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Physiology in Fractal Dimensions

Author(s): Bruce J. West and Ary L. Goldberger
Source: American Scientist, Vol. 75, No. 4 (July-August 1987), pp. 354-365
Published by: Sigma Xi, The Scientific Research Society
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Physiology
Dimensions
Fractal

in

Bruce J.West
Ary L. Goldberger

swirling spiral of the cochlea and the finely

on a key assump
brains. Thompson's
approach relied
that
tree
the
structure of the bronchial
tion, namely,
branched
biological processes, like their physical
suggest
are
and regu
between
continuous, homogeneous,
interrelations
counterparts,
biological development,
complex
the
lar.
and
Observation
1900s
In
however,
the
and
function.
suggest
form,
experiment,
D'Arcy Thompson
early
Most biological systems, and many physical
in exquisite detail (2). Thomp
relations
these
opposite.
explored
and irregular.
son was convinced that although biological systems may
ones, are discontinuous,
inhomogeneous,
structure and behavior of
The variable, complicated
evolve by rules distinct from those governing the devel
on chaos as
violate basic
living systems seem as likely to be verging
opment of a physical system, they cannot
on
some
converging
regular pattern.
physical laws. This idea of underly
these kinds of sys
Characterizing
ing physical constraints led to the
tems evidently requires new models.
formulation of several important scal
The mathematical
In this article, we discuss how the
in
relations
biology?describing,
ing
related concepts of fractals, nonan
for example, how proportions tend
an
to vary as
animal grows.
functions, and
alytic mathematical
new
an
transforma
on
renormalization
that
group
brings
elegant
depend
Relationships
to
tions provide novel approaches
scale can have profound implications
the study of physiological
form and
for exam
for physiology. Consider,
function.
structure, growth, and
ple, one of the standard problems of
The most obvious feature of all
as the cube of
mass
increases
scaling:
area only as the
but
surface
systems is their com
physiological
length,
the richness of
if
to
this
Capturing
plexity.
square. According
principle,
_
structure and function
one species is twice as tall as another, _
physiological
in a single model is one of the major
it is likely to be eight times heavier
of
modern
but to have only four times as much surface area. This
challenges
biology. The treelike bronchial
for
tells us immediately that the larger plants and animals
system of the lung (Fig. 1) serves as a paradigm
anatomic complexity.
must compensate for their bulk; respiration depends on
Two paradoxical features of the bronchial tree strike
surface area for the exchange of gases, as does cooling by
is the extreme variability of tube lengths
One
the
nutrition
and
skin
from
the
eye.
by absorption
evaporation
and diameters; the other is the high level of organization.
to add surface to a given
One
membranes.
way
through
volume is to make the exterior more irregular, as with
By convention, successive bifurcations of the bronchial
as dia
tree are labeled by "generation"
branches and leaves; another is to hollow out the interi
number,
in
or. The human lung, with
Figure 2. The
grammed
first generation of tubes
about 300 million air sacs,
includes just two mem
fa
the more
approaches
ratio of surface
vorable
bers, the left and right
mainstem bronchi, which
to volume enjoyed by
branch off the trachea.
ances
our evolutionary
second
The
tors, the single-celled mi
generation
consists of four tubes, and
crobes.
so forth. Clearly,
from
The classical concepts
one generation to the next
of scaling developed by
the tube sizes vary, tend
and
others,
Thompson
while of great importance,
ing to get smaller and
smaller. But the variability
fail precisely at this point:
are not capable of
is not restricted to com
they
the
for
parisons between genera
irregu
accounting
tions. The tubes also vary
struc
lar surfaces and
seen
in hearts,
tures
markedly within any given
and
intestines,
generation.
lungs,

The

conceptoffractalscaling
logic to the irregular

functionof complex
biologicalforms

354

American Scientist,Volume 75

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a new geometry liberates

to some enthusiasts,
Figure 1. According
the analysis of natural objects from the tyranny of straight lines, flat
and regular solids. Mandelbrot
coined the word "fractal"
planes,
a

(ref. 4) to describe

randomness
mountains

the constrained
family of shapes which mimic
are not spheres,
in nature: "Clouds
everywhere
are not cones, coastlines
are not circles, and bark is not
found

smooth, nor does lightning travel in a straight line" (p. 1). One way
to envision
fractals is to think of them as objects with fractional
dimension?the
infinitely nesting spheres on page 358, for example,
or the
are
trees on page 359. Physiologists
infinitely branching

finding the
mammalian

new

to be a fertile source of insight. The

geometry
in
of natural
particular, has long been a paradigm
lung,
scientists to reduce its structure and growth
challenging

complexity,
to simple rules, much
early astronomers.
human bronchial

as the wanderings
of the planets
challenged
shows a plastic cast of the
photograph
tree, from the trachea to the terminal bronchioles.
a
of the new geometry, Mandelbrot
developed
The

one example
fractal model
at the bottom of the facing
of the lungs, reproduced
page, that could be based on a simpler genetic code than
conventional models would
allow.
courtesy of John B.
(Photograph
. B. Mandelbrot,
from ref. 4.)
West;
courtesy of
diagram
As

