ARTICLE IN PRESS

Biomaterials 28 (2007) 29082914

www.elsevier.com/locate/biomaterials

2D mapping of texture and lattice parameters of dental enamel

Maisoon Al-Jawada,, Axel Steuwerb, Susan H. Kilcoynec, Roger C. Shorea,
Robert Cywinskid, David J. Wooda
a
Leeds Dental Institute, University of Leeds, Leeds, LS2 9LU, UK
FaME38 at the ILL-ESRF, 6 rue J Horowitz, 38042 Grenoble, France
c
Institute for Materials Research, University of Salford, Salford, M5 4WT, UK
d
School of Physics and Astronomy, University of Leeds, Leeds, LS2 9JT, UK
b

Received 19 December 2006; accepted 16 February 2007

Available online 25 February 2007

Abstract
We have used synchrotron X-ray diffraction to study the texture and the change in lattice parameter as a function of position in a cross
section of human dental enamel. Our study is the rst to map changes in preferred orientation and lattice parameter as a function of
position within enamel across a whole tooth section with such high resolution. Synchrotron X-ray diffraction with a micro-focused beam
spot was used to collect two-dimensional (2D) diffraction images at 150 mm spatial resolution over the entire tooth crown. Contour maps
of the texture and lattice parameter distribution of the hydroxyapatite phase were produced from Rietveld renement of diffraction
patterns generated by azimuthally sectioning and integrating the 2D images. The 002 Debye ring showed the largest variation in
intensity. This variation is indicative of preferred orientation. Areas of high crystallite alignment on the tooth cusps match the expected
biting surfaces. Additionally we found a large variation in lattice parameter when travelling from the enamel surface to the enameldentine junction. We believe this to be due to a change in the chemical composition within the tooth. The results provide a new insight on
the texture and lattice parameter proles within enamel.
r 2007 Elsevier Ltd. All rights reserved.
Keywords: Enamel; Hydroxyapatite; Apatite structure; Synchrotron X-ray diffraction; Texture; Preferred orientation

1. Introduction
Dental enamel is the most highly mineralised and
hardest biological tissue. It is comprised of approximately
96% mineral, 3% water, and 1% organic matter (noncollagenous protein) by weight [1]. The mineral is nonstoichiometric calcium hydroxyapatite (Ca10(PO4)6OH2)
with carbonate, uoride, sodium, and magnesium ions
frequently found within the structure. These hydroxyapatite (HA) crystallites are laid down as nanorods with crosssectional dimensions of 50 nm  25 nm and up to 1 mm
long [2]. Clusters of these nanorods, known as prisms,
contain around 1000 crystallites. They are approximately
5 mm in diameter and may be up to several millimetres long,
and the majority are arranged with their long axes at
approximately 901 to the enamel-dentine junction (EDJ).
Corresponding author. Tel.: +441133438331.

E-mail address: m.al-jawad@leeds.ac.uk (M. Al-Jawad).

0142-9612/$ - see front matter r 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biomaterials.2007.02.019

The orientation of prisms in enamel has been studied in

the past using electron microscopy. Although this is a
valuable tool for nding the prism shape and size in a
particular plane of enamel, it is a qualitative technique and
does not give detailed, quantitative information on the
degree of alignment in different parts of a tooth. Previous
work using X-ray diffraction on human dental enamel has
established the space group and lattice parameters as P63/m
(hexagonal) and a 9.441(2) A and c 6.878(1) A respectively [35]. However, these values were obtained from
measurements of powdered enamel collected from several
teeth, and as a result any information on the spatial
variation of the lattice parameters and texture relating to
the growth of the HA crystallites was lost. It has been
reported from grazing-incidence synchrotron X-ray diffraction experiments that there is a higher degree of
crystallite alignment in surface enamel compared to enamel
close to the EDJ [6]. However, only linear slices from EDJ
to surface were probed in these experiments. In an earlier

