Comparison of conventional and synchrotron radiation

based microtomography of bone around dental implants

Paolo M. Cattaneo*a, Michel Dalstraa, Felix Beckmannb, Tilman Donathb, Birte Melsena
a
Dept. of Orthodontics, School of Dentistry, Aarhus University,
Vennelyst Boulevard 9, 8000 Aarhus C, Denmark;
b
GKSS Forschungszentrum, Geesthacht GmbH, c/o HASYLAB at DESY,
Notkestr. 85, 22607, Hamburg, Germany

ABSTRACT

This study explores the application of conventional micro tomography (µCT) and synchrotron radiation (SR) based
µCT to evaluate the bone around titanium dental implants. The SR experiment was performed at beamline W2 of
HASYLAB at DESY using a monochromatic X-ray beam of 50 keV. The testing material consisted of undecalcified
bone segments harvested from the upper jaw of a macaca fascicularis monkey each containing a titanium dental implant.
The results from the two different techniques were qualitatively compared with conventional histological sections
examined under light microscopy. The SR-based µCT produced images that, especially at the bone-implant interface, are
less noisy and sharper than the ones obtained with conventional µCT. For the proper evaluation of the implant-bone
interface, only the SR-based µCT technique is able to display the areas of bony contact and visualize the true 3D
structure of bone around dental implants correctly. This investigation shows that both conventional and SR-based µCT
scanning techniques are non-destructive methods, which provide detailed images of bone. However with SR-based µCT
it is possible to obtain an improved image quality of the bone surrounding dental implants, which display a level of detail
comparable to histological sections. Therefore, SR-based µCT scanning could represent a valid, unbiased three-
dimensional alternative to evaluate osseointegration of dental implants.

Keywords: bone structure, dental implant, microtomography, osseointegration, synchrotron radiation

1. INTRODUCTION

Over the past 30 years, endosseus dental implantation has been established as a valid method to restore oral function
in case of totally or partially edentulous patients. For a long time it was erroneously accepted that the encapsulation by
connective tissue was the only possible type of attachment of living bone tissue to implants made of polymer or metals.
In the field of dentistry this peri-implant layer was mistakenly considered to replace the periodontal ligament in the
natural dentition. Nowadays it as been recognized that this type of attachment is not strong enough 1. It was with the
work of Brånemark and the Gothenburg group 2-5 that endosseus implants have become increasingly popular in oral
rehabilitation. When working on the bone reaction in the so-called optical chamber they discovered almost by chance the
high grade of biocompatibility and strong anchorage given by titanium in bone tissue. To describe the strong attachment
of the adjacent bone to the surface of titanium implants the term osseointegration was introduced 6. Several definitions of
osseointegration have been proposed. According to the Dorland’s Medical Dictionary, 1994, osseointegration is a
“direct contact of the bone to the implant without the in-growth of fibrous tissue at bone-implant interface”. Brånemark
proposed “a direct structural and functional connection between ordered and living bone and the surface of a load-
carrying interface”. The definitions of the term osseointegration are, however, far from being universal. The dynamics of
bone as a tissue is thus not taken into consideration. As a consequence of the ongoing remodeling and modeling
osseointegration cannot be considered a static index. It is directly related to the dynamic nature of bone, whereby the

* pcattaneo@odont.au.dk; phone +45 8942 4094; fax +45 8619 27 52; www.odont.au.dk/or/staff/cpaolo/cpaolo.html

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 implant-bone interface can change over time. Additional information that should be implicit in the term osseointegration
is the amount of osseous contact that is necessary for an implant to be considered as osseointegrated. It has been
demonstrated that an implant can be clinically stable even with 25 percent of its surface in contact with bone 7, yet no
minimum values have been defined.
The direct anchorage of implants within the maxilla or mandible bone by means of osseointegration seems to be the
only reliable way to establish a long-lasting and stable anchorage. Osseointegration was indeed achieved by using
titanium implants. For these reason titanium implants became the preferable choice especially for dental implants 8.

