Prediction of Implant Loss and Marginal Bone Loss by

Analysis of Dental Panoramic Radiographs

Joe Merheb, DDS, MSc1/James Graham, PhD2/Wim Coucke, PhD3/Martin Roberts, MA, PhD4/
Marc Quirynen, DDS, MSc, PhD5/Reinhilde Jacobs, DDS, PhD, MSc, Dr hc6/Hugh Devlin, PhD, MSc, BDS7

Purpose: One of the major factors governing implant success is the quantity and density of the host bone. The
aim of this work was to determine whether mandibular bone texture and cortical width measurements on plain
radiographs could be associated with implant failure and/or marginal bone loss. Materials and Methods: A
statistical model was built to predict implant failure; it incorporated several radiographic features of cortical
and cancellous bone texture, cortical width, and patient smoking habits. Cortical width measurements and
texture measurements of cortical and cancellous bone were made on the panoramic radiographs of 460
subjects. These were used to predict implant failure and marginal bone loss after 5 years. Receiver operating
characteristic (ROC) curve analysis and area under the curve (AUC) were used to determine the diagnostic
accuracy of the variables in predicting implant failure and marginal bone loss. Additionally, for 91 of 460
subjects with periapical radiographs, marginal bone levels around implants were measured over a 5-year
period. Results: Of the 460 patients assessed for implant failure, 29 had failed implants (93.7% success
rate). The ROC curve built from this model had a sensitivity of 62.1% and specificity of 67.5%. The AUC
from the model was 0.690 (95% confidence interval [CI] 0.597 to 0.783). A model was also built to predict
marginal bone loss. The ROC curve had 78.6% sensitivity and 74.6% specificity (AUC = 0.880, 95% CI = 0.810
to 0.953). Mandibular cortical width was not a significant predictor of either implant failure or bone loss.
Conclusion: In a retrospective analysis 5 years after implant placement, features of cancellous and cortical
bone of the mandible were significant in predicting implant failure and marginal bone loss in a sample of 460
patients. Int J Oral Maxillofac Implants 2015;30:372–377. doi: 10.11607/jomi.3604

Key words: bone density, bone loss, cancellous bone, cortical bone, dental implants, failure, mandible

D ental implant therapy has evolved over the last

few decades into a safe and predictable therapy
with success rates above 95%.1 However, although the
1Consultant, Unit of Periodontology, Department of Oral Health
Sciences, University of Leuven, Belgium.
2Researcher, Centre for Imaging Science, Institute of Population
Health, Manchester Academic Health Sciences Centre, The
University of Manchester, Manchester, United Kingdom.
3Researcher, Quality Medical Laboratories, Scientific Institute
of Public Health, Brussels, Belgium.
4Reader, Centre for Imaging Science, Institute of Population
Health, Manchester Academic Health Sciences Centre, The
University of Manchester, Manchester, United Kingdom.
5Professor, Unit of Periodontology, Department of Oral Health
Sciences, University of Leuven, Belgium.
6 Professor, Oral Imaging Center, University of Leuven, Belgium.
7Professor, School of Dentistry, Institute of Population Health,
Manchester Academic Health Sciences Centre, the University
of Manchester, United Kingdom.
Correspondence to: Dr Joe Merheb, Unit of Periodontology,
Department of Oral Health Sciences, University of Leuven,
Kapucijnenvoer 33,3000 Leuven, Belgium.
Email: joe.merheb@med.kuleuven.be
©2015 by Quintessence Publishing Co Inc.
failure rate is low, retreatment is necessary after failure,
with resultant expense, disappointment, and inconve-
nience for patients.
Bone quality has been suggested as one of the main
factors influencing implant therapy success, and areas
of lesser bone quality have exhibited higher failure
rates2 and weaker primary stability.3 The anterior man-
dible often has a high bone density and a correspond-
ingly high success rate.4 An assessment of bone quality
prior to implant placement is recommended. However,
in practice, the dentist may have difficulty determin-
ing the preoperative quality of cancellous bone and
whether it is able to offer sufficient support for the
implant. Qualitative indices, such as the Lekholm and
Zarb index,5 have a variable interexaminer repeatabil-
ity, and the correlation with bone density assessed us-
ing quantitative cone beam computed tomography
(CT) shows wide variations.6,7
It was previously found that mandibular cortical
width, measured on panoramic radiographs, is sig-
nificantly correlated with bone density at other sites
throughout the body.8 It was also shown9 that radio-
graphic image texture in the cortex and in the basal
bone superior to the cortex can augment cortical

