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Jurnal CBCT 1
Jurnal CBCT 1
Jurnal CBCT 1
Norliza Ibrahim
Bassam Hassan
implant site using multislice CT,
Paul van der Stelt micro-CT, and cone beam CT
Daniel Wismeijer
Authors’ affiliations: Key words: bone density, bone volume fraction, dental implants, multislice computed tomog-
Azin Parsa, Norliza Ibrahim, Bassam Hassan, Paul raphy, micro-computed tomography, cone beam computed tomography
van der Stelt, Section of Oral Radiology,
Department of General and Specialized Dentistry,
Academic Center for Dentistry Amsterdam Abstract
(ACTA), Amsterdam, The Netherlands
Norliza Ibrahim, Department of General Dental
Objectives: The first purpose of this study was to analyze the correlation between bone volume
Practice and Oral & Maxillofacial Imaging, Faculty fraction (BV/TV) and calibrated radiographic bone density Hounsfield units (HU) in human jaws,
of Dentistry, University of Malaya, Kuala Lumpur, derived from micro-CT and multislice computed tomography (MSCT), respectively. The second aim
Malaysia
Daniel Wismeijer, Section of Implantology and was to assess the accuracy of cone beam computed tomography (CBCT) in evaluating trabecular
Prosthetic Dentistry, Department of Oral Function bone density and microstructure using MSCT and micro-CT, respectively, as reference gold
and Restorative Dentistry, Academic Center for standards.
Dentistry Amsterdam (ACTA), Amsterdam, The
Netherlands Material and methods: Twenty partially edentulous human mandibular cadavers were scanned by
three types of CT modalities: MSCT (Philips, Best, the Netherlands), CBCT (3D Accuitomo 170, J
Corresponding author: Morita, Kyoto, Japan), and micro-CT (SkyScan 1173, Kontich, Belgium). Image analysis was
Azin Parsa, DDS, MSc
Section of Oral Radiology, Department of General performed using Amira (v4.1, Visage Imaging Inc., Carlsbad, CA, USA), 3Diagnosis (v5.3.1, 3diemme,
and Specialized Dentistry, Cantu, Italy), Geomagic (studioâ 2012, Morrisville, NC, USA), and CTAn (v1.11, SkyScan). MSCT,
Academic Center for Dentistry Amsterdam (ACTA)
CBCT, and micro-CT scans of each mandible were matched to select the exact region of interest
Gustav Mahlerlaan 3004, 1081 LA Amsterdam,
The Netherlands (ROI). MSCT HU, micro-CT BV/TV, and CBCT gray value and bone volume fraction of each ROI were
Tel.: +31 20 598 0834 derived. Statistical analysis was performed to assess the correlations between corresponding
Fax: +31 20 598 0333
measurement parameters.
e-mail: a.parsa@acta.nl
Results: Strong correlations were observed between CBCT and MSCT density (r = 0.89) and
between CBCT and micro-CT BV/TV measurements (r = 0.82). Excellent correlation was observed
between MSCT HU and micro-CT BV/TV (r = 0.91). However, significant differences were found
between all comparisons pairs (P < 0.001) except for mean measurement between CBCT BV/TV and
micro-CT BV/TV (P = 0.147).
Conclusions: An excellent correlation exists between bone volume fraction and bone density as
assessed on micro-CT and MSCT, respectively. This suggests that bone density measurements could
be used to estimate bone microstructural parameters. A strong correlation also was found between
CBCT gray values and BV/TV and their gold standards, suggesting the potential of this modality in
bone quality assessment at implant site.
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 1
Parsa et al CT bone quality assessment at implant site
(Burghardt et al. 2011; Ibrahim et al. 2013a). between BV fraction derived from CBCT and Image processing
However, it is limited to ex vivo small bone CT numbers from MSCT has been reported All CT data sets were converted to Digital
samples and cannot be employed for patients. (Naitoh et al. 2010a; Gonzalez-Garcıa & Imaging and Communication in Medicine
Multiple X-ray projections with different Monje 2012). However, the relation between (DICOM3) format. As the scan orientation
angles in micro-CT allow a precise three- BV fraction and radiographic bone density in differs between micro-CT and the other two
dimensional (3D) reconstruction of the bone human jaws remains controversial (Stoppie systems, the z-axis of CBCT and MSCT
samples and assessment of bone trabeculae et al. 2006; Aksoy et al. 2009). Therefore, images was flipped to match that of micro-
(Martin-Badosa et al. 2003). Micro-CT is used the first purpose of this study was to ana- CT for further procedures. Micro-CT data
to measure several histomorphometric vari- lyze the correlation between bone volume sets were large in size therefore was not pos-
ables including bone volume (BV), total vol- fraction (BV/TV) and calibrated radiographic sible to be flipped by our workstation. Image
ume (TV), bone volume fraction (BV/TV), bone density (HU) in human jaws, derived analysis was performed using Amira (v4.1,
trabecular thickness (Tb.Th), trabecular num- from micro-CT and MSCT, respectively. The Visage Imaging Inc., Carlsbad, CA, USA),
ber (Tb.N), and trabecular separation (Tb.Sp) second aim was to assess the accuracy of 3Diagnosis (v5.3.1, 3diemme, Italy), Geoma-
(Odgaard 1997). CBCT in evaluating trabecular bone density gic (studioâ 2012, Morrisville, NC, USA), and
For bone density, multislice computed and microstructure using MSCT and CTAn (v1.11, SkyScan). MSCT images were
tomography (MSCT) is an established clinical micro-CT, respectively, as reference gold imported to 3Diagnosis software. Two cylin-
modality in which calibrated Hounsfield standards. drical shape virtual probes (with diameter
units (HU) can accurately be converted to and height of 0.7 and 8 mm, respectively)
BMD measurements (Shahlaie et al. 2003; were inserted at the edentulous region within
Material and methods
Shapurian et al. 2006). However, higher radia- the cancellous bone, with 3 mm buccolin-
tion exposure risk to patients in comparison gual distance between them (Fig. 1a, b).
