BON-09329; No.

of pages: 7; 4C:
Bone xxx (2011) xxx–xxx

Contents lists available at ScienceDirect

Bone
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / b o n e

A prospective study of mandibular trabecular bone to predict fracture incidence in

women: A low-cost screening tool in the dental clinic
Grethe Jonasson a, b,⁎, Valter Sundh c, 1, Margareta Ahlqwist d, Magnus Hakeberg b, e,
Cecilia Björkelund f, Lauren Lissner g
a
Research & Development Unit in Southern Alvsborg County, Sven Eriksonplatsen 4, SE-503 38 Borås, Sweden
b
Research Center, Public Dental Service, Region Västra Götaland, Göteborg, Sweden
c
Department of Public Health and Community Medicine, Institute of Medicine, University of Gothenburg, Gothenburg, Sweden
d
Department of Oral and Maxillofacial Radiology, Institute of Odontology at the Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
e
Department of Behavioral and Community Dentistry, Institute of Odontology at the Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
f
Primary Health Care Unit, Institute of Medicine, University of Gothenburg, Gothenburg, Sweden
g
Public Health Epidemiology Unit, Institute of Medicine, University of Gothenburg, Gothenburg, Sweden

a r t i c l e i n f o a b s t r a c t

Article history: Bone structure is the key to the understanding of fracture risk. The hypothesis tested in this prospective study
Received 7 April 2011 is that dense mandibular trabeculation predicts low fracture risk, whereas sparse trabeculation is predictive
Revised 7 June 2011 of high fracture risk. Out of 731 women from the Prospective Population Study of Women in Gothenburg
Accepted 27 June 2011
with dental examinations at baseline 1968, 222 had their first fracture in the follow-up period until 2006.
Available online xxxx
Mandibular trabeculation was defined as dense, mixed dense plus sparse, and sparse based on panoramic
Edited by Felicia Cosman radiographs from 1968 and/or 1980. Time to fracture was ascertained and used as the dependent variable in
three Cox proportional hazards regression analyses. The first analysis covered 12 years of follow-up with self-
Keywords: reported endpoints; the second covered 26 years of follow-up with hospital verified endpoints; and the third
Bone fracture combined the two follow-up periods, totaling 38 years. Mandibular trabeculation was the main independent
Mandible variable predicting incident fractures, with age, physical activity, alcohol consumption and body mass index
Osteoporosis as covariates. The Kaplan–Meier curve indicated a graded association between trabecular density and fracture
Population study risk. During the whole period covered, the hazard ratio of future fracture for sparse trabeculation compared to
Prospective
mixed trabeculation was 2.9 (95% CI: 2.2–3.8, p b 0.0001), and for dense versus mixed trabeculation was 0.21
Radiography
(95% CI: 0.1–0.4, p b 0.0001). The trabecular pattern was a highly significant predictor of future fracture risk.
Women
Our findings imply that dentists, using ordinary dental radiographs, can identify women at high risk for future
fractures at 38–54 years of age, often long before the first fracture occurs.
© 2011 Elsevier Inc. All rights reserved.

Introduction inactivity), medication predisposing to low bone mass, and conditions

Although osteoporosis is associated with a high fracture risk,
roughly 73% of all fractures occur in women who test negatively for
osteoporosis [1]. Bone mineral density (BMD) only partly explains
bone quality and fracture risk, and bone strength is also dependent on
variables such as geometry (bone shape and size) and microstructural
features (e.g., collagen fibres, crystal size) [2]. Clinical fracture risk
factors such as lifestyle (smoking, high alcohol consumption, physical
⁎ Corresponding author at: Research & Development Unit in Southern Alvsborg
County, Sven Eriksonplatsen 4, SE-503 38 Borås, Sweden. Fax: + 46 33 209870.
E-mail addresses: grethe.jonasson@vgregion.se (G. Jonasson),
valter.sundh@geriatrik.gu.se (V. Sundh), margareta.ahlqwist@gu.se (M. Ahlqwist),
magnus.hakeberg@odontologi.gu.se (M. Hakeberg), cecilia.bjorkelund@allmed.gu.se
(C. Björkelund), lauren.lissner@medfak.gu.se (L. Lissner).
1
Equal contributions.
increasing the risk of falls have been identified [3,4].
Bone structure is now considered the key to understanding frac-
ture risk [5]. Trabecular bone structure can be assessed by measuring
trabecular volume, spacing, and connectivity by computed tomogra-
phy and magnetic resonance [2]. Although progress has been made in
assessing trabecular bone structure, the cost and complexity of these
methods limit their utility for routine use.
However, trabecular bone structure can be visually evaluated in
plain dental radiographs. A large proportion of the population visits a
dentist on a regular basis every 1–2 years and dental radiographs have
been performed routinely [6]. The intra-oral and panoramic radio-
graphs provide information about the mandibular and maxillary bone
at low cost to the patient and without undue exposure to radiation.
Therefore, research teams throughout the world have tried to develop
methods for using the jawbones to predict skeletal BMD [7]. The
alveolar process of the mandible develops as a result of tooth eruption

