Assessments of trabecular bone density at implant sites on

CT images
Rubelisa Cândido Gomes de Oliveira, DDS,a Cláudio Rodrigues Leles, DDS, MS, PhD,b
Leonardo Martins Normanha, MD,c Christina Lindh, DDS, Odont dr,d and
Rejane Faria Ribeiro-Rotta, DDS, MS, PhD,e Goiânia, Goiás, Brazil and Malmö, Sweden
FEDERAL UNIVERSITY OF GOIÁS, GOIANO INSTITUTE OF RADIOLOGY AND MALMÖ UNIVERSITY

Objectives. To evaluate the association between trabecular bone density measurements of potential implant sites
made on axial DICOM images (DentaCT software) and on the same images with eFilm workstation, to correlate
bone densities in Hounsfield units (HU) with subjective classification, and to establish a quantitative scale for
each bone quality class.
Study design. Twenty-seven maxillary and 27 mandibular computed tomographic (CT) examinations of 75 potential
implant sites were selected. Trabecular bone density was evaluated with DentaCT and eFilm. Bone quality was
subjectively evaluated by 2 examiners. Descriptive statistics, between- and within-group comparison, correlation
analysis, and Bland-Altman plot were used for data analysis.
Results. DentaCT measurements were higher than eFilm (P ⬍ .001). Bone type 2 was the most prevalent, and bone
density was significantly reduced from bone types 1 to 4. Quantitative parameters ranged as follows: bone type 4
⬍200 HU, bone types 2 and 3 ⬎200 to ⬍400 HU, and bone type 1 ⬎400 HU.
Conclusion. Different qualities of bone can be found in any of the anatomical regions studied (anterior and posterior
sites of maxilla and mandible), which confirms the importance of a site-specific bone tissue evaluation prior to implant
installation. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105:231-8)

Two oft-mentioned factors that are considered important
in the consolidation of the bone-implant interface and that
can influence surgical technique, healing time, and pro-
gressive loading during prosthodontic rehabilitation are
bone quality and bone quantity.1-6 The term bone quan-
tity is most often understood as the amount of bone
(e.g., height and width of the alveolar crest) available
for implant installation, whereas bone quality is a far
more comprehensive term with no clear definition,
encompassing several aspects of bone physiology,
degree of mineralization, and structural properties
(architecture, morphology).7-9 The importance of
each aspect in implant treatment is still not fully
understood.2,9,10
a
Graduate Student, School of Dentistry, Federal University of Goiás,
Goiânia, Goiás, Brazil.
b
Associate Professor, Department of Oral Rehabilitation, School of
Dentistry, Federal University of Goiás, Goiânia, Goiás, Brazil.
c
Medical Radiologist, Director, Goiano Institute of Radiology, Goiânia,
Goiás, Brazil.
d
Associate Professor, Department of Oral and Maxillofacial Radiol-
ogy, Faculty of Odontology, Malmö University, Malmö, Sweden.
e
Associate Professor, Department of Oral Medicine, School of Den-
tistry, Federal University of Goiás, Goiânia, Goiás, Brazil.
Received for publication Dec 16, 2006; returned for revision Jul 13,
2007; accepted for publication Aug 10, 2007.
1079-2104/$ - see front matter
© 2008 Mosby, Inc. All rights reserved.
doi:10.1016/j.tripleo.2007.08.007
Numerous studies report implant treatment outcome by
using the classification of bone quality proposed by Lek-
holm and Zarb,11 which is mainly based on the subjective
feeling of the surgeon during drilling. Other approaches
used to assess bone tissue before and during implant
treatment have been conventional radiography,12,13 inser-
tion torque resistance,14-16 dual energy x-ray absorptiom-
etry,17,18 digital image analysis,19 ultrasound,20 and com-
puted tomography (CT).6,7,8,21 Most of these methods
assess bone density quantitatively, but some are imprac-
tical for the clinician and others are too invasive for
routine clinical use.
Recently, efforts in the oral imaging field have focused
on developing instruments that accurately and automati-
cally measure bone density by measurements of x-ray
absorption. The use of CT has continued to grow, al-
though systematic use in clinical practice has been limited
by concerns about high radiation doses and relatively high
cost.22,23 Such risk can be reduced considerably by low-
ering the dose output of the scanner,24 and the diagnostic
benefits of CT seem to outweigh the lower risks associ-
ated with modern improved scanners that produce low
doses of radiation. Cone-beam CT appears to be the
medium of the future, thus, many changes will be made to
improve this dental imaging method.25
Norton and Gamble21 used interactive software spe-
cially designed for the maxilla and mandible to describe
an objective scale of bone density based on mean

