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HANDBOOK OF HEMORHEOLOGY AND
HEMODYNAMICS
 Biomedical and Health Research
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ISSN 0929-6743
 Handbook of Hemorheology and
Hemodynamics

Edited by
Oguz K. Baskurt, M.D., Ph.D.
Professor and Chairman, Department of Physiology,
Akdeniz University Faculty of Medicine, Antalya, Turkey

Max R. Hardeman, Ph.D.

Clinical Biochemist, Laboratory for Clinical Hemorheology, Department of
Physiology, Academic Medical Center, Amsterdam, The Netherlands

Michael W. Rampling, Ph.D.

Honorary Senior Lecturer, Department of Bioengineering, Imperial College,
South Kensington, London, UK
and
Herbert J. Meiselman, Sc.D.
Professor and Vice-Chairman, Department of Physiology and Biophysics,
University of Southern California, Keck School of Medicine,
Los Angeles, CA, USA

Amsterdam • Berlin • Oxford • Tokyo • Washington, DC

© 2007 The authors.

All rights reserved. No part of this book may be reproduced, stored in a retrieval system,
or transmitted, in any form or by any means, without prior written permission from the publisher.

ISBN 978-1-58603-771-0
Library of Congress Control Number: 2007931478

Publisher
IOS Press
Nieuwe Hemweg 6B
1013 BG Amsterdam
Netherlands
fax: +31 20 687 0019
e-mail: [email protected]

Distributor in the UK and Ireland Distributor in the USA and Canada

Gazelle Books Services Ltd. IOS Press, Inc.
White Cross Mills 4502 Rachael Manor Drive
Hightown Fairfax, VA 22032
Lancaster LA1 4XS USA
United Kingdom fax: +1 703 323 3668
fax: +44 1524 63232 e-mail: [email protected]
e-mail: [email protected]

LEGAL NOTICE
The publisher is not responsible for the use which might be made of the following information.

PRINTED IN THE NETHERLANDS

Handbook of Hemorheology and Hemodynamics v
O.K. Baskurt et al. (Eds.)
IOS Press, 2007
© 2007 The authors. All rights reserved.

Foreword
The appearance of this Handbook is a timely event, as it is 20 years since the publica-
tion of the “Handbook of Bioengineering” [1] that dealt mainly with basic aspects of
hemodynamics and hemorheology. Also, in the 1980s and 1990s a number of books
were published that focused on clinical aspects of blood rheology [2–5]. In selecting
topics for the present handbook the editors have attempted to provide a general over-
view of both basic science and clinical hemorheology and hemodynamics. Hemorheol-
ogy and hemodynamics are closely related, the former dealing with all aspects of the
flow and interactions of the individual blood cells mostly studied in vitro, the latter
with the in vivo relationships among vessel architecture, driving pressure, flow rate and
shear stress. The linkage between the in vitro and in vivo research described in the
book will be of interest to both basic science and clinical investigators.
With respect to hemorheology, the new book successfully updates developments
and advances in the flow properties of human blood cells (microrheology). Further-
more, in the chapters on cell mechanics, these flow properties are related to events
occurring at the level of the bonds between the interacting corpuscles (platelets and
white cells as well as red cells), and between the corpuscles and the vessel wall (mo-
lecular rheology). A welcome feature of the handbook is that it includes a chapter on
comparative hemorheology, showing that the rheological properties of red cells vary
widely among the animal species, thus shedding light on the process of adaptation to a
specific environment or lifestyle, and a chapter on neonatal and fetal blood rheology
showing the considerable adaptation processes in play at birth and in infancy and
childhood. Also dealt with in some depth are the effects of diseases on the mechanical
and adhesive properties of red cells and the underlying molecular mechanisms, par-
ticularly those found in malaria. A related subject, the damage sustained by red cells
due to flow-induced mechanical trauma, is also presented.
With respect to hemodynamics, it is evident in the chapters of section III of the
handbook that the field has advanced significantly in the last 30 years, particularly with
respect to our understanding of microcirculatory blood flow using novel experimental
techniques, the latter being the subject of a separate chapter.
The handbook closes with chapters on clinical states associated with abnormal
blood rheology, including a chapter on the yet controversial subject of rheological ther-
apy.
The editors of the handbook have each been active in the fields of bio- and hemor-
heology for many years, and have published extensively. They have successfully
achieved their objective to publish a well-written and well-edited handbook that will be
valuable for researchers and students in the field.

