화학공학소재연구정보센터
홈 로그인 로그아웃 연락처 사이트맵
Korea-Australia Rheology Journal, Vol.28, No.1, 1-22, February, 2016
DOI10.1007/s13367-016-0001-z  Export Citation
A review of hemorheology: Measuring techniques and recent advances
Patrícia C. Sousa, Fernando T. Pinho1, Manuel A. Alves, and Mónica S.N. Oliveira2, †
  • Departamento de Engenharia Química, CEFT, Faculdade de Engenharia da Universidade do Porto, Rua Dr. Roberto Frias, 4200-465 Porto, Portugal
  • 1CEFT, Departamento de Engenharia Mecânica, Faculdade de Engenharia da Universidade do Porto, Rua Dr. Roberto Frias, 4200-465 Porto, Portugal
  • 2James Weir Fluids Laboratory, Department of Mechanical and Aerospace Engineering, University of Strathclyde, Glasgow G1 1XJ, United Kingdom, UK
E-mail:
Significant progress has been made over the years on the topic of hemorheology, not only in terms of the development of more accurate and sophisticated techniques, but also in terms of understanding the phenomena associated with blood components, their interactions and impact upon blood properties. The rheological properties of blood are strongly dependent on the interactions and mechanical properties of red blood cells, and a variation of these properties can bring further insight into the human health state and can be an important parameter in clinical diagnosis. In this article, we provide both a reference for hemorheological research and a resource regarding the fundamental concepts in hemorheology. This review is aimed at those starting in the field of hemodynamics, where blood rheology plays a significant role, but also at those in search of the most up-to-date findings (both qualitative and quantitative) in hemorheological measurements and novel techniques used in this context, including technical advances under more extreme conditions such as in large amplitude oscillatory shear flow or under extensional flow, which impose large deformations comparable to those found in the microcirculatory system and in diseased vessels. Given the impressive rate of increase in the available knowledge on blood flow, this review is also intended to identify areas where current knowledge is still incomplete, and which have the potential for new, exciting and useful research. We also discuss the most important parameters that can lead to an alteration of blood rheology, and which as a consequence can have a significant impact on the normal physiological behavior of blood.
Keywords:hemorheology;blood viscosity;blood viscoelasticity;RBC deformability;RBC aggregation
  1. Akers WJ, Cupps JM, Haidekker MA, Biorheology, 42, 335 (2005)
  2. Alexy T, Pais E, Wenby RB, Hogenauer W, Toth K, Meiselman HJ, Kensey KR, Clin. Lab., 51, 523 (2005)
  3. Alexy T, Wenby RB, Pais E, Goldstein LJ, Hogenauer W, Meiselman HJ, Biorheology, 42, 237 (2005)
  4. Apostolidis AJ, Armstrong MJ, Beris AN, J. Rheol., 59(1), 275 (2015)
  5. Apostolidis AJ, Beris AN, J. Rheol., 58(3), 607 (2014)
  6. Artmann GM, Kelemen C, Porst D, Buldt G, Chien S, Biophys. J., 75, 3179 (1998)
  7. Artmann GM, Sung KLP, Horn T, Whittemore D, Norwich G, Shu C, Biophys. J., 72, 1434 (1997)
  8. Barbee JH, Biorheology, 10, 1 (1973)
  9. Barnes HA, 2000, Handbook of Elementary Rheology, Institute of Non-Newtonian Fluid Mechanics, University of Wales Aberystwyth, U.K.
  10. Barnes HA, 2003, A review of the rheology of filled viscoelastic systems, In: Binding DM, Walters K, eds., Rheology Reviews, The British Society of Rheology, Aberystwyth, 1-36.
  11. Baskurt OK, Boynard M, Cokelet GC, Connes P, Cooke BM, Forconi S, Liao F, Hardeman MR, Jung F, Meiselman HJ, Nash G, Nemeth N, Neu B, Sandhagen B, Shin S, Thurston G, Wautier JL, Clin. Hemorheol. Microcirc., 42, 75 (2009)
  12. Baskurt OK, Hardeman MR, Uyuklu M, Ulker P, Cengiz M, Nemeth N, Shin S, Alexy T, Meiselman HJ, Biorheology, 46, 251 (2009)
  13. Benis AM, Lacoste J, Circ. Res., 22, 29 (1968)
  14. Bingham EC, Green H, Proc Am. Soc. Test. Mater, 19, 640 (1919)
  15. Bishop JJ, Popel AS, Intaglietta M, Johnson PC, Biorheology, 38, 263 (2001)
  16. Breedveld V, Pine DJ, J. Mater. Sci., 38(22), 4461 (2003)
  17. Bremmell KE, Evans A, Prestidge CA, Colloids Surf. B: Biointerfaces, 50, 43 (2006)
  18. Brust M, Schaefer C, Doerr R, Pan L, Garcia M, Arratia PE, Wagner C, Phys. Rev. Lett., 110, 078305 (2013)
  19. Campo-Deano L, Dullens RPA, Aarts DGAL, Pinho FT, Oliveira MSN, Biomicrofluidics, 7, 034102 (2013)
  20. Campo-Deano L, Oliveira MSN, Pinho FT, Appl. Mech. Rev., 67, 030801 (2015)
  21. Caro CG, Pedley TJ, Seed WA, 1974, Mechanics of the circulation, In: Guyton AC ed., Cardiovascular Physiology, Medical and Technical Publishers, London, 394-395.