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M. Al-Jawad et al. / Biomaterials 28 (2007) 29082914

study Hirota examined the tilting of the enamel-prism

orientation in a human canine using laboratory twodimensional (2D) X-ray diffraction [7], however only 12
points within the tooth were measured and therefore the
information obtained about the prism orientation cannot
be for the whole tooth. In this paper we aim to show for the
rst time how synchrotron X-ray diffraction can be used to
determine the basic crystallographic parameters of the HA
phase across a whole intact tooth section, allowing us to
explore composition and texture on the sub-millimetre
length-scale. Characterising the orientation distribution of
the anisotropic apatite crystallites of dental enamel aids the
fundamental understanding of the natural growth and
formation of dental enamel, and provides insights into how
synthetic enamel-like materials may be developed.
2. Materials and methods
2.1. Specimen preparation
The sample used in this study was a section of an adult mandibular
second premolar (LR5). The tooth was collected with informed consent
from a patient undergoing routine orthodontic extraction at the Leeds
Dental Institute. The extracted tooth had its pulp removed and was
sterilised by autoclaving prior to storage at 4 1C in a thymol solution to
prevent bacterial growth. A precision diamond blade cutter was used to
cut the tooth into 500 mm thick longitudinal sections perpendicular to the
buccal and lingual surfaces. The sections were then polished by hand to
remove any surface roughness. A photograph of the section used for this
study is given in Fig. 1. The four arrows mark the tracks plotted in Fig. 10.

2.2. Synchrotron X-ray diffraction

The measurements were taken on the XMaS beamline [8] at the
European Synchrotron Radiation Facility (ESRF) using an X-ray
wavelength of l 0.82 A (equivalent to X-ray energies of 15 keV) and a
sample to detector distance of 163.09 mm. The 2y angle-range for our
experiment was limited by our experimental setup and the sample to
detector distance. We compromised on the very high-angle HA reections
in order to position the 2D detector closer to the sample and therefore
greatly reduced our counting times. This allowed us to collect more
diffraction patterns per tooth and obtain higher resolution texture and

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lattice parameters distribution maps. The 2y angle-range for this

experiment was 2y 5301for comparison this corresponds to a 2yrange of 9581 on a conventional lab-based X-ray diffraction apparatus
with CuKa radiation of wavelength l 1.54 A. For our experimental
setup, the main diffraction peak of the HA phase (2 1 1) was located in the
centre of our 2y range at 16.771. Vacuum tube slits were used to focus the
X-ray beam to a diameter of 150 mm on the sample. A 500 mm thick tooth
section was mounted in transmission geometry onto a travelling sample
platform such that the tooth could be scanned in two orthogonal
directions perpendicular to the beam. A charge-coupled device (CCD) 2D
detector with 2048  2048 pixel resolution was mounted behind the sample
and perpendicular to the incident beam for the collection of 2D diffraction
images. The cross-hairs of a telescope were positioned in line with the
beam centre in order to align the beam position on the tooth. A schematic
of the experimental setup with an example 2D diffraction image is shown
in Fig. 2. A single diffraction image had an exposure time of 5 s and
therefore a 150 mm-resolution map of the tooth on a grid of 10 mm  7 mm
could be collected in approximately 8 h by moving the sample relative to
the beam in an x and y direction.

2.3. Data analysis

2D diffraction images were pre-processed with the ESRF software
Fit2D [9]. Each image was sectioned into 51 slices [10] and these integrated
slices were then used to create Intensity versus 2y patterns for Rietveld
renement [11], i.e. 72 diffraction patterns per 2D image. Conventionally
only one Bragg reection in the diffraction pattern is used in texture
analysis therefore any slight changes in sample volume as a function
of position would affect the sample absorption and could affect the texture
coefcient obtained. However, using the Rietveld method minimises the
effect of variations in sample volume since all reections are used to
obtain the t. In addition, in our study, we used a scaling factor in the
renement procedure and found that changes in the scale factor were small
as a function of position within the tooth, indicating that variations in
section thickness were negligible. A total of 1095 diffraction patterns were
rened and therefore an in-house automated batching procedure was
written and used to input the patterns into the GSAS Rietveld renement
software [12]. The instrument parameters such as X-ray wavelength,
sample to detector distance, and peak-shape prole were determined using
a LaB6 standard sample. These parameters were then kept xed for
renements of the data. The scale parameter and background parameters
(four terms) were rened rst. The lattice parameters and crystallite
size (Lorentzian particle broadening term) were rened next, starting from
the values for HA taken from Young [3]. Finally the texture was rened
using a spherical harmonics function [13] and the preferred orientation
values for the 002 reection were extracted from this. The values of
preferred orientation ranged from 0 (randomly oriented) to 3.5 (strongly
textured). The quality of the renement was determined by least squares
methods where the goodness of t increased as w2 approached unity
whereby:
w2

R2wp
R2e

where Rwp is the weighted R-factor and Re the expected R-factor.