Sample preparation and radiographic
with other modalities remains a main con- evaluation These probes were used as indicators to facil-
cern for applying MSCT for assessing bone Twenty partially edentulous human mandib- itate the selection of exact region of interest
quality (Ekestubbe et al. 1992, 1993; Freder- ular cadavers not identified by age, sex, or (ROI) from MSCT, CBCT, and micro-CT. For
iksen et al. 1995; Dula et al. 1996). Cone ethnic group were obtained from the func- MSCT, the probes were visible in a single
beam computed tomography (CBCT), due to tional anatomy department. The cadavers cross-sectional slice as the voxel size of
increased accessibility to dental practitioners, were sectioned at the mid-ramus level and MSCT scans was 0.67 mm, which is thick
more compact equipment and reduced cost fixed in formaldehyde (formaldehyde 74.79%, enough to allow the probes to be visible in
and radiation dose, has widely replaced medi- glycerol 16.7%, alcohol 8.3%, and phenol one slice. Subsequently, a rectangular area
cal CT for oral and maxillofacial imaging. 0.21%) and stored. A declaration was was drawn between the two probes from the
Several studies reported high geometric accu- obtained from the Functional Anatomy slice of interest to define the ROI for density
racy of CBCT for linear measurement (Nai- department to use this human remains mate- measurements. The mean HU values from
toh et al. 2004; Lou et al. 2007; Lagravere rial for research purposes. The restorative each ROI were calculated. All ROIs were
et al. 2008), while its reliability in bone qual- materials which can produce artifact such as totally within the cancellous bone, excluding
ity evaluation remains controversial. Only amalgam filling and metal crowns were cortical bone, inferior dental canal, and any
few studies suggested that CBCT could be removed from dentitions. The mandibles large bone defect.
applied to assess trabecular bone microstruc- were scanned by three types of CT modali- For CBCT, a volume-based 3D registration
ture (Liu et al. 2007; Corpas et al. 2011). ties: MSCT (Philips, 120 kVp, 222 mA, algorithm using Geomagic software was
Additionally, CBCT does not represent cali- 1.128 s, 0.67 mm isotropic voxel size, Best, applied to transform the inserted probes from
brated voxel gray values expressed in HU the Netherlands), CBCT (3D Accuitomo 170, the MSCT data sets to the CBCT scans. A
(Hua et al. 2009). Yet, many attempts have 90 kVp, 5 mA, 30.8 s, 4 9 4 cm FOV, 0.08 standard triangulation language (STL) surface
been conducted to assess the feasibility of mm isotropic voxel size, J Morita, Kyoto, file of the MSCT and CBCT scans were
converting CBCT gray values to actual den- Japan), and micro-CT (SkyScan 1173, 130 matched, and the probes were transferred
sity measurements. High correlation between kVp, 61 mA, 35 min, 35 lm isotropic voxel from MSCT scans to the exact region on
HU derived from MSCT and CBCT voxel size, Kontich, Belgium). In MSCT scans, the CBCT’s (Fig. 1c). As a result, new CBCT data
gray values has been demonstrated, hinting occlusal plane of each mandible was set sets which include the probes were obtained.