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width measurements as a predictor of a general dis-
position to bone loss in the skeleton. The hypothesis
here is that cortical width may be used together with
mandibular bone texture to predict implant failure
and bone loss around dental implants.
The aim of this study was to evaluate the predict-
ability of implant failure and alveolar bone loss around
implants based on the measurement of image fea-
tures from dental panoramic radiographs in the form
of cortical width and texture of the cancellous and
cortical bone.
MATERIALS AND METHODS
Screening
In this retrospective study, the dental records of 2,188
consecutive patients seeking implant treatment in the
mandible at University Hospital, Catholic University of
Leuven, were screened. Data from appointments be-
tween November 2002, when digital panoramic imag-
ing was introduced, and June 2008 were examined.
To meet the inclusion criteria, patients had to have
received implants in the mandible during this period
and were required to have received a panoramic radio-
graph within 6 months of implant placement (between
6 months before and 6 months after implant place-
ment). Radiographs were taken by qualified radiology
technicians according to the manufacturer’s instruc-
tions relative to patient positioning and appropriate
device settings. Inclusion in the study also required
that the inferior alveolar nerve canal was not too close
(eg, within eight pixels) to the inferior mandibular cor-
tex to allow trabecular bone analysis.
The screening resulted in the selection of 460 pa-
tients who met the inclusion criteria (174 men, 286
women; mean age at implant placement 65.3 years;
range, 18 to 87 years). Their data were used for bone
quality assessment in relation to implant failure. To
measure marginal bone loss around the implants, the
selected sample was filtered further; periapical radio-
graphs of the peri-implant bone, of adequate quality,
taken at insertion and after 5 years had to be available.
For this analysis, the sample was narrowed to 91 pa-
tient files. The remaining 369 patients were excluded
from the second part of the study because they lacked
sufficient periapical radiographs for evaluation and fol-
low-up of marginal bone loss. The implants included
in the study belonged to one of three systems (Astra
Tech, Nobel Biocare, Straumann) and had either ma-
chined or modified surfaces.
Implant Loss
The dental records of the recruited patients were exam-
ined and the success of implant placement assessed.
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Merheb et al
R
M D
X
Fig 1  Reference lines for measurement of marginal bone
loss around implants. R = reference line (implant shoulder);
X = implant diameter; M = mesial measurement; D = distal
measurement.
The patients’ files were examined for any mention of
implant failures caused by biologic failure. Implants
were not included in the study if they had failed for
biomechanical reasons (eg, occlusal overload, poor
surgical technique, postoperative infection). The
search revealed that 29 of the 460 patients had lost at
least one implant as a result of biologic failure. An im-
plant was recorded as lost when it had to be removed.
Marginal Bone Changes
Marginal bone loss was measured on digital periapi-
cal radiographs using Photoshop (CS3, Adobe Sys-
tems) and up to ×8.0 magnification. Marginal bone
levels were assessed at the mesial and distal surfaces
of each implant. The abutment-implant connection
point of the assessed implant was used as a reference
point (Fig 1). Then, the bone level was measured from
the reference point to the most coronal marginal bone
mesial and distal to the implant. Calibration using the
known width of the implants allowed measurements
to be converted from pixels to millimeters. Pathologic
bone loss was defined using the criteria of Albrektsson
et al,10 namely, a measured loss greater than 1 mm dur-
ing the first year of service and a subsequent threshold
of 0.2 mm per year. Bone loss was analyzed in the pres-
ent study at 60 months. Periodontal bone measure-
ments were available after 60 months for 91 implants.
Texture and Cortical Width Measurements
Image measurements on panoramic radiographs have
previously been described in the context of detection
of osteoporosis.8,11 An algorithm for cortical width
measurement was reported by Allen et al12 and refined
by Roberts et al.13 Measurement of image texture in
cancellous and cortical bone was similarly optimized
in the context of detection of osteoporosis9 using fea-
tures derived from grey-level co-occurrence matrices.14
The International Journal of Oral & Maxillofacial Implants 373
Merheb et al
This method is described briefly here. A co-occurrence
matrix is a two-dimensional histogram that shows the
frequency of occurrence of pairs of grey values of pix-
els separated by a specific pixel distance in a specified
direction. Entries to the histogram are accumulated
from all such pixel pairs in the region of interest. Typi-
cally, several such matrices are built to correspond to a