The second impression, which seems to contradict

the first, is that of organization.
The bronchial tree,
its
is
constructed
despite
asymmetries,
clearly
according
to some ordering principles. There appears
to be a
structure
the
sizes:
chaos
of
pattern underlying
lung
appears roughly similar from one generation of tubes to
the next. This paradoxical combination of variability and
order will have to emerge from any successful model of
bronchial architecture. Indeed, we will be forced to reject
as
that fails to encompass
any model
"unphysiologic"
these two features.
Over the past several years, in collaboration with a
number of colleagues, we have developed models
that
a
mechanism
the
for
inher
suggest
organized variability
ent in physiological structure and function. The essential
random
concept underlying this kind of "constrained
ness" (2, 3) is scaling. The general notion of scaling is
well established
in biology via the work of Thompson
and others. However,
the new scaling mechanism we
will discuss
adds a few unfamiliar wrinkles
to the
traditional theories. At the same time, in the nonbiologi
cal sciences, these new models have already emerged as
an
a variety of
important strategy in understanding
new
The
complex systems.
scaling appears, for example,
in related guise in the theory of critical
phenomena
(renormalization group theory), in the chaotic dynamics
of nonlinear systems, and in the description of a ubiqui
tous class of irregular structures called fractals.
in recent years by
The concept of fractals, developed
Mandelbrot
with
deals
(4),
complex geometric forms. A
fractal structure is not smooth and homogeneous. When
examined with stronger and stronger magnifying lenses,
fractals reveal greater and greater levels of detail. Further
more, the smaller-scale structure is similar to the larger

scale form.As in the diagram on the facing page, there is

no characteristic scale of length. Many objects in nature,
including trees, coral formations, cumulus clouds, and
coastlines, are fractal.As we will show, lungs, hearts, and
many other anatomic structures are also fractal-like.
In applying the new scaling ideas to
physiology, we
have seen that irregularity, when
admitted as funda
mental rather than treated as a
pathological deviation
from some classical ideal, can paradoxically
suggest a
more powerful
To
the
advan
describe
unifying theory.
tage of the new concepts, we must first review some
classical theories of scaling.

The principle of similitude

The notion of scaling is hardly novel. One of the more

intriguing scaling relations dates back at least to the
ancient Greeks and is easily derived by the
following
procedure. Draw a line of unit length
a
and divide it into two segments of
I b
'
length a and b such that the ratio of
the original line (a + b) to the longer segment, a, is the
same as the ratio of a to the shorter segment, b. There
= alb. One can
fore, (a + b)la
readily solve this algebra
ic equation and show that the proportion alb is equal to
= 1.618_This
the irrational number
(1 4- V5)/2
now
,was
scaling proportion,
generally designated as
referred to by the ancient Greeks as the golden section or
golden mean. Kepler called it the "divine proportion."
These names suggest the simple yet profound implica
tions of this kind of scaling, which has been observed in
the dimensions of the Parthenon as well as in vases and
sculptures from the same period (5).
The same proportion can be derived by generating a
series of positive integers beginning with 1, such that
each number is the sum of the two preceding numbers:
The ratio of each
1, 1, 2, 3, 5, 8, 13, 21, 34, 55....
as a
number to its immediate predecessor approaches
=
=
=
21/13
55/34
13/8
value:
1.615,
1.625,
limiting
in the
1.618, and so on. This series was popularized
Leonardo
thirteenth century by the mathematician
of
Pisa, also known as Filius Bonacci. The integers in the
sequence have come to be known as the Fibonacci
numbers.

1987 July-August 355

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The Fibonacci numbers and the golden mean are

not merely numerological curiosities. Rather, this
scaling
pattern appears to be built into a number of biological
structures, or perhaps more appropriately, such struc
tures appear to be constructed in part from a Fibonacci
blueprint (1, 5). Fibonacci scaling, for example, has been
noted in the arrangement of leaves on the stems of
certain plants. In humans,
the ratio of the total height
(head to toe) to the height from navel to toes also
1.62. More
approximates
recently we have described
Fibonacci scaling in the lung (6).
A notable feature of the bronchial tree mentioned
earlier is its asymmetry. The trachea, for instance, di
vides into a longer (left) and shorter (right) mainstem
branch, and this asymmetric partitioning continues over
multiple generations of bronchial tubes. If the architec
ture of the lung is governed in part by Fibonacci scaling
principles, one might anticipate that the ratio of the long
to short tube length at each bifurcation would be approx
imately equal to , or alternatively that the ratio of short

to long tubes

Ia) would be nearly equal to 1/

(0.618...
). To test this hypothesis, we reviewed previ
of bronchial casts. The
ously published measurements
classic study was performed by Weibel
and Gomez
the first detailed measurements
of
(7, 8), who made
human lungs in the early 1960s. While complete data
relating to this question were not reported, these investi
gators did record that the mean ratio of short to long
tube lengths for the fifth through the seventh genera
tions of a single human bronchial tree was 0.62. This
ratio is intriguingly close to that predicted for a Fibonacci
scaling process.
To further test the relevance of the golden mean

Generations

to

in the bronchial tree

2. In Wiebel's

the airways of the bronchial

tree
scheme,
to successively
numbered
The trachea is
generations.
are generation
branches
0, the two mainstem
1, and the
generation
increases with each bifurcation. Other schemes
generation number
Figure

belong

have

been

proposed

morphogenetic

356

(30,32),

development

but Weibel's
of the lung

system
(32).

reflects the

bronchial architecture, we analyzed the ratios of short to

long lengths for the first seven generations of bronchial
tubes in the lung casts of two humans, two dogs, a rat,
and a hamster, using data collected in the 1970s by Raabe
and colleagues
ratios were also sugges
(9). The mean

tivelyclose to l/

(rangingfrom0.62 to 0.67) ineach of

the six casts (6).