Fig. 1. Photograph of 500 mm thick tooth section from a human adult

lower right premolar. The arrows mark the tracks through the tooth
plotted in Fig. 10.

Fig. 2. Experimental setup at the XMaS beamline, ESRF, with an

example 2D diffraction image.

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3. Results
3.1. Preferred orientation in enamel
Preferred orientation has both a magnitude and a
direction. Through our analyses of the X-ray diffraction
data we have been able to quantify both these parameters.
In order to obtain an overview of the preferred orientation
in a tooth section the 2D X-ray scans were arranged to
form a composite map of CCD images of the tooth, as
shown in Fig. 3. Each small square in the image is one 2D
diffraction pattern. The centres of adjacent diffraction
patterns are 150 mm apart. The shape of the tooth can
clearly be seen from this composite image. The darker
patterns in the middle of the tooth are from dentine and the
lighter patterns covering these are from the enamel. At the
surface the enamel is thinner, therefore there is a halo of
darker images along the edge of the tooth where there is
partial air scattering. This can also be seen in the ssure
where there is a gap between the two cusps. Additionally, it
can be seen that below the ssure there is a circular region
of enamel which is darker than the surrounding patterns. It
is likely that this is caused by a ssure caries lesion which
has partially demineralised the enamel in that area.
In Figs. 4ad four individual diffraction scans from
different parts of the tooth are shown. Figs. 4a, c and d
illustrate the change in texture direction in the 002 plane at
different positions within the enamel. Variations in
intensity around diffraction rings are indicative of texture
in the tooth enamel. The strongest texture (the most
extreme variation in intensity) was found in the 002
reection (2y 13.71)labelled in Fig. 4a. A line through
zero degree has also been marked in Fig. 4a. Fig. 4b shows
the diffraction pattern from dentine. Here the peaks are
much broader indicating that the crystallites are smaller.
There is also much less variation in intensity around the

Fig. 4. (a), (c) and (d) Illustrate the change in texture direction at
difference positions within the enamel. (b) Shows the poorly crystalline
nature of dentine.

Debye rings indicating that the dentine is much less

textured than the enamel.
The intensity pattern around the Debye ring of the 002
reection was used to evaluate the texture direction. The
intensity was integrated over 3601 in a narrow band
containing the 002 reection and plotted versus the
azimuthal angle. Fig. 5 shows a typical example of the
resulting curve for one diffraction scan where there are two
pronounced peaks separated by approximately 1801. By
tting these peaks to a Gaussian peak shape, the deviation
angle, f, of the crystallite axis relative to vertical was
determined. By applying this procedure to each of the
diffraction images, a map of the local orientation of the
texture in the 002 direction in the enamel is obtained.
Fig. 6 shows a map of the orientation angles overlaid
onto the composite image of the tooth. In Fig. 6, for
clarity, only every fourth value of f has been drawn. It can
be seen from this that the texture direction in the 002
reection is approximately perpendicular to, and follows
the contour of the EDJ. From our knowledge of the
structure of dental enamel it would appear that the
preferred orientation in the 002 direction approximately
follows the direction of the enamel prism arrangement.
3.2. Rietveld refinement

Fig. 3. Composite of 2714 diffraction images arranged spatially to show

the outline of the tooth specimen.

The extent of preferred orientation in the tooth section

has been quantied using Rietveld renement. An example
of a typical 1D Intensity versus 2y diffraction pattern
together with the calculated pattern is shown in Fig. 7. The

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Fig. 5. Typical intensity versus Azimuthal angle curve for the 002
reection showing the pronounced texture in this sample. The left hand
peak has been tted to a Gaussian.

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open circles are the observed data points, and the solid line
is the calculated diffraction pattern. Below the pattern is a
plot of the difference (observedcalculated), and beneath
are the tick marks for the 2y peak positions for the
calculated diffraction pattern of HA. The difference plot
shows that the agreement between observed and calculated
data is generally very good with a typical value for w2 of
1.5. The nal parameters obtained from this renement
are given in Table 1. Similar renements were carried out
on all diffraction patterns.
A contour map showing the change in magnitude of
preferred orientation in the 002 diffraction peak has been
plotted in Fig. 8. The 002 preferred orientation parameters
have been extracted for the zero degree slice of each 2D
diffraction image (see Fig. 4a). Areas with higher values of
preferred orientation parameter are more strongly textured
i.e. the crystallites are more aligned to the zero degree
direction in these areas. Areas with low texture coefcient
have less well-aligned crystallites.
3.3. Change in lattice parameters
Both the a- and c-lattice parameters of HA were rened
in each diffraction pattern and after carrying out Rietveld
renements of 1095 data sets it was noticed that neither the
a- nor c-lattice parameters were constant as a function of
position. Note that the variation was not due to X-ray
wavelength drift as a function of time, but was clearly
dependent on the position within the tooth. Trends in the
lattice-parameter changes have been plotted in Fig. 9
relative to the average lattice parameters. The relative
percentage change in the a-lattice parameter (Ra) across the
tooth section was calculated using:


an  a0
Ra
 100%,
a0

Fig. 6. Texture direction of the 002 reection of hydroxyapatite crystallites in enamel, calculated using 2D diffraction images.

where an is the rened lattice parameter for diffraction

pattern n, and a0 is the overall average lattice parameter.
The same type of equation was used for dening the
c-lattice parameter variation, Rc. Both Ra and Rc have been

Fig. 7. Typical diffraction pattern including the raw data (circles), the calculated diffraction pattern (solid line), the difference, and the tick marks for the
2y peak positions for the calculated diffraction pattern of hydroxyapatite.

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Table 1
Rened structural parameters for typical diffraction pattern of dental enamel (HA)
Phase hydroxyapatite
Space group
a (A)
c (A)
a, b, g
V (A3)
Y(particle)
002(SH)
w2

P63/m (#176)
9.4660(9)
6.9018(3)
a b 901, g 1201
535.49(8)
7.83(9)
1.9(1)
1.5

Y(particle) is the coefcient for Lorentzian particle size broadening, and 002(SH) is the 002 spherical harmonic preferred orientation term.

Fig. 8. Texture distribution map generated from the calculated texture

coefcient via Rietveld renement.

plotted as contour plots in Figs. 9a and b. It can be seen

from these gures that the a- and c-lattice parameters vary
between 0.6% and +0.3% of their average values. In all
cases the uncertainty in the lattice parameters did not
exceed 1  103, and the values for the average lattice
parameters were a0 9.5165(6) A and c0 6.9394(2) A.
These plots clearly reveal that there is a systematic
variation of the lattice parameters as a function of position
within the enamel.
Figs. 10ad shows plots of Ra and Rc as a function of
distance from the surface for the four tracks through the
enamel indicated in Fig. 1. In all regions, Ra (lled
symbols) decreases with increasing distance from the tooth
surface, especially around the cusps. In Figs. 10b and c
there is second peak in the Ra curve at around 600 mm from
the surface indicating a region of enamel which has a
higher a-lattice parameter than the surrounding enamel.
This region can be seen clearly in the contour plot in Fig.
9a. Along each track, the c-lattice parameter curves (open
symbols) are much atter. This indicates that Rc is less
dependent on the distance from the enamel surface than
Ra. In both the a- and c-lattice parameter values, there is
also a difference between the lingual and the buccal sides of
the tooth.

Fig. 9. (a) a-lattice parameter and (b) c-lattice parameter contour maps
showing the change in lattice parameter value at different positions
around the tooth.

4. Discussion
It has been seen previously that there is a higher degree
of crystallite alignment in surface enamel compared to
enamel close to the EDJ [6]. However, in that work, only
linear slices from EDJ to surface were probed. The results
from our study show that the texture distribution is
much more complex than previously thought. We can see

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Fig. 10. Four tracks through the tooth section going from enamel surface
to EDJ showing the change in lattice parameter as a function of distance
from the enamel surface. The tracks are indicated in Fig. 1.

in Fig. 8 that HA crystallites are most aligned in the cuspal

regions: on both sides of the buccal cusp and on the inner
side of the lingual cusp HA crystallites are highly aligned.
Conversely, along the sides of the tooth away from the
cusps generally the crystallites are less ordered. It is
interesting to note that the areas of high crystallite
alignment match the expected occlusal surfaces of a lower
second premolar [14]. This may be an evolutionary
development of enamel so that the regions of enamel
which are exposed to the largest load are the strongest. It is
interesting to note that a strong correlation between
functionality and texture in human bone has been reported
by Bacon [15] where he observed that the living conditions
(either on a steep hillside, or on the at) of two Neolithic
tribes radically affected the HA crystallite growth and
alignment on the lower front edge of the tibia. Although
dental enamel cannot regenerate itself as bone can, it is
likely that through evolution the degree of crystallite
alignment in different regions of a tooth has been
optimised for the function of the tooth.
Changes in lattice parameter can be indicative of changes
in enamel crystal chemistry as well as changes in the stress/
strain-state of a material. Separating these two possible
effects or even using the lattice parameters to determine
compositional changes in biological apatites is not
straightforward as changes in crystal chemistry can be
the result of several ionic substitutions, such as Na, Mg, Cl
or F, as well as variations in the carbonate content and the
Ca/P ratio. However, the magnitude of the changes seen
across our tooth suggest that the changes in lattice
parameters plotted in Figs. 9 and 10 arise predominantly
from changes in the chemical composition of the enamel in
different regions of the tooth. Chemical analysis of the
distribution of uoride, carbonate and magnesium in
enamel has been carried out previously by Robinson et
al. By dissecting tooth sections into pieces weighing