Shu Chien, MD, PhD

Harry L. Goldsmith, PhD

[1] R. Skalak and S. Chien, Eds., Handbook of Bioengineering, McGraw-Hill, New York, 1987.
[2] S. Chien, J. Dormandy, E. Ernst and A. Matrai, Eds., Clinical Hemorheology, Martinus Nijhoff Publ.,
Dordrecht, 1987.
vi

[3] G.D.O. Lowe, Ed. Clinical Blood Rheology, CRC Press, Boca Raton, FL, 1988.
[4] A.M. Ehrly, Therapeutic Hemorheology, Springer-Verlag, New York, 1991.
[5] J.F. Stoltz, M. Singh and P. Riha, Hemorheology in Practice, IOS Press, Amsterdam, 1999.
 vii

Preface
The fields of hemorheology and hemodynamics are active and expanding areas of re-
search, yet no combined reviews or “handbooks” have been published within the past
20 years. It was thus felt appropriate to attempt such a task. An outlined proposal was
submitted to IOS Press and, after cordial telephone and email exchanges, was approved
for publication.
In planning for this book, the editors realized that it would be impossible to cover
in detail the entire field of hemorheology and hemodynamics, and hence that it would
be necessary to limit its scope. It was therefore decided to primarily focus on the
macro-and micro rheological behavior of blood and its formed elements, on interac-
tions between the formed elements and blood vessel walls, and on the microvascular
aspects of hemodynamics; areas such as cardiac hemodynamics and theory for pulsatile
flow in large vessels were omitted. Since many aspects of hemorheology and hemody-
namics can be affected by disease or a wide variety of clinical states, these areas were
deemed relevant as were the hyperviscosity syndromes and therapy for disturbed blood
rheology. In addition, discussions of methods in hemorheology and hemodynamics
were included to provide a practical framework for studies in these areas.
In the search for authors needed to prepare each section, the global nature of the
fields was recognized: Australia, Austria, France, Germany, Hungary, Italy, Nether-
lands, Singapore, South Korea, Turkey, United Kingdom and the United States of
America are represented. We sincerely thank every contributor for writing their section,
for allowing editorial corrections/modifications, and for accepting “helpful” criticism
without threatening the editors with hostile actions. This book would not have been
possible without their contributions. We also wish to thank Ms. Rosalinda B. Wenby
for her valuable editorial assistance.
We hope that we have been successful in reaching our objectives for this book, and
that it will be of value to researchers and clinical scientists engaged in hemorheology
and hemodynamic studies. In particular, we trust that the book will serve to foster
greater cooperative efforts between these fields. It is notable that the field of hemor-
heology was, in large part, prompted by direct observations of RBC aggregation,
“blood sludging”, white cell effects, and disturbed flow in the human retinal microcir-
culation. These observations have lead to in vitro studies of blood viscosity, cell rheol-
ogy and aggregation, and blood flow in small tubes and in more complex geometries;
studies aimed at understanding relations between in vitro and in vivo hemorheologic
and hemodynamic phenomenon are also ongoing. Further collaborative efforts will be
of mutual value, and will hopefully lead to improved health for normal individuals and
for those with various clinical conditions.