  22. Charm SE, Kurland GS, Nature, 216, 1121 (1967)
  23. Cheng DCH, Evans F, Brit. J. Appl. Phys., 16, 1599 (1965)
  24. Chien S, Science, 168, 977 (1970)
  25. Chien S, Usami S, Taylor HM, Lundberg JL, Gregerse MI, J. Appl. Phycol., 21, 81 (1966)
  26. Cho YI, Cho DJ, Korean Circ. J., 41, 287 (2011)
  27. Cokelet GR, Meiselman HJ, 2007, Macro- and micro-rheological properties of blood, In: Baskurt OK, Hardeman MR, Rampling MW, Meiselman HJ, eds., Handbook of Hemorheology and Hemodynamics, IOS Press, Amsterdam, 45-71.
  28. Dao M, Lim CT, Suresh S, J. Mech. Phys. Solids, 51, 2259 (2003)
  29. Dintenfass L, Biorheology, 16, 69 (1979)
  30. Dintenfass L, 1985, Blood viscosity, Hyperviscosity & Hyperviscosaemia, MTP Press, Boston.
  31. Dobbe JGG, Hardeman MR, Streekstra GJ, Grimbergen CA, Biorheology, 41, 65 (2004)
  32. Drasler WJ, Smith CM, Keller KH, Biorheology, 26, 935 (1989)
  33. Eguchi Y, Karino T, Ann. Biomed. Eng., 36, 545 (2008)
  34. Eugster M, Hausler K, Reinhart WH, Clin. Hemorheol. Microcirc., 36, 195 (2007)
  35. Ewoldt RH, Hosoi AE, McKinley GH, J. Rheol., 52(6), 1427 (2008)
  36. Fahræus R, Physiol. Rev., 9, 241 (1929)
  37. Fahræus R, Lindqvist T, Am. J. Physiol., 96, 562 (1931)
  38. Faivre M, Abkarian M, Bickraj K, Stone HA, Biorheology, 43, 147 (2006)
  39. Fischer TM, Stohr-Lissen M, Schmid-Schonbein H, Science, 202, 894 (1978)
  40. Fontes A, Castro MLB, Brandao MM, Fernandes HP, Thomaz AA, Huruta RR, Pozzo LY, Barbosa LC, Costa FF, Saad STO, Cesar CL, J. Opt., 13, 044012 (2011)
  41. Haidekker MA, Tsai AG, Brady T, Stevens HY, Frangos JA, Theodorakis E, Intaglietta M, Am. J. Physiol.-Heart Circul. Physiol., 282, H1609 (2002)
  42. Harkness J, Biorheology, 8, 171 (1971)
  43. Hess WR, Pflug. Arch. Ges. Phys., 162, 187 (1915)
  44. Hyun K, Wilhelm M, Klein CO, Cho KS, Nam JG, Ahn KH, Lee SJ, Ewoldt RH, McKinley GH, Prog. Polym. Sci, 36, 1697 (2011)
  45. J. Clin. Pathol., 37, 1147 (1984)
  46. Jan KM, Chien S, Bigger JTJ, Circulation, 51, 1079 (1975)
  47. Johnn H, Phipps C, Gascoyne S, Hawkey C, Rampling MW, Clin. Hemorheol., 12, 639 (1992)
  48. Kang YJ, Lee SJ, Biomicrofluidics, 7 (2013)
  49. Kang YJ, Yang S, Microfluid. Nanofluid., 14, 657 (2013)
  50. Kim S, Cho YI, Jeon AH, Hogenauer B, Kensey KR, J. Non-Newton. Fluid Mech., 94(1), 47 (2000)
  51. Koenig W, Sund M, Filipiak B, Doring A, Lowel H, Ernst E, Arterioscler. Thromb. Vasc. Biol., 18, 768 (1998)
  52. Koutsouris D, Guillet R, Lelievre JC, Guillemin MT, Bertholom P, Beuzard Y, Boynard M, Biorheology, 25, 763 (1988)
  53. Langstroth L, J. Exp. Med., 30, 597 (1919)
  54. Larson RG, J. Rheol., 49(1), 1 (2005)
  55. Laurent VM, Henon S, Planus E, Fodil R, Balland M, Isabey D, Gallet F, J. Biomech. Eng. -Trans. ASME, 124, 408 (2002)
  56. Le Devehat C, Vimeux M, Khodabandehlou T, Clin. Hemorheol. Microcirc., 30, 297 (2004)
