker, A.C. & Maddy, A. (1979). Human erythrocyte fractionation in Percoll density gradients. Clin Chim Acta 98, 119–125.CrossRefGoogle ScholarPubMed
Romero, P.J. & Romero, E.A. (1999). The role of calcium metabolism in human red blood cell ageing: A proposal. Blood Cells Mol Dis 25, 9–19.CrossRefGoogle ScholarPubMed
Schenk, E.A., Waag, R.W., Schenk, A.B. & Aubuchon, J.P. (1988). Acoustic microscopy of red blood cells. J Histochem Cytochem 36, 1341–1351.CrossRefGoogle ScholarPubMed
Selfridge, A.R. (1985). Approximate material properties in isotropic materials. IEEE Trans Sonics Ultrason 32, 381–394.CrossRefGoogle Scholar
Shemin, D. & Rittenberg, D. (1946). The life span of the human red blood cell. J Biol Chem 166, 627–636.CrossRefGoogle ScholarPubMed
Shiga, T., Sekiya, M., Maeda, N., Kon, K. & Okazaki, M. (1985). Cell age-dependent changes in deformability and calcium accumulation of human erythrocytes. Biochim Biophys Acta 814, 289–299.CrossRefGoogle ScholarPubMed
Simchon, S., Jan, K-M. & Chien, S. (1987). Influence of reduced red cell deformability on regional blood flow. Am J Physiol 253, H898–H903.Google ScholarPubMed
Snabre, P. & Mills, P. (1999). Rheology of concentrated suspensions of viscoelastic particles. Colloids Surf A 152, 79–88.CrossRefGoogle Scholar
Sutera, S.P., Gardner, R.A., Boylan, C.W., Carroll, G.L., Chang, K.C., Marvel, J.S., Kilo, C., Gonen, B. & Williamson, J.R. (1985). Age-related changes in deformability of human erythrocytes. Blood 65, 275–282.CrossRefGoogle ScholarPubMed
Tittmann, B.R. & Miyasaka, C. (2003). Imaging and quantitative data acquisition of biological cells and soft tissues with scanning acoustic microscopy. In Science, Technology and Education of Microscopy: An Overview, Méndez-Vilas, A. & Díaz, J. (Eds.), pp. 325–344. Badajoz, Spain: Formatex.Google Scholar
von Buttlar, M., Ahmed Mohamed, E.T. & Grill, W. (2011). Signal processing for time-lapse cell imaging with vector-contrast scanning acoustic microscopy. In Acoustical Imaging Volume 30, André, M.P., Jones, J.P. & Lee, H. (Eds.), pp. 135–142. New York: Springer.CrossRefGoogle Scholar
Waugh, R. & Sarelius, I. (1996). Effects of lost surface area on red blood cells and red blood cell survival in mice. Am J Physiol 271, C1847–C1852.CrossRefGoogle ScholarPubMed