8756-3282/$ – see front matter © 2011 Elsevier Inc. All rights reserved.
doi:10.1016/j.bone.2011.06.036

Please cite this article as: Jonasson G, et al, A prospective study of mandibular trabecular bone to predict fracture incidence in women: A low-
cost screening tool in the dental clinic, Bone (2011), doi:10.1016/j.bone.2011.06.036
2 G. Jonasson et al. / Bone xxx (2011) xxx–xxx
and elongation. It is subject to physiologic remodeling throughout life,
and can be influenced by masticatory demands, orthodontic move-
ments and may undergo more or less progressive resorption after
tooth extraction. The mandibular alveolar process undergoes the
same ageing processes as other bones [8], and the thickness of the
trabeculae, spacing between the trabeculae, and the trabecular con-
nectivity in the jaw are altered in patients with osteoporosis com-
pared to normal subjects [9].
A dense alveolar trabecular pattern in the mandibular alveolar
process is a reliable sign of normal BMD in dentate middle-aged
subjects, whereas a sparse trabecular pattern indicates osteopenia
[10–12]. We have previously found that mandibular sparse trabecula-
tion, evaluated visually using dental intra-oral radiographs in a small
study group, was associated with an increased likelihood of previous
fracture, and in this context performed better than BMD [13]. How-
ever, ascertainment of fracture was retrospective, i.e. we investigated
the association between current trabecular bone pattern and previous
fractures, not incident fractures [13]. In the current study our aim
was to test alveolar trabecular bone structure as a predictor of future,
incident, post-cranial bone fractures.
Materials and methods
Participants
The Prospective Population Study of Women in Gothenburg,
Sweden, is an ongoing longitudinal study of women initiated
in1968/69, in which medical and dental examinations have been
performed on multiple occasions until 2010. To ensure selection of a
representative sample of women in Gothenburg in 1968/69, women
were chosen randomly from the Revenue Office register, according to
their date of birth, on dates of the month divisible by six (five cohorts
born 1908, 1914, 1918, 1922, and 1930). Ninety percent of women
invited underwent a medical examination, 97% of whom also
participated in the dental part of the study, which corresponded to
an 87% participation rate [14]. At the second phase of the study in
1980/81, 73% of those who had taken part in the baseline study in
1968/69 participated [15]. A non-participation analysis was per-
formed in the 24 year follow-up, and the women who declined to
participate in the first study did not differ significantly from the
participants except for the long-term survival which showed to be
lower in the initial refusers [16].
The present report is based on 917 women born 1914, 1922 and
1930 and aged 54, 46 or 38 at baseline (from three of the original five
age-cohorts). The study was designed to study women before, during
and after menopause. Women born in 1908 and 1918 were not in-
cluded in this special study. A group of 151 women was only exam-
ined in 1968 and 28 of them were excluded because the panoramics
did not have a fully acceptable quality. Furthermore, 73 edentulous
women were excluded. Thus, of those with panoramic radiographs
taken in 1968/69, 816 had sufficient alveolar bone for evaluation of
trabecular pattern.
All women were invited for dental re-examinations in 1980/1981
and 579 women, including 76 new participants, had sufficient tra-
becular bone for inclusion. Seventy-three edentulous women from
the first examination had been excluded and six more women from
the second examination had to be excluded because they had too
little alveolar trabecular bone left for evaluation (Fig. 1). This is a
consequence of tooth extraction where resorption of the alveolar
trabecular bone starts at the extraction site [17]. In addition to medical
history data collected during the health examinations, verified frac-
ture data were obtained after 1980 from the hospitals and date of
death from the National Swedish Death Registry. Before 1980 registry
data from hospital care was not possible to obtain, and fractures were
ascertained by questionnaire only, as described in next section.
Please cite this article as: Jonasson G, et al, A prospective study of mandibular trabecular bone to predict fracture incidence in women: A low-
cost screening tool in the dental clinic, Bone (2011), doi:10.1016/j.bone.2011.06.036
The Ethics Committee of University of Gothenburg approved the
study (T 453-04 and T 075-09), and participants gave their informed
consent in accordance with the Helsinki Declaration.
Fracture ascertainment
Self-reported information on fractures was collected from the
1968/69, 1974/75, and the1980/81 questionnaires. Fifty-five percent
of the fractures were forearm fractures, 17% hip fractures, 14% clinical
spine fractures, and 14% upper-arm fractures. We had information
from a few women concerning the reason for self-reported fractures.
No fractures of fingers and toes were recorded, and no attempt to
separate fragility fractures from other fractures was made. Thirty-one
women had two fractures, twenty had three and 12 had more than
three fractures. Women who sustained fractures on more than one
occasion were included only with the first fracture. Women with a
fracture in childhood (b20 years old) were registered as not fractured.
Before the main analysis was performed, 85 women with self-
reported fractures were excluded (19 fracture cases from before 1968
and 66 undated fracture cases).
Women examined in 1968/69, with dated, self-reported, incident
fractures between 1968 and 1980 were included in the proportional
hazards regression analysis for the first period of 1968–1980. Sixty-
one of 731 women with sufficient trabecular bone 1968/69 reported
an incident fracture with a date during the period 1968–1980 (Fig. 1,
Table 1).
Västra Götaland County (VGR) (unification of Gothenburg and
three other counties) is the largest Health Care Organization in
Sweden, including 18 hospitals. Hospital-verified fracture data from
the whole region was available from the VGR Patient Register for the
period 1980–2006. Almost all “medical” radiography and all fracture
treatment are performed at the hospital. It means that very few
fracture cases were missed. Verified, incident fracture cases occurring
between 1980 and 2006 were used in the second regression analysis.
For the second analysis, all previous fracture cases were excluded
leaving 518 “fracture-free” women with panoramics from 1980/81 for
evaluation. They had a total of 136 dated and hospital-verified,
incident fractures from 1980 to 2006 (Fig. 1, Table 1).
The final, third analysis included 731 women, starting “fracture-
free” from baseline (1968) and experiencing 222 incident fractures.
Analysis 3 combines the two periods 1968–80 and 1980–2006. In the
first period we only have available self-reported fractures. In the
second period we only include hospital verified ones. These 2 groups
are mutually exclusive (Fig. 1).
The 61 fractures in analysis #1 and the 136 in analysis #2 do not
add up to the 222 in analysis # 3 because 25 of the dated fractures in
the final analysis were found in women who were not examined in
1980.
Ordinal classification of the radiographic mandibular alveolar trabecular
pattern
The panoramic radiographs have been performed at two different
time periods using different panoramic machines. The exposure
factors were set individually according to the size of the probands.
However, these small variations have no influence on the visual
evaluation of the trabecular pattern. The panoramic radiographs were
placed over a light-box in a darkened room, extraneous light was
masked, and magnifying lenses (*2) were used. Crestal bone around
teeth with marginal bone loss due to periodontitis and sclerotic bone
around apices of problematic teeth was disregarded in the evaluation.
With the help of three panoramic reference radiographs (Fig. 2 shows
intraoral radiographs which better visualize the trabeculation in a
journal) and a visual index proposed by Lindh et al. [18] and modified
by Jonasson et al. [10], the alveolar trabeculation was classified as
either sparse (value 1), mixed dense plus sparse (value 2), or dense
 G. Jonasson et al. / Bone xxx (2011) xxx–xxx 3

