The history of arterial wave mechanics is long and distinguished. The arterial pulse
was familiar to Chinese, Indian, Greek and Roman physicians who exploited it regularly
in the diagnosis of disease. For more than 3,000 years, palpation of the radial pulse
has been a central observation in traditional Chinese medicine. One of the first and
best known books devoted to analysis of the arterial pulse is the Mai Jing or Pulse
Classic which was written by Wang Shu-he in the late Han dynasty (circa 220 ad) [49].
Pulse diagnosis in India probably has a similar span although it is difficult to know
because much of the teaching has been oral, directly from master to student, rather
than written. The traditional texts show a detailed knowledge of the arterial pulse,
but provide little insight into the mechanics of the pulse, which is hardly surprising
since they were developed millennia before the discipline of mechanics was invented.
Galen (129–210 ad) wrote a book On Prognosis from the Pulse [16] in which he describes
27 varieties of pulses and their meaning. He reports experiments from which he concludes
correctly that the arteries are filled with blood, not air or spirits as others had
asserted. He also carried out experiments that convinced him that the pulsative property
of the heart extends from the heart by the walls of the arteries and concluded wrongly
that they are filled by ‘that pulsific force, because they expand like bellows, and
do not dilate because they are filled like skins’. In other words, he felt that the
arteries expanded pulling blood into them rather than being expanded by the blood
entering from the heart.
William Harvey
Modern understanding of the cardiovascular system undoubtedly starts with the work
of William Harvey (1578–1657) who published his discovery of the circulation of blood
in (Exercitatio Anatomica De Motu Cordis et Sanguinis in Animalibus An Anatomical
Disquisition On the Motion of the Heart and Blood in Animals) [21]. Since this work
appeared before the invention of the microscope, it is certain that Harvey never saw
the capillaries but deduced that there must be small vessels connecting the arteries
and the veins. This makes his discovery even more remarkable and a landmark of deductive
reasoning, based upon careful observations and a very early application of the conservation
of mass, in the face of centuries of teachings to the contrary. Concerning the arterial
pulse, Harvey seems to agree with previous workers that the pulse appears in all of
the arteries simultaneously supporting his assertion with a quote from Aristotle;
‘Aristotle, too, has said, "the blood of all animals palpitates within their veins
(meaning the arteries), and by the pulse is sent everywhere simultaneously."’
1
Giovanni Borelli
Giovanni Borelli (1608–1679) is seen by many as the father of bioengineering because
of his studies on muscles, joints, the cardiovascular system, respiration, reproduction
and many other aspects of the body which were published in De Motu Animalium (On Animal
Motion) after his death [4]. He studied the contraction of the heart and its interaction
with the arteries. Interestingly, he clearly understood the capacitive effect of the
elastic arteries on smoothing the flow of blood (now known as the Windkessel effect).
In Proposition XXXI he states: I do not hesitate to claim that the blood circulates
through the body of the animal in a continuous and uninterrupted movement. Although
the heart does not pour blood into the arteries during its diastoles, the blood does
not stop and remain completely immobile and stagnant in the arteries, viscera, flesh
and veins when the heart is at rest. The blood keeps moving but with varying velocity...
This results from the fact that the arteries themselves are constricted by contraction
of their circular fibres.
The Reverend Stephan Hales (1677–1746) was a self-taught scientist who successfully
combined his scientific explorations with his ecclesiastical duties. In 1733, the
Royal Society published a series of papers that he had presented before the society
as Statical Essays: containing Haemastaticks [20]. It is full of original observations
about the mechanics of the cardiovascular system including the first measurements
of in vivo blood pressure. In Experiment 3, he discusses the velocity at which blood
is ejected from the heart of a 10-year-old mare and how it is altered by the elasticity
of the arteries:
...the velocity of the blood during each systole will be thrice as much, viz. at the
rate of 5204.7 feet, i.e. 0.98 of a mile in an hour or 86.7 feet in a minute [0.44 m/s].