Computed tomography is based on the same principle by which a planar X-ray image can be produced, namely
interaction of photons with the matter they pass through.
There are three different phenomena that can happen when a photon is traveling through matter:
1. Photoelectron absorption: this happens when the photon energy is entirely absorbed by an atom and is used to
excite an electron that can be either promoted to a higher energy level or be emitted.
2. Compton scattering: this occurs when the photon energy is not entirely absorbed, but just a part of it is
transferred to an electron. As a result the photon will be deviated in another direction with a different energy level.
3. Pair production: this is a phenomenon that happens when photons have a high energy (>1.02 MeV). The
incoming photon is transformed into an electron-positron pair.
The last phenomenon is not relevant in normal CT-scanner technology, while the first one is important at low
energies (< 20-30 keV) and the second one at relatively higher energy levels (>30 keV).
All substances attenuate a homogeneous X-ray bundle by a factor depending on density (represented by the linear
attenuation coefficient µ) and thickness (d) according to Beer’s law:

I out = I in exp( − µd ) ,

where Iin is the in-going X-ray bundle intensity and Iout the outgoing intensity of the bundle. Beer’s law does only
apply to a monochromatic beam and when the object is homogenous.
Problems arise when objects are heterogeneous and the X-ray bundle, typically produced by an X-ray tube, is
characterized by a continuum spectrum. All substances attenuate low-energetic X-rays more strongly than high-energetic
rays, therefore the outgoing heterogeneous beam will be richer in high-energy photons, and hence be “harder” 9; a
phenomenon called beam hardening.
Considering an X-ray bundle characterized by an intensity distribution σ(E) as a function of energy traveling through
a heterogeneous object with a thickness d = xout – xin, the intensity of the outgoing bundle will be:

∞  xout

I out = ∫ dEσ (E) exp  − ∫ µ ( E , x ) dx  .
0

 x in 

Solving this equation will give the intensity of the outgoing bundle, but it also shows that the result is a projection
that is distorted depending on thickness, density, and the X-ray bundle properties. Generally speaking, if no correction is
made and linearity is assumed, the centre of an object will look less dense than it is in reality as its core is exposed to
more high-energetic X-ray due to this beam hardening effect.

1.1 Synchrotron radiation

Synchrotron radiation (SR) offers outstanding properties if compared to a normal X-ray tube source, because it can
be used to generate a monochromatic beam. SR is emitted by energetic electrons, typically circulating in batches or
bunches, orbiting at a velocity close to the speed of light in a storage ring. The emission is produced when the electrons
are accelerated, for example, by being forced to travel in a curved path by bending magnets, or when acted on by special
magnetic structures known as wigglers and undulators. The intensity of this kind of radiation is characterized by a high
brightness that cannot be achieved using conventional radiation sources such as X-ray tubes. For this reason it is possible
to select X-rays with a small energy bandwidth from the relative broad energy spectrum, while at the same time keeping
a fluence rate of photons high enough for efficient imaging. This technique is called X-ray monochromatization and is
achieved using a dedicated double-crystal monochromator, which is capable to filter the white synchrotron radiation
beam with a high level of accuracy allowing a beam nearly over a continuous range of energy (typically between 5 to 70

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 keV) to be produced. Moreover, the radiation produced in a synchrotron radiation facility has a parallel-beam shape,
while in a conventional X-ray source it has a fan-like shape that produces some distortion of the real object geometry.
Finally in case of a monochromatic X-ray source it is possible to create a simple table that directly relates the
attenuation coefficient and the density of the material with a high degree of accuracy 10, while, when a polychromatic X-
ray source is used the relationship between density and the attenuation coefficient would still exist 11-13 but it would
produce only approximate values 14.