Fibonacci proportionality
is one example of the
or
of
which emerges as
sameness,
similitude,
concept
the central theme in Thompson's
studies of biological
structure and function. In the case of the golden mean,
there is a sameness in proportion from longer to shorter
or in the ratios of growing numbers. Al
dimensions,

thoughThompson spends only a fewpages specifically

in nature, he devotes
sequences
describing Fibonacci
much of his attention to an apparently universal princi
this type of scaling. A striking
ple which underlies
illustration is provided by the geometry of spiral sea
shells such as the nautilus, shown in Figure 3. The
nautilus follows a pattern originally described by Des
cartes in 1683 as the equiangular spiral and subsequently
by Jakob Bernoulli as the logarithmic spiral. Bernoulli, in
fact,was so taken with this curve that he called it spira
mirabilis and allegedly requested that it be inscribed on
his tombstone (5). The special feature of this type of
spiral is that it follows the principle of similitude. As
Thompson wrote: "In the growth of a shell, we can
conceive no simpler law than this, namely that it shall
widen and lengthen in the same unvarying proportions:
and this simplest of laws is thatwhich nature tends to
follow. The shell, like the creature within it, grows in
size but does not change its shape and the existence of
this constant relativity of growth, or constant similarity
of form, is of the essence, and may be made the basis of a
definition, of the equiangular spiral" (1).
This spiral shape is not restricted to the nautilus but
was
inmany other shells. The
catalogued by Thompson
shell-like structure of the inner ear, the cochlea (from the
Greek word for snail), also appears to follow a similar
to our knowledge,
the
type of spiral. Surprisingly,
relevance of this anatomic shape to physiologic function
has not been pursued.
The ability to preserve basic
proportions is remarkable; the lung, by contrast, seems
riddled with structural variations.
In 1915, two years prior to the first edition of
book, On Growth and Form, a German
Thompson's
Fritz
Rohrer, reported some of the earliest
physiologist,
of
investigations
scaling in the bronchial tree (10). Rohrer
assumed
that the bronchial tree is homogeneous
and
that the volume of air in a tube is divided equally
between the two daughter tubes in the next generation.
He argued that since the diameters decrease
by about the
same proportion from one
generation to the next, diame
ter should decrease
exponentially with generation num
ber. Over half a century after Rohrer formulated this
principle, the same exponential scaling relationship was
in their classic studies.
reported by Weibel and Gomez
The hypothesis of exponential scaling can be tested
by plotting the logarithm of the mean diameter at any
given bronchial generation versus the generation num
ber, as in Figure 4. The straight line obtained from
Weibel and Gomez's data for the first ten generations of
tubes appears to support this model. However, when

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Classical

scaling: similitude

3. The

of similitude
is
principle
or
in the logarithmic,
equiangular,
spiral (in polar coordinates,
r ? k?). An
in such a
log
organism
growing
spiral retains its original proportions while
its size increases, as can be seen at right in
the shell of the pearly nautilus
(Nautilus
cross section). The cochlea, a
pomptlius,
bony, fluid-filled canal that transmits
inner ear
vibrations
through the human
Figure

exemplified

{above),
spiral.

seems

also

(Photograph

to follow a shell-like
by Bill Sacco.)

we examine data for the entire span of the bronchial tree

(more than twenty generations), a remarkable systematic
deviation appears. Weibel
and Gomez noted this dis
a
and
it
to
attributed
crepancy
change in themechanism
of flow through the bronchial
tree, from minimum
resistance near the beginning to molecular diffusion at
the end. We will show how this physiologic deviation
can be accounted
from exponential behavior
for by
invoking a new scaling mechanism.
The bridge between
the classical scaling principles
new
outlined
and
this
is Thomp
just
scaling mechanism
son's theme of similitude, a notion encountered
in the
golden mean and the logarithmic spiral. Fibonacci scal
ing did prove helpful inmodeling one aspect of bronchi
al asymmetry?the
relative lengths of the tubes. Howev
er, the simple scaling function implicit in the classical
notion of similitude cannot adequately describe the full
in the lung.
range of structural variability apparent
Classical scaling principles, as noted earlier, are based on
the notion that the underlying process is uniform, filling
an interval in a smooth, continuous fashion. The bron
chial system, however, is jagged and irregular, with no

single, characteristic scaling factor. At the same time, the

smaller-scale structure of die lung resembles the larger
scale structure, a type of "setf-sim?arity.'' Clearly, a new
scaling principle that can generate richly detailed, het
but self-similar architecture would be an
erogeneous,
attractive candidate to test on a physiological structure as
complex as the lung.

tree branches
in
out, its tubes decrease
Figure 4. As the bronchial
size. A theory consistent with the principle
of similitude predicts
that their diameters
should decrease
by about the same ratio from

one generation
to the next. If the ratio were \, for example,
the
relative diameters would
be 1, \, \, \, and so on?an
exponential
and
decline. This semilog graph shows measurements
from Weibel

of bronchial
tubes in the human
(7) for 23 generations
lung.
is a straight line. The anatomic data (dots) fit this
after which
prediction
they
closely until about the tenth generation,

Gomez
The

prediction

deviate

systematically

from an exponential

decline.