at the potential of CBCT in bone density perpendicular to the floor with zero gantry Using 3Diagnosis, eight consecutive slices
assessment (Aranyarachkul et al. 2005; tilt, whereas in CBCT scans, it was set passing through the probes were selected
Lagrav ere et al. 2006; Naitoh et al. 2009, parallel to the floor according to manufac- from each CBCT data set to calculate the
2010b; Nomura et al. 2010; Parsa et al. 2012; turer’s recommended protocol. The edentu- mean gray values (radiological density). This
Reeves et al. 2012; Cassetta et al. 2013). lous region of each mandible was located at is because slice thickness in CBCT is
However, the excessive scattering and tech- the center of FOV in CBCT scans. Owing to 0.08 mm which approximately amounts to
nology-specific artifacts produced in CBCT the large gantry of applied micro-CT 89 thinner than the equivalent slice thick-
have been denoted as the perpetrator for the (140 mm in diameter, 200 mm in height), ness in MSCT. A rectangular region was also
unreliable BMD measurements (Yoo & Yin mandibles were not sectioned to smaller drawn between the two probes similar to
2006; Hua et al. 2009; Araki & Okano 2011; samples. To prevent the possible micromove- MSCT and gray values from corresponding
Nackaerts et al. 2011; Schulze et al. 2011). ments during the scanning due to the large anatomical locations were derived.
High correlation between bone volume size of the samples, a cylindrical shape Styro- Cone beam computed tomography radiolog-
fraction (BV/TV) provided by micro-CT and foam was used to fix and mount the sample ical density of each mandible’s ROI was con-
voxel gray value from CBCT, and also into the holder. sidered as the mean of eight calculated gray
2 | Clin. Oral Impl. Res. 0, 2013 / 1–7 © 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Parsa et al CT bone quality assessment at implant site
Fig. 1. (a) Three-dimensional reconstruction of a mandible multislice computed tomography (MSCT) scan with inserted probes. (b) Close-up view of probes and (C) three-dimen-
sional reconstruction of a mandible cone beam computed tomography (CBCT) scan with transferred probes.
values. Subsequently, the selected ROIs were correlation coefficient was used to assess the CBCT and micro-CT BV/TV measurements
saved as a bitmap (BMP) image files to allow linear relation between corresponding (r = 0.82). Excellent correlation was observed
the trabecular microstructure evaluation. measurement parameters. Finally, a Bland– between MSCT HU and micro-CT BV/TV
Using Amira, each micro-CT scan was Altman plot was used to assess the accuracy (r = 0.91). Bland–Altman analysis showed the
cropped to have a smaller sample including of CBCT in measuring trabecular BMD and bias in measuring BV/TV between CBCT and
the ROI. Due to large micro-CT data sets, bone microstructural density by plotting the micro-CT is smaller (4.44/lm) than measur-
the superimposition of CBCT and micro-CT difference between the measurements of ing the density between CBCT and MSCT
scans was performed as follows: maximum CBCT against MSCT density and micro-CT (154.65HU) (Fig. 3a, b). The 95% measure-
alignment of both data sets was obtained by BV/TV against the means of the compared ment errors are between 21.31 to 30.19 for
manually matching and superimposition of measurements. BV/TV and 29.74–279.56 for density measure-
isosurfaces generated in Amira software. Sub- ment. The differences of CBCT and micro-
sequently, sixteen micro-CT slices (corre- CT BV/TV measurements were minimal
spondence to the eight CBCT slices) were Results (4.44/lm), suggesting strong agreement.
selected and saved as a 16-BMP image file
(65536 gray values). Then, these bmp files Excellent intra-observer reliability (ICC ≥
were exported to CTAn software for trabecu- 0.97) was revealed for repeated measurements Discussion
lar microstructure evaluations (Fig. 2a). A in the three systems. Therefore, the mean of
rectangular ROI for trabecular was selected two measurements was calculated for further It has been proven that the success of an
on each data set slice by slice (Fig. 2b). All analysis. The mean HU of the selected ROI inserted implant strongly depends on the
images were thresholded using an automated ranged from 60 to 507.6 (mean 222.85 & quality, beside the quantity, of the sur-
histogram analysis and binarized (Fig. 2c) to standard deviation [SD] 140.5), while CBCT rounded bone (Jaffin & Berman 1991; Jemt
allow the measurement process. On micro- gray values ranged from 161.6 to 665.6 (mean et al. 1992). In jawbones, density measure-
CT data sets, the ROI was again verified by 377.49 & SD 127.4). The negative HU derived ments derived from MSCT HU are highly
carefully comparing slices with CBCT’s (as from MSCT for case 4, 16, and 20 (Table 1) reliable (Schwarz et al. 1987; Shapurian et al.
reference). This was performed to reduce bias may indicate fat in trabecular spaces (Parsa 2006). However, bone density alone does not
which may have been introduced during the et al. 2012). Calculated BV/TV of the same fully represent bone quality and should be
manual superimposition of the two data sets. ROI ranged from 2.24 to 75.83 (mean 32.35 & considered together with bone micro-archi-
All measurements were performed twice SD 18.81) for micro-CT and from 3.73 to tecture to estimate bone strength and frac-
with 1-month interval by a trained maxillofa- 68.72 (mean 36.79 & SD 23.17) for CBCT ture resistance (Diederichs et al. 2009).
cial radiologist. (Table 1). Paired t-test showed significant dif- Histomorphometrically, bone volume frac-
ferences (P < 0.001) between all comparison tion, which is the trabecular BV per tissue
Data analysis pairs except for mean measurement between volume (TV) expressed in percentage, is the
Statistical analysis was performed using SPSS CBCT BV/TV and micro-CT BV/TV (P = most important parameter (Parfitt et al.