range of pixel separations and directions. This method
is described briefly in Appendix 1, which also defines
the texture measures used in this study; the reader is
referred to Haralick et al14 or to a number of secondary
sources (eg, Tucervan and Jain15 and Petrou and Garcia
Sevila16) for a complete description and a definition of
the texture features.
Roberts et al9 evaluated 13 of these features for their
effectiveness in identifying bone loss in the context
of osteoporosis. In cortical bone, these features were
derived from histograms calculated with pixel separa-
tions of 2, 3, 4, 5, and 6 in the direction perpendicu-
lar to the superior cortical border. In cancellous bone,
pixel separations of 2 and 4 pixels were used in four di-
rections: perpendicular and parallel to the direction of
the cortical border and in the two diagonal directions
between these. The same features were evaluated here
as potential predictors of bone loss around implants
and implant failure. These features were derived, in the
case of cancellous bone, from the regions bilaterally
between the mental foramen and the gonial angle,
and between the superior cortex and the mandibular
canal. This region provided an area with minimal over-
lay of other structures. The measurement area in the
cortex was defined by the superior and inferior bound-
aries of the inferior mandibular cortex, located by the
automated software12,13 between the mental foramen
and antegonion. The width of the inferior mandibular
cortex was measured at a point near antegonion on
each side of the radiograph, as described in Allen et
al.12 The cortical widths were the average value of the
measurements from both sides of the mandible.
Statistical Analysis
A linear model was built to classify outcomes of im-
plant failure and bone loss at 5 years after implant
placement. The model was constructed using the
complete set of features via stepwise variable selec-
tion. Linear models were built using all data, and for
some experiments, the data were split into training
and validation sets. In constructing the model, a num-
ber of features were found to be strongly correlated
with each other. In the trabecular bone, for example,
it is unlikely that image textures will show strong di-
rectional properties; this leads to strong correlations
between the texture features measured in different di-
rections. Likewise, some features may be similar at dif-
ferent pixel separations. When the correlating features
374 Volume 30, Number 2, 2015
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represented the same statistical property of the co-oc-
currence matrix but at different orientations or scales,
the features were averaged. Where correlations were
found between different co-occurrence matrix mea-
sures, only one was retained in the model. Correlations
were assessed by means of a biplot based on a factor
analysis. In addition to cortical width and 35 texture
features, smoking status was included in the model, so
that 37 variables were available for the stepwise selec-
tion procedure. Measures from the left and right sides
of the mandible were averaged. Each texture feature
can be determined at a specific pixel separation and
orientation. The definitions of these specific features
are found in Haralick et al.14
Because there is a danger of “overtraining” when
validating a model that is then validated on the same
dataset, a validation-training experiment was done.
Therefore, a model was developed using half of the
data, and this model was subsequently tested on the
remaining data. The training-validation experiment
was repeated and randomized. Because there were
few failed implants in comparison to the number of
successful implants, this model was only tested for
bone loss analysis.
RESULTS
Implant Loss
Of the 460 patients assessed, 29 of them had man-
dibular implants that had failed (93.7% success rate)
after 5 years. The mean mandibular cortical width of
the patients with successful implants was 3.04 mm
(standard deviation [SD] = 0.51) and that of those with
failed implants was 3.21 mm (SD = 0.50). There was a
small but nonsignificant difference between the mean
of the two groups (95% confidence interval [CI], –0.61
to –0.02).
Table 1 lists those variables that predicted implant
loss over 5 years of the study. On a receiver operating
characteristic (ROC) curve built from this model, the
point of quasiequality of sensitivity and specificity was
62.1% sensitivity and 67.5% specificity. The area un-
der the curve (AUC) from the model was 0.69 (95% CI,
0.60 to 0.78). Whether the patient smoked was not a
significant predictor of implant loss in the model, but
smoking did show an odds ratio of 2.24 for implant loss
versus those who did not smoke.
Bone Loss Around Implants
Table 2 lists those variables in the general linear model
from the trabecular and cortical analysis that signifi-
cantly predicted bone loss around the implants after
5 years. Whether the patient smoked also significantly
predicted pathologic bone loss around the implants
 Merheb et al