1.2 CT and micro-CT (µCT)

X-ray computed tomography (CT) is an imaging technique developed in the early 1970s by Godfrey Hounsfield 15
that is capable to produce cross-sectional images representing the internal structure of an object.
A series of X-rays passing through the object being investigated are taken at many different angles to generate
different attenuation measurements called projections. These projections are combined to produce a 2D data set called a
sinogram. The sinogram is processed by a computer by means of a mathematical algorithm, called a filtered back-
projection, to reconstruct slices of the object under examination.
Clinical CT-scanners typically provide images with a spatial resolution in the range of 200 to 1000 µm. This is not
enough to provide detailed information of the trabecular bone structure as the partial volume effects degrade the images.
Micro-CT (µCT) scanners using conventional X-ray sources can achieve much better spatial resolution providing 3D
images with a voxel size in the range 10 to 100 µm 16;17. With these resolutions it is possible to extract internal details on
the microscopic scale such as quantitative parameters of trabecular architecture 18. This improved resolution is achieved
by focusing the electron bundle before it reaches the target and by reducing the dimension of the specimen that is
analyzed. Moreover, in contrast to the clinical CT-scanner, in order to increase mechanical precision in the µCT scanners
the specimen rotates while the acquiring apparatus is stationary.
By using a synchrotron radiation (SR) source instead of a traditional X-ray tube, the spatial resolution could be well
below 10 µm 19, because the high X-ray photon flux can provide a good signal-to-noise ratio, even with a monochromatic
beam. As already mentioned, while in a table-top µCT-scanner the beam has a fan-like shape, in a SR-based scanner the
beam is parallel, and therefore the projection of the images on the detector is not distorted. Using a monochromatic X-
ray the beam-hardening effect is not any longer an issue, making the discrimination between the different morphological
entities easier.
Combining the advantages of both the µCT scanning technique and the SR based monochromatic X-rays it is possible
to retrieve inner features that are density-depending like new osteons or less mineralized bone and at the same time
reducing beam-hardening and scattering artifacts 18;20.

2. MATERIAL

The bone specimens used in this study formed part of a larger animal study 21, where four adult male macaca
fascicularis monkeys, 6 to 7 years of age with a mean body weight of (6.5 ± 0.5)kg, were included. Large male monkeys
were selected rather than smaller female species to ensure adequate alveolar ridge size and height for implant placement.
The second premolar and first molar of the upper and lower jaws were extracted bilaterally and one titanium dental
implant (Exacta, Biaggini Medical Devices srl, La Spezia, Italy) was inserted in each extraction site. The implants were
made of commercially pure titanium, have a conical screw shape with a maximum cervical diameter of 3.3 mm and a
length of 7 mm, and presented a sand-blasted surface with a 1.5 mm polished neck. The loading of the implants was
achieved by inserting specifically manufactured abutments in the implants and connecting each of them to a pair of 50
cN superelastic Sentalloy springs. Fourteen implants were loaded following this procedure, while the remaining two
implants (one in the upper and one in the lower jaw of the same monkey) were left unloaded and served as control (Fig.
1).
At the end of the experiment, the animals were euthanized. Following sacrifice, both lower and upper jaws were
excised and the jaws were cut in separate blocks of bone tissue around each individual implant. All blocks were
processed following a standard procedure for the generation of undecalcified sections. All specimens were then prepared
for embedding by infiltrating them in methyl methacrylate monomer for 1 week. In order to have the longitudinal
implant axis perpendicular to the bottom and upper surfaces of the blocks, prior to the final polymerization each implant
was fitted with an extension screwed in the inner thread of the implant. This extension was then fixed into specially
prepared Plexiglas holders, thus assuring that the following cutting procedure would produce slices exactly perpendicular
to the longitudinal implant axis.

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 Fig. 1. Time line of the animal experiment.

Prior to sectioning, five randomly selected blocks were µCT-scanned both with a table-top scanner and a SR-based
microtomograph.

3. METHODOLOGY

3.1 Conventional µCT-scanning

The conventional µCT-scanning was performed using a table-top µCT-scanner (µCT-40, Scanco Medical,
Bassersdorf, Switzerland). This scanner consists of a sealed X-ray tube with a current of 0.16 mA, an energy level of 30-
70 kVp (20-50 keV), and a rotating stage that holds the sample. The scanner is equipped with a CCD-array detector
(2048x256 elements, 24 µm pitch). The samples were scanned using at an energy level of 70 kVp (50 keV).
Reconstructions of the 3D data-sets were made starting from the sinograms using a filtered back-projection algorithm.