(v17.0, SPSS Inc., Chicago, IL, USA). To 0.147). In all selected ROIs, CBCT showed a 1987). Micro-CT is accepted as a gold stan-
determine the intra-observer reliability of the higher density than MSCT HU and a higher dard modality for trabecular microstructure
radiological and microstructural density mea- BV/TV than that of micro-CT. The normal assessment, but it cannot be employed in the
surement, intraclass correlation coefficient distribution of measurements was confirmed clinic (Burghardt et al. 2011). In this study,
(ICC) was used. The Shapiro–Wilk test was by visually inspecting the histogram and the our aim was to investigate the possible corre-
used to verify the normality of the data. result of the Shapiro–Wilk test (P > 0.05). lation between bone quality measurements
Paired t-test was used to assess the mean dif- Therefore, the use of the t-test and Bland– of clinically applicable scanners in compari-
ference between MSCT and CBCT density Altman test is justified. Strong correlations son with micro-CT.
measurements and between CBCT BV/TV were observed between CBCT and MSCT A study on porcine vertebral cancellous
and micro-CT BV/TV, while Pearson’s density measurements (r = 0.89) and between bone revealed a high correlation between HU
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 3 | Clin. Oral Impl. Res. 0, 2013 / 1–7
Parsa et al CT bone quality assessment at implant site
4 | Clin. Oral Impl. Res. 0, 2013 / 1–7 © 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Parsa et al CT bone quality assessment at implant site
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 5 | Clin. Oral Impl. Res. 0, 2013 / 1–7
Parsa et al CT bone quality assessment at implant site
the potential influence of varying voxel size each model. Developing such a standard for absorb the beam causing extinction artifacts
on visibility of hard tissue structures such as manufacturing CBCT systems may help in rather than beam-hardening artifacts (Hara-
bone remains largely unknown. A recent sys- generalizing research findings in the future. mati et al. 1994). Resulted artifacts degrade
tematic review of the literature concluded The study was also limited as surrounding the quality of images and affect the gray
that there is a systematic lack of evidence anatomical structures including the tongue scales of normal anatomical structures close
regarding the impact of varying voxel size in and vertebra were absent. As a result, in to foreign bodies. The severity of mentioned
CBCT on diagnostic performance and that CBCT scans, partial object artifacts resulting effect is also dependent on the energy of
possibly different voxel sizes might lead to from structures placed outside the scan field applied X-ray beam, density, and geometry of
comparable diagnostic outcomes (Spin-Neto were not simulated. It has been previously artifact inducing materials (Schulze et al.
et al. 2013). Only one study could be identi- noted that artifacts resulting from partial 2010). Therefore, further CBCT studies on
fied which demonstrated a possible effect of sampling of objects outside the scan field assessing the effect of dental restorative
varying voxel size on cancellous bone mea- could result in a deviation in voxel gray val- materials on bone density and microstructure
surements in micro-CT (Yeni et al. 2005). ues with CBCT (Katsumata et al. 2009; Araki measurements are suggested.
However, it remains unknown whether the & Okano 2011). Gray values obtained from In conclusion, this present study demon-
same applies to CBCT. In this study, a con- the cadaver may also deviate from the clini- strates the reliability and validity of CBCT in
scious effort was made to optimize image cal situation. bone quality assessment. However, unlike
quality through selecting the scan protocols In present study, restorative materials the bone volume fraction measurement, the
and voxels sizes as recommended by the which could induce artifacts were removed accuracy for density measurement is unfavor-
manufacturer for the chosen FOV’s. Our from our samples. However, in normal clini- able. In assessing density using CBCT, the
results are limited to one CBCT system cal settings, presence of metallic materials in microstructural assessment (BV/TV) is there-
(Accuitomo 170), and results may vary on oral cavity is quite common. In CBCT scans, fore recommended. However, based on the
other systems. The design specifications of restorative materials with high atomic num- inconsistencies in CBCT designs, further
different systems still vary (De Vos et al. bers harden the X-ray beam causing streak studies are suggested on validation of differ-
2009). The lack of a technical standard for artifacts in reconstructed images (Schulze ent systems.
the development of CBCT systems has led to et al. 2011), while many high-density filling
a wide disparity in the physical parameters of materials such as amalgam completely
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