Table 1  Variables in Trabecular and Cortical Bone Predicting Implant Failure After 5 Years
Variable Pixel separation Orientation* P value
Cancellous variance 4 0123 .0001
Cancellous angular second moment 4 0 .0001
Cancellous difference entropy 4 123 .0053
Cortical angular second moment 4 1 .0001
Cortical inverse difference moment 4 1 .0001
Cancellous sum entropy 4 0123 .0475
*0 = parallel to the upper border of the mandibular cortex; 1 = perpendicular to this border; 2,3 = diagonal directions between 0 and 1;
0123 = average of measures at all four orientations; 123 = average of orientations other than that tangential to the cortical border.

Table 2  Variables in Trabecular and Cortical Bone Predicting Pathologic Bone Loss
Around Implants After 5 Years
Variable Pixel separation Orientation* P value
Smoking status – – .0017
Cortical sum entropy 2 1 .0001
Cortical sum entropy 3 1 .0001
Cortical sum average 4 1 .0053
*0 = parallel to the upper border of the mandibular cortex; 1 = perpendicular to the upper border of the mandibular cortex.

(P = .0017). For this model, the point of quasiequality of
sensitivity and specificity on the ROC curve was 78.6%
sensitivity and 74.6% specificity (AUC = 0.88; 95% CI,
0.81 to 0.95). This model successfully predicted 20 of
the 28 cases with pathologic peri-implant bone loss
(sensitivity = 71.4%) and 56 of the 63 cases with no
pathologic bone loss (specificity = 88.9%). Mandibular
cortical width was not a significant predictor variable
of bone loss.
The validation-training experiment showed that the
model developed from half the data and tested on the
remainder gave an AUC of 0.67 (95% CI, 0.51 to 0.83).
DISCUSSION
Implants tend to fail more frequently in areas of poor
bone quality because they depend on the surround-
ing bone for support and retention.17 It can be difficult
for the implant surgeon to determine noninvasively
whether there is sufficient bone quality in the man-
dible prior to implant placement and thereby offer a
realistic treatment prognosis for the patient. Lettry et
al18 found a weak correlation between the mechanical
properties of fresh mandibular bone and CT Hounsfield
numbers, but this was insufficient to accurately predict
the mechanical properties in an individual given the
variability in this relationship. Some authors recom-
mend cone beam CT to assess bone volume prior to
implant placement, as these machines are optimized
for imaging of hard tissue,19 but the low contrast reso-
lution of the technique may limit the ability to distin-
guish between tissue types.
The use of textural features based on co-occurrence
matrices for assessment of bone quality has been re-
ported previously. Kolacinski et al20 used the entropy
measure as a quantitative texture feature in intraoral
radiographs for assessing bone healing following sur-
gery. Dudek21 and Kozakiewicz et al22 used a different
co-occurrence matrix feature—sum of squares of vari-
ance—to assess damage to bone in response to dif-
ferent implant designs. Interestingly, the same feature
arose from the present analysis as one of the predictors
of bone loss around implants in panoramic radiographs.
In this study, the patients selected had panoramic
radiographs taken immediately before or after implant
placement. Although the aim of the study was to deter-
mine the predictive value of panoramic radiographs, it
was hypothesized that cancellous and cortical bone
features would not vary significantly over such a short
period of time. The algorithm was not optimized to
distinguish between failed and successful implants,
but numerous textural features of the mandibular can-
cellous bone were significantly predictive of implant
failure, indicating that cancellous bone plays a major
role in resisting the functional loading exerted by the
implant. The same conclusion was reached using fi-
nite element analysis models of implants placed in the
mandible.23 Experiments using high-resolution mag-
netic resonance imaging have shown that the trabecu-
lae are preferentially oriented in the long axis of the
tooth24 and therefore functionally adapted to resist oc-
clusal loads. Cortical and cancellous bone quality influ-
ences the primary stability of implants and therefore
the success of treatment,25 and the textural features
of both were important in predicting implant success.