  57. Lee BK, Alexy T, Wenby RB, Meiselman HJ, Biorheology, 44, 29 (2007)
  58. Lee BK, Xue S, Nam J, Lim H, Shin S, Korea-Aust. Rheol. J., 23, 1 (2011)
  59. Lee BS, Lee YU, Kim HS, Kim TH, Park J, Lee JG, Kim J, Kim H, Lee WG, Cho YK, Lab Chip, 11, 70 (2011)
  60. Lee SS, Yim Y, Ahn KH, Lee SJ, Biomed. Microdevices, 11, 1021 (2009)
  61. Li T, Fan Y, Cheng Y, Yang J, Lab Chip, 13, 2634 (2013)
  62. Li XJ, Peng ZL, Lei H, Dao M, Karniadakis GE, Philos. Trans. R. Soc. Lond. Ser. A-Math. Phys. Eng. Sci., 372 (2014)
  63. Li YJ, Wen C, Xie HM, Ye AP, Yin YJ, Colloids Surf. B: Biointerfaces, 70, 169 (2009)
  64. Lim CT, Dao M, Suresh S, Sow CH, Chew KT, Acta Mater., 52, 1837 (2004)
  65. Lim HJ, Lee YJ, Nam JH, Chung S, Shin S, J. Biomech. Eng. -Trans. ASME, 43, 546 (2010)
  66. Presti RL, Hopps E, Caimi G, Korea-Aust. Rheol. J., 26(2), 199 (2014)
  67. Marcinkowska-Gapinska A, Gapinski J, Elikowski W, Jaroszyk F, Kubisz L, Med. Biol. Eng. Comput., 45, 837 (2007)
  68. Mark M, Hausler K, Dual J, Reinhart WH, Biorheology, 43, 133 (2006)
  69. Marton Z, Kesmarky G, Vekasi J, Cser A, Russai R, Horvath B, Toth K, Clin. Hemorheol. Microcirc., 24, 75 (2001)
  70. Merrill EW, Physiol. Rev., 49, 863 (1969)
  71. Merrill EW, Shin H, Cokelet G, Gilliland ER, Wells RE, Britten A, Biophys. J., 3, 199 (1963)
  72. Mills JP, Diez-Silva M, Quinn DJ, Dao M, Lang MJ, Tan KSW, Lim CT, Milon G, David PH, Mercereau-Puijalon O, Bonnefoy S, Suresh S, Proc. Natl. Acad. Sci. U.S.A., 104, 9213 (2007)
  73. Moreno L, Calderas F, Sanchez-Olivares G, Medina-Torres L, Sanchez-Solis A, Manero O, Korea-Aust. Rheol. J., 27(1), 1 (2015)
  74. Morris CL, Smith CM, Blackshear PL, Biophys. J., 52, 229 (1987)
  75. Muramoto Y, Nagasaka Y, Biorheology, 25, 43 (2011)
  76. Neuman KC, Nagy A, Nat. Methods, 5, 491 (2008)
  77. Ong PK, Lim D, Kim S, Crit. Rev. Biomed. Eng., 38, 189 (2010)
  78. Owens RG, J. Non-Newton. Fluid Mech., 140(1-3), 57 (2006)
  79. Picart C, Carpentier PH, Galliard H, Piau JM, Am. J. Physiol.-Heart Circul. Physiol., 276, H771 (1999)
  80. Picart C, Piau JM, Galliard H, Carpentier P, J. Rheol., 42(1), 1 (1998)
  81. Pirofsky B, J. Clin. Invest., 32, 292 (1953)
  82. Popel AS, Johnson PC, Annu. Rev. Fluid Mech., 37, 43 (2005)
  83. Pozrikidis C, 2003, Modeling and Simulation of Capsules and Biological Cells, CRC Press, Boca Raton.
  84. Puig-De-Morales-Marinkovic M, Turner KT, Butler JP, Fredberg JJ, Suresh S, Am. J. Physiol.-Cell Physiol., 293, C597 (2007)
  85. Radtke H, Schneider R, Witt R, Kiesewetter H, Schmid-Schonbein H, Adv. Exp. Med. Biol., 169, 851 (1984)
  86. Rampling MW, 2007, Compositional properties of blood, In: Baskurt OK, Hardeman MR, Rampling MW, Meiselman HJ, eds., Handbook of Hemorheology and Hemodynamics, IOS Press, Amsterdam, 34-44.