1987 July-August 357

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Beyond similitude: Self-similarity,

fractals, and

renormalization

To make
the transition from classical similitude to the
we must backtrack in our
new scaling mechanism,
historical sketch and return to the late nineteenth centu
addressed the
ry. Itwas at this time thatmathematicians
that
of
structures
have
features
of
self-similarity
problem
but lack a characteristic scale. Although
they were not
motivated by physiologic concerns, theirwork has obvi
ous relevance to the type of self-similar branching found
in the lung. At any generation of the bronchial treewe
can consider the distribution in tube sizes as constituting
a mathematical
the bronchial tree,
set. To understand
therefore, we need a model of a set that can be progres
sets
sively "thinned out." The study of such self-similar
was initiated in the previous century by themathemati
cian Georg Cantor, and they now bear his name (11).
A simple example of what has come to be called a
Cantor set can be constructed starting from a line of unit
length and systematically removing segments from spec
ified regions. Figure 5 shows that removing the middle
third of each line segment at each generation produces a
more depleted structure at the next generation. When
is taken to the limit of infinitelymany
this procedure
as a
generations, the resulting set of points is referred to
The universe:

set. The line segments, like the bronchial tube

sizes, become smaller and smaller, and the set of points
at the limit of this trisecting operation is not continuous.
How can one characterize it?
In the early 1900s, Felix Hausdorff determined that
one could
a set by means of a fractional
classify such
Hausdorff's
(4).
reasoning can be fol
dimensionality
lowed by considering the distribution of "mass-points"
in a spherical volume of space, where a mass-point
is a
convenient fiction used to denote an indivisible unit of
at some point in space. One way of
physical mass
a
ofmass-points having a fraction
distribution
picturing
al dimension
it from a great
is to imagine approaching
distance. At first, the mass will seem to be in a single
cluster. As one gets closer, itwill be observed that the
cluster is really composed of smaller clusters, such that
each smaller cluster, upon approaching, will seem to be
composed of still smaller clusters. This apparently con
trived example of self-similarity describes the distribu
tion of stars in the heavens, and the Hausdorff dimen
sion has been determined by astronomical observations
to be approximately 1.23 (12). The box at the bottom of
this page describes how the totalmass of such a cluster is
related to itsHausdorff dimension.
In a similar way the Cantor set can be characterized
Its Hausdorff dimension, or
by a fractional dimension.
Cantor

infinitelynesting spheres
The totalmass of a distributionofmatter inspace ispropor
tional to rdtwhere ris a unitof lengthand dis the dimen
sion of space occupied by the object inquestion. Using the
standard notation formathematical functions,we can write,
forunit-mass density,M(r) = r d; forexample, themass of
a solid sphere?say a beach ball of radius r filleduniformly
with sand?is proportional to r3. In the absence of other
knowledge it is usually assumed that thematter is uniformly
distributed in the available space and thatd is equal to the
Euclidean dimension of the space. Let us suppose, howev
er, thaton closer inspectionwe observe that the sand is not
distributed,but instead clumped indistinctspheres
uniformly
of radius rib, each having a mass that is 1 la smaller than
the totalmass.
visualized as a beach ball
Thus, what we had initially
with sand turnsout to resemble one filled
filleduniformly
with basketballs, each of the basketballs being filleduni
with sand. We now examine one of these basketballs
formly
and findthat itconsists of still smaller spheres, each of radi
us rib2and each having a mass 1 /a2smaller than the total
mass. Now again the image changes, so that the basket
balls appear to be filledwith baseballs, and each baseball is
uniformlyfilledwith sand. Ifwe assume that thisprocedure
of constructingspheres within spheres can be telescoped
we obtain, after telescoping operations, M(r)
indefinitely,
n=
=
This relationyields a finiteval
M(rlbn)a
r^lb"*).
ue for the totalmass in the limitof becoming infinitely
=
(Ina)/(ln b). This fractionalvalue ford is
largeonly ifd
called the Hausdorff (or fractal)dimension of themass dis
persed throughoutthe Euclidean volume of radius r.The
Hausdorffdimension can thereforebe distinct fromthe Eu
clidean dimension of the space inwhich themass isem
bedded.

358

American

Scientist,

Volume

75

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Figure 5. A Cantor set can be generated

by cutting out the middle
third of a line segment at each generation
(z). The set of points
in the limit as
remaining
infinity is called a Cantor
approaches
set. The

each
and

The Cantor set: infinitelydivided lines

line segments are distributed more and more sparsely with

and the resulting set of points is both discontinuous

iteration,

inhomogeneous.

using the term introduced in recent years by Mandelbrot

can again be specified by
(4), the fractal dimension,
invoking the fiction of mass-points.
Imagine that the
a line of length
mass-points are initially distributed along
r. In
the line, we
out
the
third
middle
of
cutting
redistribute themass along the remaining two segments
so that the totalmass of the set remains constant. At the
next stage, where the middle third is cut out of each of
these two line segments, we again redistribute themass
so that none is lost. We now define the parameter a as
the ratio of totalmass to the mass of each segment after
one
since each
In this example,
trisecting operation.
= 2. We
mass
half
the
of
receives
its
segment
parent, a
also define a second parameter, b, as the ratio of the
length of the original line to the length of each remaining
=
segment. Since we are cutting out themiddle third, b
3. The parameter a gives us an idea of how quickly the
mass is being concentrated, and the parameter b gives us
a
comparable idea of how quickly the available space is
d, of the
being thinned out. The fractal dimension,

Cantor set is theratioof logarithms(Ina)/(Inb),

resulting

A physiological

II II II II

II

II

fili

II fi

II
II II

II
IMI

which in our example is (In2)/(ln3) = 0.6309.