The International Journal of Oral & Maxillofacial Implants 375

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Merheb et al

failure, but a combination of cortical texture measures

i
and cancellous texture measures produces a signifi-
cant area under the curve in the receiving operator
characteristic analysis.
d
j Pd (i, j)

ACKNOWLEDGMENTS

Increment element (i, j) The authors reported no conflicts of interest related to this study.
Grey level j
Grey level i

Fig 2  Formation of the grey-level co-occurrence matrix. For APPENDIX 1:

each pixel in the region of image under consideration, its grey CO-OCCURRENCE MATRIX FEATURES
level (i) and the grey level (j) of a pixel separated from it by the
vector d constitute a co-occurring pair, and the matrix element
Pd(i,j) is incremented. When all pixels have been considered, the Let the digital image be quantized to G grey levels. The grey level
matrix represents a two-dimensional histogram of co-occurring co-occurrence matrix Pd is a G × G matrix in which the entry
grey levels. Pd(i,j) represents the frequency of occurrence of a particular pair
of grey levels, i and j, in pixels separated by a vector d (see
Fig 2). After the matrix is normalized to ensure that the sum of all
The current authors showed that cancellous bone fea- entries is 1.0, each entry can be regarded as the probability of
tures, mean cortical width, and cortical texture clas- observing each pair of grey levels. To keep the dimension of the
matrix within practical limits for calculation, the grey level quan-
sifiers are, together, important in predicting implant
tization range is usually reduced. In this case, G = 32 was used.
success, but cortical width is of limited significance as Although the matrix captures textural properties, it is not it-
a lone predictive factor. Previous studies have shown self a convenient representation for analysis. A number of sum-
a significant correlation between osteoporosis and mary statistics can be calculated from the matrix, reported in
the width of the mandibular cortex.8,11,26 The present Haralick et al14 and further summarized in Tucervan and Jain15
and Petrou and Garcia Sevila16 among others. The features that
results are compatible with recent clinical trials that
predict implant failure (Table 2) are defined as follows:
failed to find a correlation between skeletal osteopo-
rosis and implant failure.27,28 Angular second moment (sometimes referred to as energy):
The analysis in this study was disadvantaged by the
G G
much smaller number of patients with failed implants Pd 2 ( i, j )
than successful implants. Most studies have observed i=1 j=1
Sum of squares of variance:
an implant failure rate of less than 10%, irrespective of
G G
the technique and implant system used. For example, (i j )Pd (i, j )
Bain and Moy29 found an overall implant failure rate of i=1 j=1
Inverse difference moment:
5.92%. More recently, Le et al30 found a similar failure
rate for short implants. G G
1
2 Pd ( i, j )
Many other clinical factors can influence implant i=1 j=1 1+ ( i j )
success, and these were difficult to measure and con- Sum average:
trol in the present analysis (eg, surgical expertise, dy- 2G

namic occlusion, bruxism). This was unavoidable given IPx+y (i )

i=2
the retrospective nature of the project. In addition, the Sum entropy:
small number of implant failures in the study popula- 2G

tion meant that the CIs for the diagnostic ability (AUC Px+y (i)log Px+y (i)
{ }
i=2
in ROC analysis) were large. Difference entropy:
G 1
Px y (i)log Px y (i)
{ }
CONCLUSION where
i=0

G G

In a retrospective study, co-occurrence matrix (accord- Px+y ( k ) = d P (i, j ), k = 2, 3,…, 2G

i=1 j=1
, the probability
ing to Haralick et al14) features of the cancellous and i+ j=k

of co-occurrence matrix coordinates summing to x+y and

cortical bone of the mandible had a significant asso- G G
ciation with implant failure in a sample of patients. Px y (k ) = d P (i, j ), k = 0,1,…,G 1
Bone loss around implants seems to be best associated i=1 j=1
i j =k

with features of the cortical bone. The cortical width the probability that the difference between co-occurrence matrix
did not have a significant relationship with implant coordinates is x-y.

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