3.2 Synchrotron radiation based µCT-scanning

The SR-based microtomography was performed at beamline W2 at HASYLAB at DESY (Hamburg, Germany). The
scanner is a 3D parallel beam acquisition apparatus 19, which uses a 2D detector. This consists of a fluorescent screen
(CdWO4, single crystal, thickness 500µm) that converts the monochromatic X-rays into visible light. The images are
acquired by a CCD (charge couple device) camera (KX2, Apogee Instruments, Inc.: 14 bit digitalization at 1.25 MHz,
1536x1024 pixels, each 9x9 µ m2). The samples were mounted on a rotator stage driven by several computer controlled
step motors that allow to position the sample in respect to the beam and to the detector and to turn the sample holder in a
precise way for the acquisition of the images. The energy used for scanning was set at a level of 50 keV.
At beamline W2 the X-ray beam is limited by collimators to 13 x 3.5 mm².
Thus, to be able to investigate the entire volume of the samples (about 20 x 21 x 11 mm³), the samples were scanned
having a field of view corresponding to only half of their width and thus the full images were acquired by turning the
samples around their axis from –180 to +180 degrees with an increment of 0.25 degrees. Up to eight different heights,
slightly overlapping, were necessary to scan one entire block. The reconstruction of each 3D data volume was made
starting from the sinograms using a filtered back-projection algorithm using IDL software (Research System Inc.,
Clolorado). Following reconstruction the resulting data volumes at different heights were combined to build five data
sets with a spatial resolution of 16 µm.

4. RESULTS

The data-sets generated with the conventional µCT scanner consisted of about 1024x1024x600 voxels, while the ones
generated with the SR-based µCT-scanning technique contained about 1467x1467x1300 voxels.

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 Fig. 2. Volume renderings of one sample as obtained from conventional µCT (left) and SR-based µCT (right).
Note the different level of details (arrows).

Fig. 3. Close up images of the bone-implant interface obtained from conventional µCT (left), SR-based µCT
(middle), and conventional histology (right).

The main differences between the images obtained by the table-top µCT scanner and the ones obtained with the SR
µCT scanner were the better resolution (respectively 37 µm and 16 µm) and the outstanding image quality obtained at
DESY. Two volume renderings of the same sample, with approximately the same voxel dimension (37 µm for the
conventional µCT and 32 µm for the SR-µCT, obtained by re-binning the original data-set), are presented (Fig. 2).
Although detailed morphology parts are recognizable in both of them, from a more careful inspection it can be noticed
that some of the smallest trabeculae that are clearly visible in the SR-based µCT data-set are not depict in the other data-
set (see arrows). The differences are becoming more evident on 2D slices extracted from both the reconstructed data sets.
The images obtained from SR scanning (Fig. 3, left and middle) are less noisy and the edges are sharper than on the
conventional µCT image. The difference between the two scanning methods is also expressed in their ability to represent
the implant-bone interface. Here the SR µCT scanning technique clearly displays all its superiority over the conventional
µCT scanning method: it is able to generate sharp and clear representations of the bone, even in close contact with the

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 Fig. 4. Slice-image obtained from the SR-based µCT- Fig. 5. Slice image obtained from the SR-based
scanner. Root resorption appears as a scalloped µCT-scanner. Marginal bone loss on the alveolar
surface (A); new bone formation can be observed crest can be noticed around the implant (circles).
around the roots of the premolar (B); the cementum
layer in the roots appears as a brighter ring around the
dentin core (C).