Now this velocity is only the velocity of the blood at its first entering into the
aorta, in the time of the systole; in consequence of which the blood in the arteries,
being forcibly propelled forward, with an accelerated impetus, thereby dilates the
canal of the arteries, which begin again to contract at the instant the systole ceases:
by which curious artifice of nature, the blood is carried on in the finer capillaries,
with an almost even tenor of velocity, in the same manner as the spouting water of
some fire-engines, is contrived to flow with a more even velocity, notwithstanding
the alternate systoles and diastoles of the rising and falling embolus or force; and
this by the means of a large inverted globe, wherein the compressed air alternately
dilating or contracting, in conformity to the workings to and fro of the embolus,
and thereby impelling the water more equably than the embolus alone would do, pushes
it out in a more nearly equal spout.
The origin of quantitative mechanics in the cardiovascular system begins, as does
so much of quantitative mechanics in general, with Leonhard Euler (1707–1783). In
1755 he submitted an essay Principia pro motu sanguinis per arterias determinando
(On the flow of blood in the arteries) as an entry in a prize competition set by the
Academy of Sciences in Dijon [8]. In it he set out the one-dimensional equations of
conservation of mass and momentum in a distensible tube. In his notation
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\begin{document}$$ \left({\frac{{\text d}s} {{\text d}t}}\right) + \left({\frac{{\text
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\begin{document}$$ 2g\left({\frac{{\text d}p} {{\text d}z}}\right) + v\left({\frac{{\text
d}v} {{\text d}z}}\right) + \left({\frac{{\text d}v} {{\text d}t}}\right) = 0 $$\end{document}
where s is the cross-sectional area, v is the average velocity, p is pressure, g is
the density of blood, t is time and z is the axial distance.
Euler posited some rather unrealistic constitutive laws (tube laws) for arteries and
unsuccessfully tried to solve the equations as he had done for rigid tubes by reducing
them to a single equation that could be solved by integration. He concludes his letter
with the plaintive comment; ‘In motu igitur sanguinis explicando easdem offendimus
insuperabiles difficultates, quae nos impediunt omnia plane opera Creatoris accuratius
perscrutari; ubi perpetuo multo magis summam sapientiam cum omnipotentia coniunctam
admirari ac venerari debemus, cum ne summum quidem ingenium humanum vel levissimae
vibrillae veram structuram percipere atque explicare valeat.’
2 Unfortunately, Euler’s letter was lost for nearly a century, the surviving fragments
being discovered and published by the Euler Opera postuma project in 1862. The conservation
equations set out by Euler were rediscovered, but only in their linearised form, by
Wilhelm Weber over a century later (see below).
Thomas Young
The next major event in the the history of haemodynamics is the ’Croonian lecture
on the functions of the heart and the arteries’ delivered to the Royal Society in
1808 by Thomas Young (1773–1829) [60]. In the lecture, he stated the correct formula
for the wave speed in an artery but gave no derivation of it. In an associated paper,
he does give a derivation which is extremely hard to follow, being based on an analogy
to Newton’s derivation of the speed of sound in a compressible gas, some incomprehensible
algebra and numerical guesses [59].
Fourier (1768–1830) did not contribute directly to the mechanics of arteries, his
most notable work involving the physics of heat. In his treatise Theorie Analytique
de la Chaleur (The Analytical Theory of Heat) in 1822 [10], he asserted that periodic
functions can be expressed as the superposition of an infinite series of sinusoidal
functions and this observation has had such an impact on arterial haemodynamics that
it deserves a mention here. In fact, his assertion is not true for all periodic functions;
the first rigorous proof of Fourier’s theorem is due to Dirichlet [7] who showed that
it is true for piecewise regular functions with a finite number of discontinuities
and extrema (conditions that are met by virtually all physiological signals).