O.K. Baskurt
M.R. Hardeman
M.W. Rampling
H.J. Meiselman
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 ix

Contents
Foreword v
Shu Chien and Harry L. Goldsmith
Preface vii
O.K. Baskurt, M.R. Hardeman, M.W. Rampling and H.J. Meiselman

I. History of Hemorheology

I. History of Hemorheology 3
Michael W. Rampling

II. Hemorheology

1. Basic Aspects of Hemorheology 21

Giles R. Cokelet and Herbert J. Meiselman
2. Compositional Properties of Blood 34
Michael W. Rampling
3. Blood Rheology
a. Macro- and Micro-Rheological Properties of Blood 45
Giles R. Cokelet and Herbert J. Meiselman
b. Viscoelasticity of Human Blood 72
George B. Thurston and Nancy M. Henderson
4. Cell Mechanics
a. Mechanical and Adhesive Properties of Healthy and Diseased Red
Blood Cells 91
Brian M. Cooke and Chwee T. Lim
b. Red Blood Cell Aggregation 114
Björn Neu and Herbert J. Meiselman
c. Mechanical Properties of Leukocytes and Their Effects on the Circulation 137
Roger Tran-Son-Tay and Gerard B. Nash
d. Adhesion of Circulating Leukocytes and Platelets to the Vessel Wall 153
Susan L. Cranmer and Gerard B. Nash
5. Pathophysiology of Blood Rheology
a. Mechanisms of Blood Rheology Alterations 170
Oguz K. Baskurt
b. Hemorheology of the Fetus and Neonate 191
Otwin Linderkamp
c. Mechanical Trauma to Blood 206
Marina V. Kameneva and James F. Antaki
x

d. Hemorheological Considerations in Stored Blood Transfusion 228

James P. Isbister
6. Methods in Hemorheology 242
Max R. Hardeman, Peter.T. Goedhart and Sehyun Shin
7. Comparative Hemorheology 267
Ursula Windberger and Oguz K. Baskurt

III. Hemodynamics

1. Basic Principles of Hemodynamics 289

Timothy W. Secomb and Axel R. Pries
2. Blood Rheology Aspects of the Microcirculation 307
Herbert H. Lipowsky
3. In Vivo Hemorheology 322
Oguz K. Baskurt and Herbert J. Meiselman
4. Endothelium and Hemorheology 339
Tommaso Gori and Sandro Forconi
5. Methods in Hemodynamics 351
Sehyun Shin, Hideyuki Niimi, Max R. Hardeman and Peter.T. Goedhart

IV. Clinical Aspects of Hemorheology

1. Hyperviscosity: Clinical Disorders 371

James P. Isbister
2. Clinical Significance of Hemorheological Alterations 392
Kalman Toth, Gabor Kesmarky and Tamas Alexy
3. Treatment in Clinical Hemorheology: A Current Overview 433
Michel R. Boisseau, Katalin Koltai, Zsolt Pecsvarady and Kalman Toth
A Note on the Editors 445
Subject Index 447
Author Index 455
I. History of Hemorheology
This page intentionally left blank
Handbook of Hemorheology and Hemodynamics 3
O.K. Baskurt et al. (Eds.)
IOS Press, 2007
© 2007 IOS Press. All rights reserved.

History of Hemorheology
Michael W. RAMPLING1
School of Medicine, Imperial College, South Kensington, London SW7 2AZ, UK.

Introduction

If the rate of appearance of publications in the field can be taken as a criterion,

hemorheology can be considered as coming of age in the fairly recent past - perhaps
forty or so years ago. This relative lateness is due largely to the previous lack of
measuring equipment with the required sophistication; a particular problem being the
complex nature of blood viscosity and the need for adequate viscometers capable of
measuring it. Nevertheless the ease of availability of blood, its dramatic color and its
obvious connection to well being have made it a subject of study since ancient times.
What is more, many of those ancient studies were of physical properties of blood that
have direct hemorheological relevance. So it could be said that hemorheology is one of
the oldest of clinical research areas.