implant, thereby limiting the artifacts and the beam hardening effects to almost nothing. It is evident that an accurate
discrimination between the implant boundary and the true extension of bone in direct contact with the implant is only
possible using the SR-based scanning method. On conventional µCT-scans it is very difficult to identify the bone in
contact with the implant and in fact the amount of bony contact is overestimated. (Fig. 3, left). From the comparison of
the SR µCT scanning and the histological sections it is clear that the level of details is similar, whenever just bone
against marrow is to be discriminated (Fig. 3, middle & right). Moreover subtle changes in the morphology of the
calcified tissues can be observed in the SR-based images as evidence of biological activity. The root of the canine is
subject to severe root resorption and this appears as a scalloped surface (Fig. 4, A). Newly formed bone, characterized by
a lesser degree of mineralisation, can be observed around the roots of the premolar (Fig. 4, B). Finally, the difference in
mineral content between the dentin (~70 %) and the cementum (~55 %) in the roots can be noticed (Fig. 4, C).
From both a qualitative evaluation of the 3D data-sets, and visual evidence from the histological sections, it could be
seen that the implants were well osseointegrated and that a so-called lamina dura, had been formed and was almost
completely covering the implant endosseous surface. Moreover a small decrease in marginal bone height was found
around the insertion point for all the implants (Fig. 5).

5. CONCLUSIONS

Microtomography as applied in the present study has become a well-established tool in the field of bone mechanics
since it is a non-destructive technique and may provide unique 3D images of the bony architecture 22. It is predominantly
used to reconstruct the structure of trabecular bone, more seldom for cortical bone, and just recently to investigate bone
around dental implants 23;24. The reasons for this are to be found in the fact that due to beam hardening and scattering
effects, bone morphology around implant cannot be properly identified. Both problems can be solved using a
monochromatic X-ray source produced by synchrotron radiation instead of a traditional X-ray tube for the µCT-
scanning. The enhancement of microradiograph images of osseointegrated titanium implants using a monochromatic
beam compared to traditional microradiographs was observed previously 25, but SR-based X-rays have never been
applied to produce 3D reconstructions.

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 In the present study, the SR-based µCT-scanning techniques generated more detailed and sharper images than the
ones generated by conventional µCT scanner. This is more evident at the implant-bone interface, where due to beam
hardening and scattering artifacts, a clear picture of the bony structure could not be retrieved when the conventional X-
ray source was used. This set some reservations with respects to what was previously reported about the ability of table-
top µCT scanners in retrieving the amount of bone in contact with the implant surface 23;26.
More bone-implant contacts are generally associated to improved implant osseointegration and thus stability. From
the histological examination of undecalcified sections it is possible to retrieve both the amount of bone directly in contact
with the implant and the type of bone present at the interface, while from the µCT scans only the first quantity can be
calculated. This could suggest that the serial sectioning method may provide more reliable results. Yet with conventional
histology it is only possible to obtain cross sections in one particular plane and, because of the different physical
properties of bone and implants, the sections have to be cut using a milling diamante saw, which is typically 450 µm
thick. Indeed with this technique a significant amount of material is lost in the cutting process, so that the tissue
quantification is normally restricted to a few 2D sections. The advantage of the µCT technique is the ability to produce
3D data-sets that are equally detailed in all dimensions and therefore the possibility exists to reconstruct images in any
arbitrary plane. For the present, only qualitative analyses have been performed to investigate the correspondence
between the histological sections and the SR-tomographic virtual sections. The accuracy of the SR-based µCT-scanning
technique in retrieving the morphometric parameters conventionally used in histomorphometry (e.g. bone volume
fraction, surface to volume ratio, the extent of bone/implant contact) has not been estimated yet.
This investigation shows that both conventional and SR-based µCT scanning techniques are non-destructive methods
that provide detailed images of bone. However with the SR-based µCT scanning it is possible to generate improved
image quality of bone surrounding titanium dental implant even in the close vicinity of the bone-implant interface. This
resembles the level of details obtained with histological sections. Therefore SR-based µCT scanning could represent a
valid, unbiased truly three dimensional in vitro alternative to the serial sectioning method to evaluate the
osseointegration of dental implants.

ACKNOWLEDGMENTS

We acknowledge Thomas Kofod, Dept. of Maxillofacial Surgery, Aarhus University Hospital, Denmark, for his
support in the surgical procedure. This research was partly supported by IHP-contract II-00-064 EC of the European
Commission. The dental implants and the Sentalloy springs were kindly provided by Biaggini Medical Devices srl (La
Spezia, Italy) and Scanorto (Charlottenlund, Denmark), respectively.

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