The development by Jean Louis Poiseuille (1799–1869) of his law of flow in tubes is
the next landmark in arterial mechanics. Although it is never observed in the arteries
because of the pulsatile nature of arterial flow and their complex anatomy of curves
and bifurcations, it has become the benchmark against which all other flows in tubes
are compared; probably because of its simplicity. Despite its shortcomings, it is
cited by many medical and physiological textbooks as the law that governs flow in
the whole of vasculature. Poiseuille, who trained as a physician, conducted a very
thorough investigation of flow in capillary tubes motivated by his studies of the
mesenteric microcirculation of the frog. In 1839, he deposited a sealed copy of his
experimental results with the French Academy of Sciences and continued his experiments
which were finally approved for publication in 1846 [39]. Poiseuille claimed from
his experiments that the volume flow rate Q varied as
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\begin{document}$$ Q = {\frac{KPD^4} {L}} $$\end{document}
where P is the pressure drop along the tube, D and L are the diameter and length of
the tube and K is a constant that depends on the temperature and the fluid flowing
in the tube. At nearly the same time Hagen (1797–1884), a German hydraulic engineer,
carried out similar experiments on the flow of water in cylindrical tubes with diameters
2.55, 4.01 and 5.91 mm which he published in 1839 [18]. A least squares fit for the
power of the dependency on diameter from his experiments yielded the value −4.12 but
he thought that this may have been due to errors in his experiments and suggested
the law
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\begin{document}$$ P = {\frac{ALQ + BQ^{2}} {D^4}} $$\end{document}
where A and B are constants depending upon temperature. Hagen appreciated that the
Q
2 term was associated with the generation of kinetic energy in the fluid. At sufficiently
low values of Q, this relationship reduces to that given by Poiseuille. Although the
coefficient of viscosity, introduced by Newton, was used in the study of tube flows
by Navier [34] (in which he derived an incorrect version of Poiseuille’s law including
an inverse dependence on D
3, the same law cited by Young in his Croonian lecture in 1808), neither Poiseuille
nor Hagen incorporated viscosity into their empirical formulae. The first derivation
of Poiseuille’s law (for horizontal tubes)
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\begin{document}$$ Q = {\frac{\pi PD^4} {128\mu L}} $$\end{document}
where μ is the coefficient of viscosity, is usually attributed to Hagenbach [19] who
generously suggested that the formula be named after Poiseuille, although there are
claims of prior publication on behalf of Jacobson, Neumann, Helmholtz, Stephan and
Mathieu [46]. To complicate attribution even further, it seems that Stokes also derived
Poiseuille’s law from the Navier–Stokes equation as early as 1845 but did not publish
the work because he was unsure about the validity of the no-slip condition at the
tube walls [45].
The question of the speed of travel of waves in elastic tubes was studied theoretically
by Wilhelm Eduard Weber (a noted physicist who is best known for his work on electromagnetism)
and experimentally by his brother Ernst-Heinrich Weber (an equally noted physiologist
who is considered by many to be the founder of experimental psychophysics) and published
in 1866 [50, 51]. The theoretical results are based on an independently derivied linearised
form of Euler’s conservation equations and the assumption of a constant distensibility
of the tube dr = kdp where dr is the increase in the radius and dp is the increase
in pressure. He derived the equation for the wave speed c
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\begin{document}$$ c = \sqrt{{\frac{R} {2k\rho}}} $$\end{document}
where ρ is the density of the fluid, k is the radial distensibility defined above
and R is the radius of the tube. This is the same relationship as proposed by Young
nearly 50 years earlier, but it has the advantage of a rigorous, easy to follow derivation.
Bernhard Riemann
Georg Friedrich Bernhard Riemann (1826–1866) did not work on arterial mechanics or
waves in elastic tubes, but he did make an important contribution to the subject when
he published a general solution for hyperbolic systems of partial differential equations
in 1860 [41]. His solution was inspired by a problem in gas dynamics but, like Fourier’s
theorem inspired by heat conduction, it has mathematical implications that transcend
its origins. Briefly, his work provides a general solution for a whole class of linear
and nonlinear partial differential equations by observing that along directions defined
by the eigenvalues of the matrix of coefficients of the differential terms, the partial
differential equations reduce to ordinary differential equations. Without knowing,
he provided the solution to Euler’s equations that Euler had sought in vain.
In 1877–1878, two more important works on the wave speed in elastic tubes were published.
Moens (1846–1891) [32] published a very careful experimental paper on wave speed in
arteries and Korteweg (1848–1941) [23] published a theoretical study of the wave speed.