There are several ways inwhich one can intuitively
make sense of such a fractional dimension. Note first
that in this example d is greater than zero but less than
one, the dimension of a line in Euclidean geometry. This
sense when one thinks of the Cantor set as a
makes
physical structure with mass: it is something less than a
continuous line, yet more than a vanishing set of points.
Justhow much less and more is given by the ratio (Ina)/
(Inb). l?a were equal to b, the structure would not seem
to change no matter how much we magnified
our
mass
as
the
would
line;
original
clump together
quickly
as the
see a one
length scaled down, and we would
line on every scale. If a were
dimensional
Euclidean
than
b, however, we might see a branching or
greater
flowering object, one that seemed to develop finer and

fractal: the infinitelybranching tree

levels
of
Figure6. Fractalsare a familyof ?hapea ta^
detail, as observed in?ie Cantor set ajitf^
spheresoil ?ie facingpage. In thetracta^
^
of each branch continuesbranchingover in^^^ on
mailer and smaller scales, and eadi ina^ul^^ sroaller^^e
structureis similarto the largerforni,a propertycalled self
As the fractal(Hausdorff)dimension increasesbetween
similarity.
one and two deft toright in thefigure), the treesproutsnew
blanchesmore andmore vigorously.Fractalobjects are ubiquitous
in tilephysicalworld, seen, forexample, jutthe self-sirn?ar

accretionsof cumulus cl^ds, in turbulentflowsm fluidi, and in

me patterrungof
Hie orgart?c^treelikefractalsshown here bear a
temperature.
strikingresemblanceto many physiological structures.(Fromref.4.)
1987 July-August

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359

The fractalmathematical

function: infiniteharmonic overtones

not look likethe branching fractalsof Figure 6, butmore like
the irregularlineon a map representinga very rugged sea
coast.

The German mathematician KarlWeierstrass cast the argu

ment for fractals intoa particularmathematical form.His
was to construct a series representationof a continu
intent
ous, nondifferentiablefunction.His functionwas a superpo
sition of harmonic terms: a fundamentalwith frequency <*>0
and unitamplitude, a second periodic termof frequency
b(?0 with amplitude Ma, a thirdperiodic termof frequency
b^o with amplitude 1 la2, and so on. The resultingfunction
is an infinite
series of periodic terms,each termofwhich
has a frequency that is a factorb largerthan the preceding
termand an amplitude that is a factorof 1 la smaller. Thus,
ingiving a functionalformtoCantor's ideas,Weierstrass
was the firstscientist to construct a fractalfunction.
Note that forthisconcept of a fractalfunction,or fractal
set, there is no smallest or characteristic scale. For b > 1 in
the frequency
the limitof terms,as
approaches infinity,
and there is no highest frequencycon
b%o goes to infinity,
tributionto theWeierstrass function.Of course, ifone thinks
in termsof periods rather than frequencies, then the shor
test period contributingto the series is zero.
In the drawing above, the lightgray curve shows the
contributionto theWeierstrass functionof a fundamental
frequency 0. The dark gray curve is the sum of the first
two terms in the series when a = 4 and b = 8, so that the
fractaldimension isd = ?, close to the value used in the
Cantor set shown inFigure 5. The black curve shows this
series with the first36 terms contributing.
Consider now what is imphedby the lackof a small
est scale inperiod, or equivalents by the lackof a largest
scale in frequency. Imagine a continuous lineon a two
dimensional Euclidean plane and suppose that the linehas
a fractaldimension greater than unitybut less than two.
How would such a curve appear? In thiscase, we are su
perimposing smaller and smaller wiggles; the curve would

360

American

Scientist,

Volume

At firstglance, thiscurve would seem to be a ragged

linewithmany abrupt changes indirection,as in the first
we now magnify a small regionof the line,
drawing below. If
as in the second drawing,we see that the enlarged region
appears qualitatively the same as the original curve. Ifwe
now magnify a small regionof thisnew line,as in the third
drawing,we again obtain a curve that is qualitatively indis
tinguishable fromthe firsttwo.
This procedure can be repeated indefinitely,
just as in
the geometric example of infinitely
nesting spheres, and the
behavior of themathematical function is analogous to the
discontinuous, inhomogeneous clumping ofmatter inspace.
The equivalence of the functionfromone scale to the next
of the
(its self-similarity)isanalogous to the self-similarity
nesting spheres and of the fractals inFigure 6, and the
measure of the degree of self-similarityin theWeierstrass
function(in termsof frequencyand amplitude) is precisely
the fractal,or Hausdorff, dimension: (Ina)/(In b).
Because of the infinitelayersof detail, one cannot
draw a tangent to a fractalcurve, which means that the
function,although continuous, is not differentiate. Italso
means that themore termsone allows to contribute to the
function(themore accurately one maps the coastline), the
longer the curve becomes, and there is no upper limitto its
length.

tim?

'
:v -*' ' "'?

75

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finer structure under magnification;

we might see some

thinglikethe fractaltreesofFigure6,which burstout of

a one-dimensional
space but do not filla two-dimension
al Euclidean plane. Again, the precise character depends
on the value of d: the tree at the left has a fractal
dimension barely above one, and thus it is wispy and
broomlike; as the dimension increases between one and
two, the canopy of branches becomes more and more
lush.