  87. Replogle RL, Meiselman HJ, Merrill EW, Circulation, 36, 148 (1967)
  88. Rosencranz R, Bogen SA, Am. J. Clin. Pathol., 125, S78 (2006)
  89. Schmid-Schonbein H, Gaehtgens P, Hirsch H, J. Clin. Invest., 47, 1447 (1968)
  90. Secomb TW, Microvasc. Res., 34, 46 (1987)
  91. Sharma K, Bhat SV, Physiol. Chem. Phys. Med. NMR, 24, 307 (1992)
  92. Shin S, Hou JX, Suh JS, Singh M, Clin. Hemorheol. Microcirc., 37, 319 (2007)
  93. Shin S, Lee SW, Ku YL, KSME Int. J., 18, 1036 (2004)
  94. Shung KK, 2006, Diagnostic Ultrasound : Imaging and Blood Flow Measurements, CRC Press, Boca Raton.
  95. Simchon S, Jan KM, Chien S, Am. J. Physiol., 253, H898 (1987)
  96. Smith PD, Young RCD, Chatwin CR, Measurement, 43, 144 (2010)
  97. Sousa PC, Carneiro J, Pinho FT, Oliveira MSN, Alves MA, Biorheology, 50, 269 (2013)
  98. Sousa PC, Pinho FT, Oliveira MSN, Alves MA, J. Non-Newton. Fluid Mech., 165(11-12), 652 (2010)
  99. Sousa PC, Pinho FT, Oliveira MSN, Alves MA, Biomicrofluidics, 5, 014108 (2011)
  100. Squires TM, Mason TG, Annu. Rev. Fluid Mech., 42, 413 (2010)
  101. Srivastava N, Davenport RD, Burns MA, Anal. Chem., 77, 383 (2005)
  102. Steffen P, Verdier C, Wagner C, Phys. Rev. Lett., 110, 018102 (2013)
  103. Sutera SP, Skalak R, Annu. Rev. Fluid Mech., 25, 1 (1993)
  104. Taguchi Y, Nagamachi R, Nagasaka Y, J. Therm. Sci. Technol., 4, 98 (2009)
  105. Thiriet M, 2008, Biology and Mechanics of Blood Flows, Springer, New York.
  106. Thurston GB, Biophys. J., 12, 1205 (1972)
  107. Thurston GB, Biorheology, 16, 149 (1979)
  108. Thurston GB, Adv. Hemodyn. Hemorheol., 1, 1 (1996)
  109. Thurston GB, Henderson NM, Biorheology, 43, 729 (2006)
  110. Thurston GB, Henderson NM, 2007, Viscoelasticity of human blood, In: Barskurt OK, Hardeman MR, Rampling MW, Meiselman HJ, eds., Handbook of Hemorheology and Hemodynamics, IOS Press, Amsterdam, 72-90.
  111. Travagli V, Zanardi I, Boschi L, Gabbrielli A, Mastronuzzi VAM, Cappelli R, Forconi S, Clin. Hemorheol. Microcirc., 38, 65 (2008)
  112. Valant AZ, Ziberna L, Papaharilaou Y, Anayiotos A, Georgiou GC, Rheol. Acta, 50(4), 389 (2011)
  113. Vlastos G, Lerche D, Koch B, Samba O, Pohl M, Rheol. Acta, 36(2), 160 (1997)
  114. Waite L, 2006, Biofluid Mechanics in Cardiovascular Systems, McGraw-Hill, New York.
  115. Yaginuma T, Oliveira MS, Lima R, Ishikawa T, Yamaguchi T, Biomicrofluidics, 7, 054110 (2013)
  116. Yao A, Tassieri M, Padgett M, Cooper J, Lab Chip, 9, 2568 (2009)
  117. Yilmaz F, Gundogdu MY, Korea-Aust. Rheol. J., 20(4), 197 (2008)
  118. Zeng H, Zhao Y, 2009, On-chip blood viscometer towards point-of-care hematological diagnosis, 22nd IEEE International Conference, Sorento.
  119. Zhu HY, Sencan I, Wong J, Dimitrov S, Tseng D, Nagashima K, Ozcan A, Lab Chip, 13, 1282 (2013)
  120. Zydney AL, Oliver JD, Colton CK, J. Rheol., 35, 1639 (1991)