Korteweg’s analysis showed that the wave speed was determined both by the elasticity
of the tube wall and the compressibility of the fluid. In the case of blood (which
is effectively incompressible) and thin-walled tubes, this reduces to the relationship
generally known as the Moens–Korteweg equation for the wave speed c
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\begin{document}$$ c = \sqrt{{\frac{Eh} {2\rho R}}} $$\end{document}
where E is the Young’s modulus of the wall whose thickness is h.
E.J. Marey (1830–1904) included a chapter on arterial blood flow in his popular textbook
of medicine Le circulation du sang á l’état physiologique et dans des maladies (The
Circulation of Blood in the Physiological State and in Disease) [27]. He cites work
by himself and others on the measurement of arterial blood velocity, using Pitot tubes
and bristle flow meters. The velocity waveforms he presents look surprisingly similar,
given the relative crudity of the methods, to modern waveforms obtained using the
latest technology. He shows large reverse flow at the end of systole in more distal
arteries such as the femoral artery. For some reason, this work was forgotten and
there was heated debate about the nature of flow in the femoral artery in the 1950s.
Otto Frank
Otto Frank (1865–1944) was one of the giants of quantitative physiology. He worked
primarily on the cardiovascular system and his work has had a lasting effect on the
practice of cardiology. His first of many contributions to arterial mechanics was
the mathematical formulation of the Windkessel effect in his paper of 1899 Die Grundform
des Arteriellen Pulses (The basis of arterial pulses) [11]. He took his inspiration
from the work of Stephan Hales, expressing his qualitative arguments in mathematical
terms.
3 He considered the arteries as a single compliant compartment and used the conservation
of mass to analyse their change of volume during diastole.
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\begin{document}$$ {\frac{{\text d}V} {{\text d}t}} = {\frac{P} {w}} \quad \hbox{and}
\quad {\frac{{\text d}P} {{\text d}V}} = c $$\end{document}
where V is the volume of the arterial compartment, P is its pressure, w is the resistance
to flow in the microcirculation, and c is a constant (confusingly to modern readers
equal to the inverse of the compliance). From these equations, he obtains an exponentially
falling pressure
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\begin{document}$$ P = P_0 {\text e}^{-ct/w} $$\end{document}
where P
0 is the pressure at the start of diastole. He then considers the systolic part of
the cardiac cycle and obtains a differential equation in terms of the input to the
arteries from the heart i. Although this equation has a general solution, he seems
unaware of it and instead solves it for the special cases i = constant and
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Frank’s next major contribution to arterial mechanics is a series of three papers
papers Der Puls in den Arterien (The pulse in the arteries) in 1905 [12], Die Elastizität
der Blutgefässe (The elasticity of blood vessels) in 1920 [13] and Die Theorie der
Pulswellen (The theory of pulse waves) in 1926 [14]. In the 1905 paper, he introduces
the theory of waves in arteries. In the 1920 paper, he correctly derives the wave
speed in terms of the elasticity
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\begin{document}$$ c = \sqrt{{\frac{\kappa} {\rho}}} $$\end{document}
where
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is the inverse of the distensibility of the vessel, A being the cross-sectional area
of the vessel. In the 1926 paper, he considers the effect of viscosity, the motion
of the wall and the energy of the pulse wave before turning to a number of examples
of special cases. These examples include the use of Fourier analysis and probably
the first treatment of the reflections of the pulse wave, including the reflection
and transmission coefficients due to a bifurcation.
There is a fundamental conflict between the two theories advanced by Frank, the Windkessel
and the pulse wave model for arterial mechanics. The Windkessel model assumes that
the entire arterial system acts like a single compartment while the wave model predicts
that information travels through the arteries in the form of waves. Frank was fully
aware of this dichotomy and discussed it, without resolving it, in his 1930 paper
Schätzung des Schlagvolumens des menschlichen Herzens auf Frund der Wellen- und Windkesseltheorie
(Estimation of the stroke volume of the human heart based upon wave and Windkessel
theory) [15]. The failure of the Windkessel theory to describe arterial pressure during
systole led to it being abandoned by cardiologists despite its success in describing
diastolic behaviour. As Milnor writes: ‘The great virtue of the initial Windkessel
model was its simplicity, and it still has an explanatory value as a rough approximation
that is readily grasped. For almost all research purposes, however, a more detailed
and realistic model that conforms to the distribution of properties in the vascular
tree is to be preferred.’ [30]. The Windkessel-wave dilemma has been revisited recently
and is the subject of a paper in this volume [48].