231

232 de Oliveira et al.
Hounsfield unit (HU) values determined in CT examina-
tions. This scale may help clinicians classify bone tissue
before implant treatment and is based on the densities of
trabecular, and when present, cortical bone, but the au-
thors gave no detailed description of the quantitative
relationship between bone density and bone quality.
Bone density measurements like those suggested by
Norton and Gamble21 are restricted to clinicians who
have access to the particular CT software, which is
usually costly and generally has limited applicability.
Nowadays, digital imaging and communications in
medicine (DICOM) images can be displayed not only on
workstations but also on personal computers (PCs) with
little monetary investment. Personal computer software
allows clinicians to use image processing tools (e.g., to
determine bone density and reformat images for greater
clarity) from their own offices.21,26 No study has shown
whether bone density measurements made on electroni-
cally transferred images differ significantly from those
made on original DICOM images.
The aims of this study were therefore to (1) correlate
the mean densities of trabecular bone measured with 2
software applications, eFilm and DentaCT, at potential
implant sites on the anterior and posterior maxilla and
mandible, (2) correlate these measurements with bone
quality classifications made according to Lekholm and
Zarb,11 and (3) establish a quantitative scale for each
bone quality classification.
MATERIAL AND METHODS
Selection of CT examinations and potential
implant sites
Images from 27 maxillary and 27 mandibular CT
examinations of 51 patients (31 women, 20 men)
were chosen. The patients had been referred to the
Instituto Goiano Institute of Radiology/José Nor-
manha Foundation, Goiânia, Brazil, between 1999
and 2004 for radiographic examination as part of
implant treatment planning. Scans were made ac-
cording to the following technical protocol: Elscint
Twin II helical scanner (Elscint, Haifa, Israel), 120
to 140 kV, 200 to 400 mAs, 250-mm field of view,
dual 1-mm-thick slices, 1-mm increments, ultrahigh
resolution, 512 ⫻ 512 matrix, 1.5 zoom, filter D, 0°
gantry angulation.
The patients were either fully or partially edentate, and
selection criteria included edentulous areas with the po-
tential for implant placement and an alveolar thickness
sufficient to support a region of interest (ROI) of at least
0.1 cm2 in trabecular bone. In the 54 CT examinations, 75
potential implants sites were identified. The local ethics
committee of the Hospital das Clínicas/School Hospital/
Federal University of Goiás, Goiânia, Brazil, approved the
study protocol.
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February 2008
Measurements of bone density with eFilm
workstation
Three sequential axial images (1-mm thickness, origi-
nal magnification ⫻1.5) of each of the 75 potential im-
plant sites were selected (N ⫽ 225) using eFilm (eFilm,
version 1.5.3, Merge Healthcare, Milwaukee, WI) soft-
ware application in an IBM-compatible PC. The operator
determined the center of the ROI in all sites. The spatial
coordinate tool (x, y) was manually set to define a circular
or oval ROI at the same anatomic location on each of the
3 axial images. The y-coordinate, which could vary ver-
tically, was held constant, and the x-coordinate, which
could vary horizontally, was adjusted according to the
anatomic morphology of the arch and placed at the center
of the trabecular bone in each axial image (Fig. 1). The
distance between the most posterior part of the dental arch
and the ROI in trabecular bone (Fig. 2) was established in
the central axial image. This distance was used as a
reference to determine the anatomic position of the ROI
when the DentaCT software application (DentaCT, ver-
sion 3.000, Picker International Inc., Cleveland, OH) was
used, since DentaCT does not have a coordinate tool. The
ROI was defined from the point of interest and bone
density was automatically displayed using an elliptical
measurement tool.
The examiner measured the bone density of each
ROI 3 times on each of the 3 axial images. The mean
was calculated from the 9 measurements made for each
potential implant site.
DentaCT bone density measurements
The distance between the most posterior part of the
dental arch and the point of interest for each potential
implant site was reproduced in the central axial image of
each selected site. The ROI was defined from a point of
interest, and bone density was automatically displayed
using DentaCT in a Silicon Graphics Workstation (SGI
Company, Mountain View, CA). Bone density values in 2
other axial images (coronally and apically to the central
image) were obtained automatically by dragging the
scrollbar to select the images. Mean densities and standard
deviations in HU and the circumferential area of the ROI
(mm2) in trabecular bone were automatically calculated
by the software (Fig. 3).
The same examiner made all measurements of bone
density and calculated the mean in the same way as
described for the eFilm workstation.
Classification of bone quality
Axial images were reformatted with DentaCT (n ⫽
75) into transversal sectional images to produce a buc-
cal-lingual view of each potential implant site. The
bone windows of the transversal views were printed on
25.7 ⫻ 36.4-cm radiographic film (Fujifilm, Fuji Photo
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Volume 105, Number 2 de Oliveira et al. 233

