Fractal-based image texture analysis of

trabecular bone architecture

C. Jiang I R.E. Pitt 2 J.E.A. Bertram 2 D . J . Aneshansley 3
1Computer Design and Applications, Analogic Corporation, 8 Centennial Drive, Peabody, MA 01960, USA
2Department of Agricultural and Biological Engineering, Cornell University, Ithaca, NY 14853, USA
3Anatomy Department, Cornell University, Ithaca, NY 14853, USA

Abstract--Fractal-based image analysis methods are investigated to extract textural

features related to the anisotropic structure of trabecular bone from the X-ray images
of cubic bone specimens. Three methods are used to quantify image texture/
features: power spectrum, Minkowski dimension and mean intercept length. The
global fractal dimension is used to describe the overall roughness of the image
texture. The anisotropic features formed by the trabeculae are characterised by a
fabric ellipse, whose orientation and eccentricity reflect the textural anisotropy of the
image. Tests of these methods with synthetic images of known fracta/ dimension
show that the Minkowski dimension provides a more accurate and consistent
estimation of global fracta/ dimension. Tests on bone x-ray (eccentricity range
0.25-0.80) images indicate that the Minkowski dimension is more sensitive to the
changes in textural orientation. The results suggest that the Minkowski dimension is
a better measure for characterising trabecular bone anisotropy in the x-ray images of
thick specimens.

Keywords--Textura/ anisotropy, Fabric ellipse, Minkowski dimension, Power spectrum,

X-ray
Med. Biol. Eng. Comput., 1999, 37, 413-418

1 Introduction X-ray radiographs of trabecular bone have been shown to

contain information about bone mineral distribution and trabe-
BIOMECHANICAL STUDIES have shown a clear association
cular architecture CRUTTIMANNet al., 1992; OXNARD, 1993).
between bone elastic properties and apparent density (CARTER
Fractal analysis using the power spectrum has been used to
and HAYES, 1977; KEAVENYet al., 1993). Significant correla-
characterise the global roughness of these images (BERRY et al.,
tions have been found between mechanical properties and
1994; BENHAMOU et al., 1994; SOUTHARDet al., 1996). The
apparent density determined from non-invasive imaging techni-
Minkowski dimension is a class of fractal dimension that can be
ques based on quantitative computed tomography (BENTZENet
used to characterise image textures and can be computed using
al., 1987; HVID et al., 1989). However, only 40-70% of the
mathematical morphology (SERRA, 1982; HARALICK et al.,
variation in mechanical properties has been explained by
1987; MARAGOS, 1994).
apparent density. Thus, in clinical practice, it has been difficult
SAMARABANDUet al. (1993) used morphological fractals to
to separate patients with and without osteoporosis using density
extract textural information from x-ray radiographs of bone.
alone, because of the overlap in the distributions of non-
ACHARYA et al. (1995) compared the performance of the
invasively measured bone density of healthy and osteoporotic
morphological method to describe trabecular bone structure
individuals (RIGGS et al., 1981; MUNDINGERet al., 1993).
with box-counting, power spectrum and wavelet methods. The
Trabecular bone architecture has been shown to be an
morphological estimator performed better than the other esti-
important factor affecting the mechanical properties of bone.
mators, especially for smaller window sizes. These studies were
WHITEHOUSE(1974) used mean intercept length to measure the
primarily focused on characterising the global roughness of
microscopic structural anisotropy oftrabecular bone sections; a
image texture. Use of fractal analysis to extract the anisotropic
polar diagram of mean intercept length as a fimction of testing
features from trabecular bone x-ray images has not been
angle produced an ellipse. HARRIGAN and MANN (1984)
intensively studied.
extended mean intercept length measurements to three dimen-
The objectives of this study were to estimate global and
sions by extracting ellipses from sections cut from the perpendi-
directional fractal dimensions from tmbecular bone images
cular faces of a cubic specimen. These methods are usually
obtained from thick sections, and to compare the ability of the
invasive, because the morphometric parameters are measured on
Minkowsld dimension, power spectrum and mean intercept
machined thin sections. Also, unless multiple sections are used,
length methods to characterise bone textural anisotropy.
the non-homogeneity of tmbecular structure through the
specimen thickness is not taken into account (SNYDER et al.,
1993).
2 Materials and m e t h o d s