To explore the physiological implicationsof these

concepts, we need to find out how such a self-similar set

of points can be generated, or in a more general case
how a curve with a fractal dimension can be constructed.
Cantor's
the representation of
original interest was
mathematical
functions by means
of a trigonometric
series whenihe
function is discontinuous or divergent at
a set of
points. Although he became more interested in
how to choose
such a set of points than in their
representation as a series, another German mathemati
cian, Karl Weierstrass, who was a teacher and later a
colleague of Cantor, was keenly interested in the theory
of functions and suggested to him a particular series that
is continuous everywhere but differentiable nowhere.
This series is illustrated in the box on the facing page.
For a function to be differentiable, one must be able
to draw a weU-determined,
straight-line tangent to every
point on the curve defined by the function. Functions
describing curves forwhich this tangent does not exist
lack certain of the properties we have come to expect
from mathematical
representations of physical proper
ties. For example, in the empirical science of thermody
namics, one often differentiates certain functions to
determine the physical properties of the materials, such

as how readily they absorb heat or how easily they

conduct electricity. In some circumstances, however, the

as in
becomes discontinuous,
property being measured
the case of themagnetization
of a piece of ironwhen the
temperature approaches a critical value called the Curie
temperature (13). At this critical temperature, the mag
netic susceptibility?that
is, the change inmagnetization
induced by a small applied field?becomes
infinite. Thus
the magnetic susceptibility is a nonanalytic, or singular,
function of the temperature. We find that such nonan
alytic functions tend to be exceptional in the physical
sciences, although thismay stem in part from a habit of
as intractable. At any rate,
avoiding such problems
behavior
appears to be more the rule than
nonanalytic
the exception in the social and medical sciences. In order
to understand
such singularities, we shall explore the
function.
implications of theWeierstrass
The dominant behavior of the self-similar Weier
strass function is expressed by the functional relation
=
F(z)
F(bz)/a, where a and b are scaling parameters
is
analogous to those we defined for the Cantor set and
to
the
number
of
trisecting operations per
analogous
formed. To interpret this relation, imagine that you are
examining the properties of the function on the magni
fied scale te. What you will see at this smaller-scale
is
the same function observed at some larger-scale
but
with details that are scaled (increased or decreased) by
the factor a. This is the mathematical meaning of self
similarity. The nonanalytic behavior of magnetic suscep
tibility is described by this scaling relation, often called
the renormalization group transformation (13, 24, 15).

7. When we replot Weibel

and Gomez's
data from Figure
diameter
log-log graph (top), we find that average bronchial
In
not exponential,
follows inverse power-law,
addition
scaling.
to be a harmonic
there appears
(periodic) variation of the data

Figure
on a

points about
which makes
measurements
and hamsters
bottom
observed

line. The harmonic variation,

the power-law
regression
the series of dots appear wavy,
is also present in
tube diameters
obtained
of bronchial
for dogs, rats,
and
(center) taken by Raabe
shows the close fit between

graph
in the bronchial

the renormalization

colleagues
the mean

tubes of a hamster

and

(9). The

diameters

those predicted

by

(fractal) model.

1987 July-August 361

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Indeed, renormalization group theory, through thework

of Kenneth Wilson,
found its first successful application
in the study of phase transitions (critical phenomena)
such as magnetization.
Because we now have a mathematical expression for
the property of self-similarity, we can predict how the
function varies with z. The renormalization group trans
formation can be solved to yield F(z) = A(z)z ,where the
power-law index dmust be related to the two parameters
a and b in theWeierstrass
series expansion by d = (Ina)/
(Inb). Also, since the function A(z) must be equal to
A
), itwill be periodic in the logarithm of the variable z,
with period In b.
the Weierstrass-renormalization
Thus,
equation
leads to a power-law relationship: F(z) is proportional to

Themost excitingprospectfor thenew

scaling is thatitwill providea unifying
themetomany investigations
which up
to now have been considered unrelated

raised to the power d, the fractal dimension. This is

to the example of the clustering spheres,
analogous
is
where the total mass of a distribution of mass-points
proportional to the dominant power-law behavior deter
mined by the radius r raised to the power d. The
is a consequence of the
algebraic increase of F(z) with
z. Note that ifeither
with
the
of
function
scaling property
a or b is less than unity (but not both), then the sign of d
will change; that is to say, the dominant behavior of F(z)
will be an inverse power law, \lzd. Finally, observe that
in addition to the dominant power-law behavior deter
func
mined by the fractal dimension d, theWeierstrass
tion has a slowly varying (periodic) coefficient, A(z).
To apply the concept of fractals and renormalization
group theory to physiology, we require one additional
extension into the arena of fluctuations and probability
(3, 26), since physiological data sets are usually under
stood in terms of averages. We can also interpret F(z) as a
random function, so that in analogy with theWeierstrass
function the probability density associated with the
random variable satisfies a scaling relation. Thus the self
similarity that arises in the statistical context implies that
is
the graph of the random function F(z) versus
statistically equivalent at all scales rather than being
geometrically equivalent. One can visualize this by not
function shown
ing the self-similarity of theWeierstrass
in the box on page 360. In the case of a random function,
the wiggles are random fluctuations that are statistically
as one
indistinguishable
telescopes sections of the time
series.