Fig. 1. A-C, Sequential axial images of the mandible. The center of the region of interest was determined at all potential implant
sites by using the spatial coordinate tool (x, y). The y-coordinate, which could vary vertically, was held constant (y ⫽ 136), and
the x-coordinate, which could vary horizontally (x ⫽ 168, 154, 152), was adjusted according to the anatomical morphology of the
arch and placed at the center of the trabecular bone in each axial image.

Film Co., Tokyo, Japan). A black mask was affixed to
the films to restrict viewing on the light box to the ROI.
Two trained and calibrated independent examiners (an
oral maxillofacial radiologist and an implant specialist)
classified the bone tissue imaged in the transversal sec-
tions according to the bone quality classifications pro-
posed by Lekholm and Zarb.11 Each examiner assessed
the bone tissue twice to ensure intraexaminer reliability.
The subjective classification of the bone tissue was the
classification with the highest agreement in the 4 evalua-
tions. When the examiners disagreed, the final decision
was determined by consensus.
Statistical analysis
Descriptive statistics included means, standard devi-
ations, and confidence intervals. Between-group com-
parisons of trabecular bone density in the ROI were
made with the paired Student t test. Within-group com-

234 de Oliveira et al.
Fig. 2. Axial image of the mandible. The distance between
the most posterior part of the dental arch and the point of
interest was determined in the central axial image.
parisons of trabecular bone density measurements of 4
anatomic jaw regions were made for each software by
using the Kruskal-Wallis test. Pearson’s correlation co-
efficient (r) and Spearman’s correlation coefficient (rs)
were used to measure correlations between variables.
Bland-Altman plot was used to assess how much the
difference between eFilm and DentaCT differ system-
atically from zero (bias) and how much the difference
varies (error).27 Statistical significance was set at P ⬍
.05 and MedCalc software (version 9.3.8.0; Mari-
akerke, Belgium) and SPSS 10.0 (SPSS Inc., Chicago,
IL) were used for data analyses.
RESULTS
The distribution of the 225 axial images was as follows:
6 anterior maxillary (AMx) sites (18 axial images), 6
anterior mandibular (AMd) sites (18 axial images), 29
posterior maxillary (PMx) sites (87 axial images), and 34
posterior mandibular (PMd) sites (102 axial images).
Table I lists the bone densities of 75 potential man-
dibular and maxillary implant sites. The mean densities
determined in both software applications were greater
in the anterior mandible, followed by the anterior max-
illa, the posterior mandible, and the posterior maxilla, but
wide ranges of bone density were observed for all ana-
tomic regions, that is, high and low bone density values
were found in all anatomic regions. The Kruskall-Wallis
test showed no significant differences among anatomic
regions for either software.
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February 2008
DentaCT measurements of trabecular bone density
were significantly higher than eFilm measurements (t ⫽
4.50; P ⬍ .001). Mean differences were 41.3 HU, 70.9
HU, 11.5 HU, and 15.1 HU for AMd, AMx, PMd, and
PMx, respectively. Measurements with each software
were highly correlated (r ⫽ 0.95; P ⬍ .001). According
to the Bland-Altman plot analysis (Fig. 4), eFilm ap-
peared to consistently underestimate bone density com-
pared with DentaCT; 95% of the differences in the