Correspondence should be addressed to Dr. ChungshengJiang:
email: cjiang@ana/ogic.com
First received26 June 1998and in final form 2 February 1999
9 IFMBE: 1999
Medical & Biological Engineering & Computing 1999, Vol, 37
2.1 Sample collection and data analysis
Bovine femurs and tibias were harvested from an 18-month
old bull, a three-year old steer and an eight-year old cow.
Trabecular bone blocks (1.2-2.0 cm in cross section and 1.2-
413
4.0 cm in length) were cut from all possible locations with a band
saw, and 70 cubic specimens (8 • 8 • 8 mm) were machined
from these blocks using an Isomet low-speed bone saw. The
anatomical axis was marked on the bone blocks and on each
specimen at each step in the process.
An x-ray radiograph was taken for each specimen at each of
the three orthogonal orientations. A Faxitron x-ray system* was
used to collect bone radiographs on X-Omat TL filmt. After
exploratory tests, the x-ray system was set to 40 kVp, with an
exposure time of 65 s for all specimens. The radiographic images
were digitised using a custom-built system that included an
adjustable light source~:, an image sensor, a lens with adjustable
field of view and a frame grabber board and host computer.
Image size was set to 256 • pixels, corresponding to
6.5 x 6.5 mm, or 25 l~m per pixel. Further details of sample
preparation, x-ray image collection and image digitisation can
be found in JIANG (1997).
To evaluate the accuracy and consistency of different methods
of computing fractal dimension, synthetic images with known
fractal dimension were generated using the random midpoint
displacement algorithm (Voss, 1985; SAUPE, 1988; VOSS,
1988). The power spectrum was computed using the discrete
Fourier transform with IDL software**, and all other calcula-
tions were carried out using algorithms written in C. Statistical
analyses were performed using Minitab.

2.2 Computation of fractal dimension using power spectrum

Global and directional fractal dimensions were estimated
using the procedures suggested by ANGUIANO et al. (1993). b
The power spectrum of an image was represented in polar co- Fig. 1 Typical digitisedX-ray image of trabecular bone specimen in
ordinates as PS(r, 0), where r is discrete frequency ranging from one plane. (a) Raw image; (b) power spectrum of image
rmin = 1 to rmax = 127 pixels, 0 is the angle of orientation on the against angle on image
image (Omi,= 0~ Omax= 360~ and Nr is the number of data
points available for each frequency r. Fig. la shows the X-ray
image of a trabecular bone specimen, and Fig. lb shows its 2.3 Computation of Minkowski dimension using mathematical
power spectrum, PS(r, 0). morphology
The average power spectrum over all orientations was A" two-dimensional image can be regarded as a gray-level
calculated from surface, represented by a matrix f . The global Minkowski
dimension DM[f] was computed from the equation
G~x PS(r, O) (MARAGOS, 1994)
PS(r) = (1)
0=0mi. Nr
,. Iog[Vg(E)/E 3]
DM[f] -----nm - - (3)
A least-square fitted straight line between log(PS(r)) and log(r) E~o log(1/Q '
was computed, and the global fractal dimension D was calcu-
lated from the slope/3 using D = (8 - fl)/2. where Vg(e) is the volume between the upper and lower envelope
The directional fractal dimension D(O) was computed from for a given structuring element g at scale e. The volume V~(E)was
the power spectrum PS(r, O) for each 0 as computed from