Self-similar physiological structures

How do these apparently abstract and interrelated no

tions of self-similar scaling, renormalization group the
ory, and fractals apply to the architecture of the lung?
The classical model of bronchial tube scaling, as we saw,
predicts an exponential decay inmean diameter. How
ever, the observed anatomy diverges markedly from the
362

American

Scientist,

Volume

predicted exponential scaling beyond the tenth genera

tion of bronchial tubes. The classical theory assumed the
existence of a characteristic scale governing the decrease
in bronchial diameters across generations. If, however,
the lung is a fractal structure, no characteristic scale will
be present. Instead there should be a distribution of
scales contributing to the variability in diameter at each
generation, each scale having a different probability of
occurrence (in statistical terms, differentweighting). The
dominant variation of the average bronchial diameter
with generation number should then follow power-law,
not exponential, behavior (27).
led to exponential
The traditional models which
the
scaling deliberately neglected
variability in bronchial
dimensions at each generation and used only average
values for the tube diameters. The fractal (renormaliza
tion) model, on the other hand, based on a multiplicity
of scales, provides a mechanism
for this physiologic
we
now
If
the
renormalization
variability.
interpret
=
as
the diameter of
function
F(z)
F(bz)/a
(Weierstrass)
the self-similar bronchial tree at the zth generation, then
the parameter b is a measure
of the intervals between
scales that contribute to variations in diameter and the
the importance (weighting) of a
parameter a denotes
particular scale relative to other contributing scales.
in the
Thus, in contrast to the single scale assumed
traditional model of the lung, the fractalmodel
implies
that an infinite sequence of scales, each a factor of b
smaller than its neighbor, contributes to the structure.
Each such factor, bn, isweighted by the coefficient llan.
This is exactly analogous
to the weighting of different
in
the
Weierstrass
function. Therefore, the
frequencies
=
average diameter at the zth generation r(z)
A(z)lzd,
where d is a fractal dimension
associated with the
variability in bronchial tube diameter and A(z), as noted
earlier, is a periodic function. The fractalmodel of the
in average
lung, therefore, predicts that the decrease
bronchial tube diameter from one generation to another
will follow a power-law
by a
relationship, modulated
variation.
periodic
To test this new model of the lung, we can simply
and Gomez's
data using log-log graph
replot Weibel
on
a
which
inverse
paper,
pure
power-law relationship
will be represented as a straight linewith negative slope.
As is apparent from Figure 7, the data points do follow
the predicted scaling. However,
the line appears wavy,
not straight. This waviness
is due to an apparent har
monic (periodic) variation around the power-law regres
sion line, as anticipated from the renormalization func
we
tion. When
the data from Raabe
and
plotted
a
in
measurements
similar
of
way, using
colleagues
bronchial tube diameters from three other species, the
same kind of
harmonically modulated power-law behav
iorwas observed (27). Furthermore, their data showed
the same type of scaling for bronchial tube lengths.
This new scaling mechanism
to capture
appears
some fundamental
of
the
architecture
of
properties
lungs, properties that hold true from one species to
another and are not encompassed
by traditional models.
At the same time, as we have seen, the bronchial tree
does seem to incorporate one type of classical scaling,
a fuller
namely, the golden mean. However,
description
of bronchial variability and organization goes beyond
similitude to the novel concept of renormalization, based

75

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The human heart as a fractal

nary artery
great
cardiac
vein
right con

tricuspii

chordae
tendineae

anterior
cardiac
veins

leftpapillary
muscle

inferior
vena cavai
descending

thoracic aorta

right

ventricle

leftventricle

bundleofHis
bundle branch

bundlebranch
right

Figure 8. The fractalgeometryof theheart is apparent fromseveral

perspectives.

Inside

the cardiac

chambers,

the tricuspid

and mitral

valves are attached to thepapillarymuscles with

branching strands

Purkinjefibers

of connective
vascular

tissue, the chordae tendineae

(above). A self^imilar
network
(above, right) consisting of coronary arteries and

veins distributesand collects theheart's own blood

supply.
Furthermore,
an irregular,

the cardiac

fractal neural

impulse is transmitted to the ventricles via

the His-Purkinje
network,
system (right).

on a
multiplicity of scales. The final product, which we
have dubbed the "fractal/Fibonacci
lung tree/' provides
a remarkable balance between
physiological order and
chaos.

Not surprisingly, fractal

anatomy is not limited to
the lung (4,15,18,19).
The vascular system, like the
bronchial tree, is a
branching network of tubes with
in the early 1950s, intro
many apparent scales. Cohn,
duced the notion of an
"equivalent bifurcation system"
to describe the vascular tree
(20). This was among the
firstphysiological
applications of the idea of self-similar
ity, predating the formal description of fractals.
Many other fractal-like structures in physiology are

also readily identifiedby theirmultiple levels of self

similar
branchings or foldings?for
example, the bile
duct system, the
urinary collecting tubes in the kidney,
the brain, the
lining of the bowel, neural networks, and
the placenta. The fractal nature of the heart
(18,19) is
particularly striking (Fig. 8). The cardiac surface is tra
versed and penetrated
a
by
bifurcating system of coro

nary arteries and veins. Within its chambers, branching

strands of connective tissue, called chordae tendineae,
anchor themitral and
tricuspid valves, and the eledxical
impulse is conducted by a fractal neural network, the
system, embedded within themuscle
His-Purkinje
(19).