readings between eFilm and DentaCT (⫾1.96 SD) lie
between 60.1 and ⫺102.2 (mean ⫽ ⫺21.0).
Interexaminer and intraexaminer agreement ranged
from 44% to 69% for subjective evaluation of bone
quality, and Spearman correlation coefficient ranged
from 0.50 to 0.71 (P ⬍ .01).
According to the subjective evaluation (Table II),
bone type 2 was most prevalent (49.3%), of the 4
anatomical regions, was most frequently observed in
AMd (4:6), AMx (4:6), and PMd (21:34). Bone type 1
occurred in only 3 potential implant sites (4%). Table
III presents trabecular bone density values in each
category of bone quality as determined with DentaCT
and eFilm according to the classification of Lekholm
and Zarb.11 Bone density was significantly reduced
from bone type 1 to bone type 4 (P ⬍ .001).
Reference parameters for predicting bone quality from
known values of trabecular bone density are defined in
Table III by using 95% confidence intervals for each bone
type. Actual values were rounded off for clinical purposes
(Table IV).
DISCUSSION
DentaCT is a well-known software application used to
reformat images of the maxilla and mandible that are pro-
duced according to digital imaging and communications in
medicine (DICOM) standards. The PC-compatible software
eFilm can read, receive, and send DICOM images, allowing
the clinician to evaluate, in his own office, bone density and
other bone tissue parameters on sectional images. This
software creates a database that can be used in patient-
clinician communication and in the development of a
variety of files, such as teaching files.
Trabecular bone density is an important factor for
achieving good osseointegration because it may be re-
sponsible for the biologic response, and to a certain extent,
the mechanical support of an implant. Regeneration and
remodeling of bone at the implant-tissue interface (sec-
ondary stability) can be determined by trabecular bone
density.15,28,29 In this study, original axial images were
used to define an ROI in the trabecular bone fraction of
the receptor site.
Comparison across studies that measured HU bone
density is difficult due to differences in methodological
approaches. The use of different softwares,6,7,8,21,30,31 the
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Volume 105, Number 2 de Oliveira et al. 235

Fig. 3. A, Reproduction of the distance between the most posterior part of the dental arch and the point of interest in the central
axial image. B, The region of interest in trabecular bone was defined from a point of interest, and trabecular bone density was
automatically displayed using DentaCT software (Mean [Av] ⫽ 481.40 HU; SD ⫽ 226.50; Area [Ar] ⫽ 0.115 cm2). Bone
densities in the coronal (C) and apical (D) views were obtained automatically by dragging the scrollbar to select the images.

Table I. Trabecular bone densities of potential implant sites determined with the eFilm and DentaCT
software applications
Software Region No. Minimum (HU) Maximum (HU) Mean (HU) SD 95% CI P value*
eFilm AMd 6 61 716 341.83 233.06 97.24-586.41 .674
AMx 6 71 601 287.33 181.26 97.10-477.55
PMd 34 72 1010 294.85 191.92 227.88-361.81
PMx 29 ⫺58 560 240.44 177.79 172.81-308.07
DentaCT AMd 6 100.50 782.82 383.22 243.33 127.85-638.58 .344
AMx 6 95.96 568.49 370.38 176.71 184.93-555.83
PMd 34 88.07 999.92 306.30 187.15 241.00-371.60
PMx 29 ⫺41.06 589.83 255.52 184.01 185.53-325.52
HU, Hounsfield units; CI, confidence interval; AMd, anterior mandible; AMx, anterior maxilla; PMd, posterior mandible; PMx, posterior maxilla.
*Kruskall-Wallis test.