log(PS(r, 0)) = fl(O)log(r) + C (2) M N

where fl(O) is the slope at angle 0; r is frequency in number of
pixels; C is a constant; and fractal dimension
O(O) = [8 - fl(O)]/2. The D(O) was computed for each 0 in 1~
increments. As the number of available pixels was unequal to the
number of angles of interest (360), especially at the lowest
frequencies (near the centre of Fig. lb) for which there were far
fewer than 360 pixels in the radial direction, a bi-linear inter-
polation method was used to find values of the power spectrum
that were not exactly on the grid (JIANG, 1997).
* Model 43855A, Hewlett Packard
t Kodak
150 Illuminator, D.O. Industries
** Research Systems, Inc.
414
V0(e) = Y~. Y~ {07 @ Eg) -- 07 @ e#)} (4)
m=0n=0
where 07 @ eg) and (.f Qeg) are the dilated and the eroded
conversions of the image f with a structuring element g at the
scale E, respectively. Plotting the numerator against the denomi-
nator in eqn. 3 and finding the slope using least-square fitting
gave DM[f ].
Eqn. 3 was derived by MARAGOS (1994) with the assumption
that the structuring element was a three-dimensional ball. In
digital image processing, both the image and the structuring
element are discrete. Therefore, to apply eqn. 3, the structuring
element must be symmetric and convex (MARAGOS, 1994) and
should be as small as possible to reveal the fine details of the
surface. In digital space, the smallest convex structuring
elements are those within a box of 3 x 3 x 3 voxels that are
Medical & Biological Engineering & Computing 1999, Vol. 37
symmetric around their origins or the central voxels. The
structuring elements that met these requirements and were
used in this study are shown in Fig. 2.
To compute the directional Minkowski dimension, the image
was rotated from 0 = 0 ~ to 180 ~ with a 10~ increment. For each
rotation 0, the cover volume was calculated from
M N
v~(o, E = E ~ {]o 9 Eg) - (.?o e ~g)}
m = 0 n=0
where J~0 is the original image rotated by 0, and g was selected
from the vertical structuring elements constructed for this study,
as shown in Fig. 2. The directional Minkowski dimension as a
function of 0, DM(O), was then computed from eqn. 3 by using
the calculated volume from eqn. 5 for each rotation. For each
image, 18 dimensional data (from 0 ~ to 180 ~ with a 10~
increment) were computed, and a total of 36 dimensional data
(from 0 ~ to 360 ~ with a 10~ increment) were generated based on
symmetry, and the 36 dimensional data were used for ellipse
fitting.
For comparison, the mean intercept length method
(WHITEHOUSE, 1974) was modified and used to characterise
the textural anisotropy of the x-ray images. The grey-level
images were rotated from 0 ~ to 180 ~ in 10~ increments. For
each rotation, the image was globally thresholded based on the
mean and standard deviation of the image grey levels, to produce
a binary, black-and-white image. The mean intercept length was
then computed from the binary image for each orientation.
Following WH[TEHOUSE (1974), in which the directional
measures of mean intercept length were fitted to an ellipse, the
directional fractal dimensions using power spectrum and direc-
tional Minkowski dimensions were also fitted to an ellipse to
describe the textural anisotropy of the x-ray images. Fig. 3 shows
the parameters of the ellipse that were used to characterise image
texture: the major and minor diameters a and b, eccentricity e,
and orientation 0 o.
3 Results and discussion
3.1 Estimates o f fractal dimensions from synthetic images
The power spectrum and Minkowski dimension methods
were compared using synthetic images with fractal dimensions
of 2.5, 2.7 and 3.0, respectively. These fractal dimensions were
chosen to correspond to the range observed for the majority of
the bone x-ray images. For each fractal dimension, six images
were generated. The correlation coefficient between actual and
estimated fractal dimensions was 0.986 for the power spectrum
method, and 0.979, 0.989, 0.996 and 0.990 for the Minkowski
3D structuring elements
27-voxel cube 11-voxel pyramid 7-voxel rhombus 9-voxel flat
e ;,