Many clinical cardiologists in the early twentieth century contributed to our understanding
of the form and function of the cardiovascular system, but relatively few contributed
significantly to our understanding of arterial mechanics. An outstanding exception
is Sir James MacKenzie. In medicine, he is best known for his pioneering work on cardiac
arrhythmias. However, his book The Study of the Pulse, Arterial, Venous, and Hepatic,
and of the Movements of the Heart contains many insights into the measurement and
the understanding of pressure and flow in blood vessels [26]. Most significantly,
he devised the ‘polygraph’ for the simultaneous measurement of arterial and venous
pressure pulses and showed how these waveforms altered in response to various types
of cardiac disease.
The analysis of waves in elastic tubes, that is generally associated by modern workers
with Womersley (1907–1958) [56], has a very long history that deserves a chapter on
its own. Much of the theory was derived by Gomelka in 1883, including the effects
of wall inertia on the wave speed. Unfortunately he published his work in Russian
in the Proceedings of the Kazan University which was not widely available to other
workers [17]. The problem was further developed by Lamb in his definitive book Hydrodynamics
(1879) who formulated the problem in very general terms [45]. His formulation was
used by Witzig [55] in a PhD thesis in the University of Bern where he obtained the
general solution for the velocity profiles as a function of vessel radius for rigid
tubes. This work was largely unnoticed and his results were rediscovered independently
by Morgan and Kiely [33] and Womersley [58]. It was this work that was taken up by
McDonald and other researchers for application to arterial mechanics [56–58].
These results rely essentially on the observation that the Navier-Stokes equations
are linear for parallel flow, in modern notation
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is perpendicular to u for parallel flows and so the nonlinear convective acceleration
term in the Navier–Stokes equation is zero because
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The resulting linear equations are then amenable to solution using Fourier methods.
In particular, flows with periodic boundary conditions can be solved exactly in terms
of the fundamental frequency and all of its harmonics.
A work that deserves wider recognition is the 1940 paper by Apéria [2]. Its undeserved
obscurity may be due to its publication in Berlin during the Second World War, which
would have limited its dissemination. The paper, entitled Haemodynamical Studies,
deals very comprehensively with both the Windkessel model and the ’undulatory’ (wave)
theory. He explores the basic assumptions of both theories and their variants and
reaches interesting results both theoretically and practically. In one brief passage
entitled ’Poiseuille’s flow with pressures changing in time’ he anticipates the later
results of Womersley in a prescient but, given the last sentence, unprophetic way:
"The solution for each Fourier term can be got without any special difficulty with
power-series with regard to the variable radial distance from the axis r, and it leads
moreover for every u (≠ 0) to Bessel-functions with complex arguments. Though the
complete mathematical treatment is here actually possible, it is of only minor interest
to the physiologist."
A very important thread in the tapestry of arterial mechanics has been the application
of electrical analogues to the circulation, generally known as impedance methods.
This approach to arterial haemodynamics presumes that there is a linear relationship
between pressure and flow that is given by an analogue of Ohms law
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\begin{document}$$\tilde{P} = \tilde{Z} \tilde{Q},$$\end{document}
where the pressure
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is analogous to the voltage, the flow rate
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is analogous to the current and
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is the impedance. With this analogy, complex RCL electrical networks can be formulated
to represent the resistance, capacitance and inertance of the different parts of the
vasculature.
According to Milnor [30], "the Fourier analysis of pressure and flow waves ... had
been suggested much earlier by Frank (1926) [14], championed by Apéria (1940) [2],
and finally introduced into cardiovascular physiology by Porje (1946) [40].’ Probably,
the first transmission line theory of the arteries was proposed by Landes [25] and
developed significantly by Taylor [47].