1. Ancient history

It quickly becomes clear to anyone who has left a tube of blood undisturbed for a
significant period that it will separate out into different phases. The very fact that, in
these circumstances, movement of blood components is taking place makes it a
hemorheological phenomenon, and the phenomenon was well known to the ancients,
and probably the first hemorheological phenomenon to be studied. They found that
such settled blood generally formed four layers, so the idea developed that blood was
composed of four fluids. The top layer, the first of the fluids, became known as the
yellow bile or cholera, and is now known to be serum, i.e. the fluid that separates from
the blood clot. The next layer was called the mucus or phlegma. This is now referred
to as the buffy coat of leukocytes, platelets and fibrin that settles on top of the third
layer called the blood or sanguinis. The third layer is actually the packed red cells.
Finally, at the bottom is the last layer, i.e. the black bile or melancholia; this is really
the red cells that have failed to oxygenate after the blood collection [1]. This
separation, and the fact that the rate of separation of the layers is increased in
association with disease, was known to the ancients Greeks and they developed it into a
diagnostic tool dependent on the relative proportions of the four layers.
It would have been a small step for the ancients to have moved from the ideas
presented above to an interest in the rate at which the blood layers settle out.
Strangely, it was many centuries before proper study of this took place. The person to
give it comprehensive investigation and to allow its development into a proper

1
Corresponding author: School of Medicine, Imperial College, South Kensington, London SW7 2AZ, UK;
E mail: [email protected]
4 M.W. Rampling / History of Hemorheology

quantitative diagnostic tool was Robin Fåhraeus in the early twentieth century. It
became known as the Erythrocyte Sedimentation Rate Test, and we shall return to it
later in this chapter.

2. Middle Ages

Following on from the idea of the humours in the blood, and their disturbance in
disease, it was not a great conceptual jump to the idea that the physician might do
something about the imbalance with the aim of alleviating the pathology. The method
for doing that was blood letting, which was to become a common therapeutic tool. The
bleeding could be induced grossly by lancing a major vessel or, perhaps more subtly,
by leaches. As might be expected the efficacy of the treatment was not high and,
indeed, often resulted in death of patients already weakened by the disease from which
they were suffering. Nevertheless the concept in principle is very close to that of a
hemorheological technique that was developed in the twentieth century, i.e.
hemodilution, to reduce blood viscosity and assist blood flow [2].

3. Age of Reason

The discovery by William Harvey, in the early seventeenth century, of the circulation
of the blood was one of the greatest physiological discoveries of all time (Figure 1).
Prior to Harvey’s insight, it had been believed that blood ebbed and flowed in the veins
and arteries spreading “vital spirit” to all the tissues, and the massive flow from the
heart was considered to be involved in the replenishment of the blood that was
consumed in the process.[3]. Harvey’s opus magnus, usually referred to as “De Motu
Cordis”, was published in 1628 [4]. His insight was based primarily on the
observations of the one-way valves in the veins and in and around the heart, the
different pressures in the veins and arteries and the effects of ligations on blood flow.
They enabled him to hypothesize the idea of blood circulating from the heart through
the arteries and returning to the heart via the veins. This was a huge physiological
insight and is obviously of great hemorheological significance as, for the first time, the
importance of flowing blood became exposed and so the rheological properties of
blood became relevant. Harvey’s discovery stands as one of the pivotal points in the
history of hemorheology. It is also interesting that, after the discovery, the raison
d’etre of blood letting gradually changed from being to readjust the humours to being,
rather, to thin the blood and so make blood flow easier. Harvey’s insight can be seen to
have been especially acute as he did not have access to microscopy and so, though he
could see the arteries and the veins, he could not see the microcirculatory vessels.
However, his evidence for a complete circulatory system was so compelling that he
assumed that there were “anastomosis of these vessels or pores in the flesh and solid
parts permeable to the blood” [5]. It was left to Malpighi in 1660 to be the first to see
the microcirculation [6] and to prove microscopically the connection of the network of
small vessels between the arterial and venous sides of the circulation.
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