vertical structuring elements
9-voxel flat 5-voxel rhombus 3-voxel bar
b
Fig. 2 Structuring elements used for computing (a) global and (b)
directional Minkowski dimensions
Medical & Biological Engineering & Computing 1999, Vol. 37
measuring
direction
(5)
0
x/,
Fig. 3 Parameters of fabric ellipse for characterising bone textural
anisotrophy, x i and xj are horizontal and vertical axes on
image; a and b are major and minor diameters; 0o is angle
between major axis of ellipse and x i axis on image; 0 is an
angle of interest. (Eccentricity: e = sqrt(a 2 - bZ)/a)
dimension method, with 27-, 11-, 9- and 7-voxel structuring
elements, respectively. The highest correlation was obtained
with the Minkowski dimension and a 9-voxel structuring
element.
The consistency of the fractal dimension estimates was
evaluated from the six fractal dimensions estimated for each
image set. The standard deviations using the Minkowski dimen-
sion with 9-voxel structuring element were 0.010-0.016 across
the fractal dimensions, whereas those using the power spectrum
method ranged from 0.024 to 0.035 for the three image sets. The
lower standard deviations for the Minkowski dimension method
indicated greater consistency than with the power spectrum
method.
These results suggest that the Minkowski dimension with a 9-
voxel structuring element provided a more accurate and consis-
tent estimate of the global fractal dimension than the power
spectrum method. Similar findings were obtained for bone by
SAMARABANDUet al. (1993) and ACHARYAet al. (1995). Note
that the two methods produced slightly different values in
estimated fractal dimensions. However, the absolute values are
of little importance because only relative fractal measurements
or textural roughness were used for characterising trabecular
bone structure.
3.2 Fractal properties o f bone x-ray images
An x-ray image of a typical trabecular bone specimen is
shown in Fig. 1a. Owing to x-ray attenuation through the 8 mm
thick specimen, light and dark areas indicate the amount of
overlapping trabecular structure through the entire thickness of
the specimen, rather than individual trabecular elements or
marrow spaces as seen in a thin section. This image also
shows a moderately oriented texture, so that both trabecular
orientation and the amount of material aligned with that orienta-
tion are visible.
Figs. 4a and b show representative log-log plots for
computing global and directional fractal dimensions, respec-
tively, using the power spectrum method. Fig. 4c shows the log-
log plot for computing the global Minkowski dimension of the
same image. For both methods, only part of the curve was linear
(solid dots). The maximum R 2 of the least-square fitting was
used to estimate the linear range. For the power spectrum
method, the linear portion was found to be in the frequency
range between approximately 11 and 60 pixels. For the
Minkowski dimension method, on the other hand, the linear
portion was between the scale of 6 and 55 pixels.
Table 1 lists the coefficients of determination R 2 for log-log
fitting to compute the global and directional fractal dimensions.
Using the Minkowski dimension, the R 2 were greater than 0.996
415
Table 1 Coefficients of determination R 2 for log-linear fit for Table 2 Coefficients of determination R 2 between estimated angle of
estimating global and directional fractal dimensions of 70 trabecular orientation and known angle of rotation for four trabecular bone
bone images using power spectrum and Minkowski dimension meth- images using mean intercept length (MIL), power spectrum (PS) and
ods Minkowsla" dimension (MD) methods, with 9-voxel (MD-9), 5-vox-
el(MD-5) and 3-voxel (MD-3) structuring elements
Power spectrum Minkowski dimension
Known MIL PS MD-9 MD-5 MD-3
global directional global directional eccentricity
Mean 0.992 0.833 > 0.9999 0.9998 0.25 0.976 0 0.998 0.999 0.999
Standard deviation 0.004 0.062 < 0.0001 0.0002 0.38 0.990 0.667 0.998 0.999 0.999
Minimum 0.978 0.265 0.9998 0.9967 0.65 0.998 0.932 0.999 0.999 0.999
Maximum 0.997 0.964 > 0.9999 > 0.9999 0.80 0.999 0.986 0.999 0.999 0.999