It is probably not a coincidence that the rapid growth in the application of Fourier
analysis to arterial mechanics coincides with the development of the digital computer
and the publication of the fast Fourier transform [6] (actually a rediscovery of an
algorithm known to Gauss). This meant that Fourier transforms that previously took
hours to compute could be calculated in seconds. The success of the impedance method
quickly lead to an explosion of work using it: D. A. McDonald and his students (notably
W. W. Nichols); M. G. Taylor, who provided much of the theoretical basis, and his
students (notably M. F. O’Rourke); Noordergraaf [52] (also see his influential review
[36]) and his group (notably N. Westerhof,, who proposed the three-element Windkessel
model [53], and J. K. Li); Milnor [30] and his students. It has been very successful
and is now, by far, the most common approach to arterial mechanics [3, 31, 37, 54].
An alternative approach to the problem has been the application of the method of characteristics
based upon the work of Riemann [41] to solve the nonlinear form of the conservation
equations derived by Euler [8]. The methods were first developed in the field of gas
dynamics where there was intense development, both theoretically and experimentally,
during and after the Second World War because of the emergence of high-speed flight.
The first application of the theory to arterial flows is probably the work of Lambert
who applied the theory to arteries using experimental measurements of the radius of
the artery as a function of pressure [24]. The approach was developed by Skalak [42]
and most completely by Anliker and his colleagues who mounted a systematic study of
the different elements of the vascular system with the goal of synthesising a complete
description of the arterial system using the method of characteristics [1, 22, 43,
44]. It is these works that inspired the development of wave intensity analysis [38].
Afterword
The author has worked for more than 20 years on the application of the method of characteristics
to the cardiovascular system. Although every effort has been made to make this brief
historical review as unbiased as possible, it is inevitable that some of my prejudices
have coloured both the content and the comments contained herein.
This brief sketch of the long and varied history of the subject has been compiled
mainly from secondary sources. Wherever possible, I have consulted the original works
but my knowledge of Latin, French, German and Russian is rudimentary at best and I
have had to rely upon the comments of others about the original sources for much of
the work. I have relied heavily upon Boulanger’s detailed and deep study of the history
of elastic tube waves for work prior to 1900 [5]. My source for much of the discussion
of Poiseuille’s law comes from Sutera and Skalak’s excellent essay [46]. Truesdell
provides his usual sharp and learned commentary about the work of Euler and his antecedents
in the introduction to the volume of the Leonhardi Euleri Opera Omnia [9]. Frank’s
earliest work on the mechanics of the cardiovascular system has been translated and
the authors’ introduction provides several insights into his extensive body of work
on arterial mechanics. [11].
I have chosen to conclude this historical essay in 1960 as that was the date of publication
of the first edition of Blood Flow in Arteries by McDonald (1917–1973) [28]. The first
edition of this book had limited circulation but a very large influence. A greatly
expanded second edition was published after McDonald’s death, edited by his daughter,
his colleague W. R. Milnor and former student W. W. Nichols [29]. In my opinion, this
book marks the beginning of the modern era of arterial mechanics and, incidentally,
it contains an excellent historical review that has been most helpful in compiling
this short history. Subsequently this book has been revised and expanded as McDonald’s
Blood Flow in Arteries, currently in its 5th edition [35]. As would be expected from
one of the fathers of the impedance method and his students, this book uses the Fourier
approach to cardiovascular mechanics almost exclusively and its influence on the subject
has been profound. In the context of this special issue, however, it is relevant to
quote from McDonald’s introduction to the 2nd edition of his book:
The main developments since 1950 have been in terms of treating the whole arterial
system as being in a steady-state oscillation produced by the regularly repeated beat
of the heart. This describes the pressure pulse as a collection of sinusoidal waves
of frequencies determined by the harmonic, or Fourier, series ...
The method of characteristics is also being introduced as a method of improving our
analysis of our non-linear system but has not yet undergone any severe experimental
testing. Intellectually, these investigations into non-linearity are greatly to be
commended. That they receive very little consideration in this book is not because
I regard them as negligible but, quite apart from considerations of space, because
my emphasis throughout has been on experimental findings. [29] p.12.