inclusion of cortical bone in the ROI,6,21,31 and the use of
reformatted images to assess bone density6,7,8,21,30-32 are
important factors that limit inferences about other studies.
The definition of the ROI was also different from Taguchi
et al.,26 in which an ROI greater than 1 cm2 in quantitative
computed tomography presented higher precision for
bone density measurements. Nevertheless, the softwares
used in our study do not allow manually outlining of an
ROI. Consequently, obtaining a 1-cm2 area restricted to
the trabecular bone is very difficult to achieve in a narrow
bone with anatomical heterogeneity, as commonly ob-
served in the jaws.
Strong correlation was found between DentaCT and
eFilm bone densities (r ⫽ 0.95), but Bland-Altman anal-
ysis showed that the scatter of the differences increases as
the bone density increases (i.e., the variation depends on
the magnitude of the differences). It was considered that
differences within mean ⫾1.96 SD are clinically impor-
tant, and the 2 softwares may not be used interchangeably
(Fig. 4).
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236 de Oliveira et al. February 2008

The mean bone densities (HU) of the different bone

types were not distributed anatomically as reported by
Norton and Gamble.21 When only trabecular bone density
was considered, bone types 1, 2, and 3 were found in all
examined regions, except for bone type 1 in the anterior
maxilla. Bone type 4 was found only in maxillary regions
(Table II). This large variation between neighboring zones
limits the significance of mean bone density values and
emphasizes the importance of site-specific measurements
of bone tissue before implant treatment, as suggested by
Lindh et al.9 Site-specific measurements are important,
not only for a general prediction of treatment outcome but
also in the evaluation of how long of an interval between
first- and second-stage surgical procedure and loading is
Fig. 4. Bland-Altman plot analysis of bone density as mea- needed.2,4,15,16 According to Ericsson and Nilner,10 it is
sured with eFilm and DentaCT. important that an objective tool for the evaluation of bone
tissue be developed so that clinicians can more easily
determine when to load an implant: immediately, earlier,
or later.
Table II. Distribution of subjective classifications of In the subjective evaluation, a wide range of mean bone
bone type according to anatomical region in the axial densities (HU) was observed in each of the 4 bone types
images (n ⫽ 75) defined by Lekholm and Zarb,11 particularly for types 2
Subjective classification and 3. The same was also observed by Norton and Gam-
Region Type 1 Type 2 Type 3 Type 4 Total ble21 and Shahlaie et al.6 This may be a reflection of the
AMd 1 4 1 0 6 limitations of a subjective system of bone density assess-
AMx 0 4 1 1 6 ment.
PMd 1 21 12 0 34
A density scale, rather than absolute values, would
PMx 1 8 10 10 29
Total (%) 3 (4%) 37 (49.3%) 24 (32%) 11 (14.7%) 75 (100%) be more flexible and accurate in helping the clinician
categorize bone quality, as a diagnostic predictor.
AMd, anterior mandible; AMx, anterior maxilla; PMd, posterior man-
dible; PMx, posterior maxilla.
Such a scale, like the one proposed by Norton and
Gamble,21 would accommodate the “gray zones” be-
tween the bone groups, which exist due to standard
deviations. Quantitative parameters for bone type 4
Differences in the bone densities of the 4 anatomical were all values below ⫹200 HU. This type of bone
regions in the mouth were significant, with the anterior requires a meticulous surgical technique.11 Interme-
mandible yielding a higher mean bone density value, diary values between ⫹200 and ⫹400 HU represent con-
followed by the anterior maxilla, the posterior mandible, ditions favorable for osseointegration (bone types 2 and
and the posterior maxilla. These differences have also 3),11 and values above ⫹400 HU indicate denser bone
been observed by other authors.11,18,21,31 But independent (bone type 1), which has a greater risk of overheating
of method, the bone densities reported in those studies during implant installation11 (Table IV). The difficulty in
were higher than those found in this study because their differentiating between bone types 2 and 3 based on a
measurements included the trabecular portion and the subjective visual evaluation or quantitative bone density
outer cortical shell. Lindh et al.9 used CT to evaluate measurements in the present study was also found previ-
maxillary bone and measured total bone density (cortical ously by other authors.21,30,33
and trabecular) and trabecular bone alone. Mean trabecu- Shapurian et al.30 evaluated trabecular bone density and
lar bone density was on average 24% lower than total found a variation that ranged from ⫺240 to 1159 HU (the
bone density; in the anterior region (canine and incisor amplitude found in this study was ⫺57-1010 HU) in the
sites) and in the posterior region (molar and premolar anterior mandible, with the highest mean density value,
sites), mean trabecular bone densities were 19% and 28% followed by the anterior maxilla, the posterior maxilla,
lower, respectively, than corresponding total bone densi- and the posterior mandible.
ties. Shapurian et al.30 detected no significant differences A small sample of sites located in high-density re-
between the posterior maxilla and mandible, even though gions11,18,21 and usually classified as type 111 had a wide
the posterior maxilla had a slightly higher mean density confidence interval for the trabecular bone densities de-
than the posterior mandible. termined with both software applications (Table III).
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Volume 105, Number 2 de Oliveira et al. 237