for both global and directional fractal dimensions. Similar values
were obtained using the power spectrum method for computing
the global fractal dimension. This indicates that the x-ray images
were statistically self-similar, i.e. fractal, over a certain range of
scales. The upper limit on the range could be set by the largest
overlaying structure oftrabecular bone, whereas the lower limit
was not strongly oriented (e = 0.25 or 0.38). This is expected,
because the thresholding used for determining mean intercept
length resulted in a loss of some o f the image's texture.
-- In

could be dictated by image resolution, digitisation noise and film

grain size. E~
A relatively poor fit was obtained using the power spectrum 2

method compared with the Minkowski dimension for the

estimation of directional fractal dimension (Table 1). The
relatively noisy power spectrum visible in Fig. 1b could be a
major cause. Note that, in the computation of the global fractal
dimension, the noise was smoothed or suppressed by the circular
0 84
averaging from 0 = 0 ~ to 360 ~ as implied by eqn. 1. Therefore a
better fit was achieved for the determination of the global fractal
dimension using the power spectrum method. I
1 2
log (frequency)

3--

3.3 Characterisation o f image textural anisotropy 0 0 CIEIO

2-
To represent the textural anisotropy of x-ray images using a ~,
fabric ellipse, it is necessary to show that the directional
measurements were in fact elliptical. For the 70 trabecular _o
bone specimens, the R 2 for an ellipse fitted to the directional
data had means of 0.979, 0.767 and 0.954 (standard deviation o-
0.044, 0.052 and 0.088) for the mean intercept length, power
spectrum and Minkowski dimension (with 3-voxel structuring
element) methods, respectively. Thus, both the mean intercept -1 - !
length and Minkowski dimension produced a good fit, whereas
the power spectrum was relatively poor. Fig. 5 shows the ellipses log (frequency)
for a typical image using the three methods. Note that the major
axis of the ellipse for mean intercept length was oriented with the 6-
visible direction of the trabeculae, whereas the major orientation
for both fractal-based methods, which indicates direction of ~ 5-
greatest roughness, was perpendicular to the trabecular orienta- <|
tion. ~ 4--
To evaluate the performance o f the three methods in detecting >o
image directionality, four trabecular bone x-ray images were ~ 3-
selected that varied in their degree of anisotropy, measured in o
terms of eccentricity e. Among the 70 specimens, about 90% of 2-
the x-ray images had eccentricities between 0.30 and 0.75. The
selected images had e = 0.25, 0.38, 0.65 and 0.80, to cover a 1- I I
range from weakly to strongly oriented. Each of the four images -2 -1 0
was digitally rotated by 5, 10, 15, 16, 17, 18, 19, 30, 45, 60 and log (1/scalel
75 degrees, and fabric ellipses were computed with each method
for the original image and each rotation. Fig. 4 Representative log-log plots for determining fractal dimen-
sion from the power spectrum and Minkowski dimension
The R 2 between the computed and actual degrees of rotation methods. (a) Global fractal dimension using power spectrum;
of the images are given in Table 2 for the different eccentricities. slope = - 2. 72; D = 2. 64; R 2 = 0.995; (b) directional fractal
The power spectrum method was less accurate than the mean dimension using power spectrum," slope = - 2. 76; D = 2.62;
intercept length and Minkowski dimension methods, regardless R 2 = 0.891; (c) global fractal dimension using Minkowski
of structuring element. The Minkowski dimension performed dimension (9-voxel structuring element); DM =log
slightly better than mean intercept length when the image texture (vol/scalea) /log(1/scale) = 2.73; R 2 = 0.999

416 Medical & Biological E n g i n e e r i n g & C o m p u t i n g 1999, Yol. 37

 a b

@
.r9 v,,?, ~ , .