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2050 mg, the amount of uoridated apatite was determined

by etching the tooth sections and analysing the uoride
concentration in the post-etched buffer solution [16], the
concentration of carbonate was determined by dissolving
each piece in acid and measuring the volume of CO2
emitted [17], and concentration of magnesium was found
using an atomic absorption spectrophotometer [18]. They
found that uoride concentrations decreased in going from
the enamel surface to the EDJ, while carbonate and
magnesium concentrations increased (from 2% to 46%,
and from 0.2% to 0.5% respectively) across the same
distance [19]. In dentine, changes in the a-lattice parameter
of up to 0.5% have been reported in going from the EDJ
into the centre of the dentine [20]. This trend has been
explained principally as a result of the increased substitu3
tion of CO2
3 for PO4 associated with the more immature
dentine crystallites. Our results are of a comparable order
of magnitude and we believe them to be the result of
compositional change. Comparing Figs. 9a and b it can be
seen that there is more variation in the a-lattice parameter
than in c. This trend has also been seen in dentine [20]
where the a-lattice parameter decreased by 0.5% with
increasing distance from the EDJ into the dentine, whereas
the c-lattice parameter only decreased by 0.1% over the
same distance. In addition to a decrease in lattice
parameters going from the surface enamel to the EDJ,
there is a difference in the lattice parameters on the buccal
and lingual sides of the tooth indicating a change in crystal
chemistry on the different sides of the tooth. This could
either be due to the different functions of the two sides of
the tooth or due to their slightly different oral environments, or a combination of both.
Cuy et al. have generated 2D distribution maps for the
hardness (H) and Youngs modulus (E) of enamel using
nanoindendation [21]. In the molars they investigated, they
found that the cuspal regions had higher hardness and
Youngs modulus. They report values ranging from
H46 GPa to Ho3 GPa and E4115 GPa and Eo70 Gpa,
respectively, going from the enamel surface to the EDJ.
The contour maps they generated of H and E show similar
features to our lattice-parameter distribution maps, indicating that the crystallographic and mechanical properties of enamel are closely linked, therefore an
understanding of both is necessary in order to fully
understand the function of enamel in different parts of a
tooth.
5. Conclusions
Using spatially resolved synchrotron X-ray diffraction
we have quantied the changes in texture and lattice
parameters in dental enamel as a function of position
within the tooth. With this technique, in a few hours of
data collection, we have generated 2D distribution maps of
both texture and lattice-parameter changes in enamel with
150 mm resolution. This has given detailed quantitative
information on the degree of crystallite alignment in

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different regions of tooth enamel not previously reported.

It has also shown that the lattice parameters maps, related
to changes in crystal chemistry, are more complicated that
previously thought indicating that understanding heterogeneities within a single tooth is as important as realising
the differences between teeth. We have shown that
characterising the crystallographic properties of dental
enamel is crucial in order to design optimised dental
restorative materials. Finally, we have shown through this
work that synchrotron X-ray diffraction is a powerful
technique in the study of the crystallography and microstructure of dental enamel and it could be equally
successful in the study of other biological hard tissues, in
the study of synthetic biomaterials, and in the study of biosynthetic complexes.
Acknowledgments
This work was performed on the EPSRC-funded CRG
beamline (XMaS BM28) at the ESRF. We are grateful to
L. Bouchenoire and J. Wright (ESRF) for their invaluable
assistance and to S. Beaufoy for additional administrative
support. Also, we would like to thank the FaME38 facility
for providing the VAMAS approved precise sample
mounting system. Thanks to C. Sullivan at Leeds Dental
Institute for producing the photograph in Fig. 1. This
research was funded by the UK Medical Research Council.
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