Table III. Trabecular bone densities determined with DentaCT and eFilm for bone type*
Software Bone type Minimum (HU) Maximum (HU) Mean (HU) SD 95% CI P value†
eFilm Type 1 559.90 1010.30 762.06 228.71 193.92-1330.20 ⬍.001
Type 2 61.30 538.60 316.74 142.00 269.39-364.09
Type 3 ⫺57.83 600.78 223.22 159.48 155.88-290.56
Type 4 ⫺5.43 321.24 127.98 108.61 55.01-200.94
DentaCT Type 1 585.82 999.92 789.52 207.13 274.98-1304.06 ⬍.001
Type 2 100.11 589.83 341.72 140.41 294.91-388.54
Type 3 ⫺41.05 568.49 243.81 164.09 174.52-313.10
Type 4 9.20 331.50 134.75 105.81 63.66-205.83
HU, Hounsfield units; CI, confidence interval.
*Type 1, n ⫽ 3; type 2, n ⫽ 37; type 3, n ⫽ 24; and type 4, n ⫽ 11. Bone types according to Lekholm and Zarb.11
†Kruskal-Wallis test.

Table IV. Reference values of trabecular bone density for each bone type*
Norton and Gamble21 Trabecular bone density
Bone quality according to trabecular bone according to this study
Lekholm and Zarb11 density scale (HU) (HU)
Bone type 1 ⬎⫹850 ⬎⫹400
Almost the entire jaw is
comprised of
homogenous compact
bone

Bone type 2
A thick layer of compact
bone surrounds a core
of dense trabecular
bone

Bone type 3 ⫹500 to ⫹850 (Bone ⫹200 to ⫹ 400 (Bone

A thin layer of compact types 2 and 3) types 2 and 3)
bone surrounds a core
of dense trabecular
bone, favorable
strength

Bone type 4 0 to ⫹500 ⬍⫹200

A thin layer of cortical
bone surrounds a core
of low-density
trabecular bone

— Bone type 4† ⬍0 —
HU, Hounsfield units.
*According to the classification of Lekholm and Zarb.11
†Additional bone quality category described as failure zone by Norton & Gamble. The implant will have considerable surface contact with fat
marrow.

238 de Oliveira et al.
In conclusion, this study confirms the importance of a
site-specific bone tissue evaluation prior to surgical pro-
cedures in implant installation. A quantitative reliable
scale could be helpful if it is taken together with all
clinical relevant information for implant planning. Besides
the subjectiveness of data interpretation, the extent to
which every single factor of bone quality influences im-
plant treatment outcome has not been defined yet.34 Large
epidemiological studies will be necessary to investigate
this, and user-friendly software may facilitate the process.
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Reprint requests:
Rubelisa Cândido Gomes de Oliveira, DDS
School of Dentistry
Federal University of Goiás
Rua C-259, n 35, ap 801
Nova Suíça, Goiânia, GO
74280-220 Brazil
rubelisa@cultura.com.br