~" "' " '4.

c d

Fig. 5 (a) Trabecular bone x-ray image and corresponding fabric ellipses using (b) mean intercept length, (c) power spectrum, and (d)
Minkowski dimension methods

150 -
0 +

§
.4,.
"6 100 -
i + +4 a

tj '
"0
50-
I:z
E
0
o
+
O-
I I l I I I I I I I I ( I I I
a b

80-

~ 40- + 4- 4-

2o-

o
0-
I I i i I I I i I I t | I i I I
0 20 40 60 80 0 20 40 60 80
degree of rotation degree of rotation
C d

Fig. 6 Graphical comparison of estimated against actual orientation of test images using mean intercept length (MIL), power spectrum (]aS) and
Minkowski dimension (AID) methods. Results shown are for images with (a) very weakly oriented texture with eccentricity e = 0.25; (b)
less weakly oriented texture with eccentricity e = 0.38 strongly oriented texture with eccentricity e = 0.65 (c); and (d) very strongly
oriented texture with eccentn'city e=0.80, ([:]) MIL; ( + ) PS," ( x ) MD 3-voxel

Medical & Biological Engineering & Computing 1999, Vol. 37 417

 Fig. 6 shows the computed angle of orientation against actual
degree of rotation for each method and eccentricity. There was
considerable error with the power spectrum method, even for the
strongly oriented image, e = 0.65. The relatively noisy power
spectrum data (Fig. 4b) could explain most of the error. Also, for
the power spectrum data, an ellipse was less than adequate in
describing the directional fractal dimension data (Fig. 5c). Star-
and rhombus-shaped power spectra were observed in some
images in this study, and were similar to those presented by
OXNARD (1993) and BENHAMOU et al. (1994) for bone.
In this study, fractal dimensions were computed directly from
grey-level x-ray images obtained from 8 mm thick specimens.
Thus, the image being analysed was a two-dimensional projec-
tion of the three-dimensional trabecular structure. Compared
with the mean intercept length method performed on binary
images of thin slices o f bone, the methods presented here could
better assess three dimensional trabecular bone structure from
images of in situ specimens. More work is needed to determine
whether the information in these images correlates with the
mechanical properties of bone, and whether images can be
collected from specimens of whole bone of normal thickness.
4 Conclusions
In this study, two aspects of trabecular bone structure were
studied using the fractal dimension: the overall roughness of an
x-my image using the global fractal dimension, and textural
anisotropy using the fabric ellipse computed from directional
fractal dimensions. It was found that the x-ray images of
trabecular bone cubic specimens were fractal both globally
and directionally in a limited range of scales. Among the two
methods for calculating global fractal dimension and three
methods for extracting the fabric ellipse, the Minkowski dimen-
sion method provided the most accurate and consistent estima-
tion o f global fractal dimension and textural anisotropy. Among
the four structuring elements for estimating the global
Minkowski dimension, the 9-voxel fiat structuring element
performed better than the other methods. The three structuring
elements for estimating directional Minkowski dimension
performed equally well.
Acknowledgment--This research was supported by a USDA
National Needs Fellowship.
Special thanks go to Susan G. Capps for her support and helpful
discussions and to James A. Throop for his assistance with the system
setup.
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Author's biography
CHUNSHENGJIANGreceived an MS degree and a
PhD degree in Bio-engineering from Comell
University, Ithaca, New York, in 1994 and 1997,
respectively. His research interests include medi-
cal imaging, digital image processing and analy-
sis, biomechanics, biomedical instrumentation,
and bone quality evaluation. He worked as a
Postdoctoral Fellow in the Kurt Rossmann
Laboratories for Radiologic Image Research at
The University of Chicago on computerised radiographic analysis of
bone quality using fractal analysis, geometric modelling and bio-
mechanical analysis. He currently works at the Analogic Corporation,
USA.
Medical & Biological Engineering & Computing 1999, Vol. 37