Fractal time
Our review has focused on the relevance of fractals to
static structures. However,
structures like
physiologic
the bronchial tree are static
only in that they represent
the "fossil remnants," or casts, of an active
developmen
tal process.
It seems reasonable
to suspect that the
of the lung is itself a
morphogenesis
dynamic fractal
process, a type of critical phenomenon
evolving over
time (17,18).
In this regard, the new fractal
scaling
mechanism has interesting implications for the
develop
ment of
complex but stable structures using a minimal
code based on
self-similarity. One of the many chal
for
future
research will be to unravel themolecu
lenges
1987 July-August 363

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larmechanisms whereby self-similar scaling information

is encoded and processed. The evidence for these scaling
principles thatwe have seen in the bronchial data from
several species suggests theworking of some potentially
universal embryological principle.
In addition tomorphogenesis,
other complex phys
iological processes may also require fractal concepts for
their complete description. A fractal process is one that
cannot be characterized by a single scale of time (a single
frequency), analogous to a fractal structure like the lung,
which does not have a single scale of length. Instead,
fractal processes have many component frequencies (a
broad-bandwidth
spectrum). Fractal dynamics can be
detected by analyzing the output of a process (a time
series) using spectral analysis techniques. If the spec
trum shows inverse power-law
scaling, the higher the
its power. We recently
the
lower
frequency component
related the fractal geometry of theHis-Purkinje system of
nerves in the heart to the inverse power-law spectrum of
the electrocardiogram
(19). Broad-bandwidth
spectra
with inverse power-law
distributions have also been
reported for other physiological processes, ranging from
the electrical activity of a single neuron to the beat-to
beat variability in heart rate seen in normal individuals
(22, 22). This kind of scaling suggests that the processes
that regulate different complex physiological
systems
over time are also governed by self-similar (fractal)
(18, 19).
scaling mechanisms

Fractal scaling and disease

Of obvious interest are the potential medical implications

of these new scaling concepts (28). Healthy physiological
systems apparently require a balance between order and
variability. Available data suggest that such constrained
can be
randomness
represented by broad-bandwidth
with
inverse
spectra
power-law distributions. Some dis
eases may be associated with a disruption in this normal
fractal scaling (28).
How will these scaling pathologies be evidenced? At
present, only preHminary answers can be given to this
important question. A number of diseases are character
ized by a loss of the variability associated with fractal
structure and fractal function (28, 29, 23). This decrease
in healthy variability will be reflected in a narrowing of
the frequency spectrum?a
"loss of spectral reserve"
(28). Variability in heart rate, for example, ismodulated
by the interaction of the sympathetic and parasympa

(B.A. physics, SUNY Buffalo, 1965;Ph.D.

physics, University
a
visiting
of Rochester, 1969J is the director of the La folia Institute and
research physicist at the Institute forNonlinear Science, University of

Bruce J.West

are in the
nonequilib
California, San Diego. His current research interests
rium statistical mechanical description of complex systems, including

quantum
ofcoherent
geophysical
fluidflowfieldsand thepropagation

structures in biopolymers, as well as biomedicai phenomena. Address: INLS,

L.
R-002, University of California?San
Diego, La folla, CA 92093. Ary
Yale Medical School, 1974)
Goldberger (A.B. Harvard College, 1970; M.D.

isAssistant Professor ofmedicine at Harvard Medical

School and codirector
of theArrhythmia and Electrocardiography Laboratories at Boston 's Beth
Israel Hospital. His current research is concerned with the application of
nonlinear dynamics to physiology and clinical medicine, and in particular to
the problem of sudden cardiac death. Address: Beth Israel Hospital (GZ
435), 330 Brookline Avenue,

364

American

Scientist,

Boston, MA

Volume

02215.

thetic branches of the autonomie nervous system. Dis

eases that interfere with autonomie function, such as
diabetes mellitus, and certain drugs have been shown to
decrease the normal variability in heart rate (18).
In the most severe cases of pathology, this loss of
variability, or spectral reserve, may eventually lead to
the appearance of highly periodic (predictable) behavior.
The medical
literature is replete with examples
of
For
low
(23, 24).
"pathological periodicities"
example,
frequency, periodic fluctuations in heart rate and respira
tionmay be a prominent feature in patients with severe
congestive heart failure (23) as well as in the fetal distress
syndrome (25, 26). The detection of a loss of spectral
reserve and the onset of
pathological periodicities in both
adults and infants at risk for sudden death promises to
to cardiovascular monitoring
provide a new approach
similar
(18, 23). Furthermore,
techniques may provide
novel ways of monitoring other systems. For
example,
an inverse
power-law spectrum characterizes the appar
ently erratic, daily fluctuations in counts of neutrophils

(a typeofwhite blood cell) inhealthy subjects (27). In

contrast, periodic (predictable) fluctuations in neutrophil

counts have already been detected in certain cases of
chronic leukemia (28). Spectral analyses of fluctuations in
blood counts may provide a useful means of identifying
states and also perhaps of following pa
preleukemic
tients' responses
to chemotherapy.
Finally, a loss of
physiological variability in a variety of systems appears
to be characteristic of the
aging process (29).
In all these areas of medical
research, there is a
common
theme.
physiological
Complexity is the salient
feature shared by all the systems we have discussed?a
feature that is attracting more and more attention in
physical systems as well. Until today, scientists have
assumed
that understanding
such systems in different
various physiological
contexts, or even understanding
systems in the same organism, would require completely
differentmodels. The most exciting prospect for the new
scaling is that itwill provide a unifying theme tomany
investigations which up to now have been considered

unrelated.

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