Participants Dental Exam1968

Analysis # 1
Included: 731 women Time to fracture: 1968-1980
Sample group without any previous 61 reported fractures
fracture
1968: 816 women with
1974: 19 reported fractures
trabecular bone structure Excluded :19 with 1980: 42 reported fractures
evaluation on radiographs fractures before1968

Excluded: 66 with
non-dated fractures

Participants Dental Exam1980

Included: 518 Analysis # 2

Sample group Time to fracture: 1980-2006
without fractures
136 verified fractures
1980: 579 women with
trabecular bone evaluation
(including 76 new women). Excluded: 61 with
fractures 1968-1980

Analysis # 3
Time to fracture: 1968-2006
222 fractures reported (1968-80)
or from hospital registries (1980-2006)

Fig. 1. Flow-chart showing number of women with sufficient trabecular bone, excluded fractures, self-reported and hospital-verified fractures. The first sustained fracture was used
i.e. only one fracture for each woman. Analysis #3 consisted of 731 women with 222 fractures from the period 1968 to 2006. Note that the total number of fractures in analysis #3
exceeds the numbers in parts #1 and 2 because of different analytic samples in the 2 follow-ups.

(value 3). When the trabecular pattern was evaluated as sparse, the Densitometric measurements
criterion was large intertrabecular spaces in most of the alveolar
process, especially in the cervical, dentate, premolar area. When the In order to validate the visual index used in this study, objective
trabecular pattern was evaluated as dense, the whole radiographed densitometric measurements in the premolar area of the panoramics
alveolar premolar area had small intertrabecular spaces. When the were performed in a subsample of 192 panoramics. The optical
trabecular pattern was assessed as mixed dense plus sparse, the density was measured with a densitometer (Macbeth TD-500 with an
trabeculation was mostly dense cervically and sparse apically [10]. aperture of ~ 2 mm, Macbeth Division of Kolmorgen Co., Newburgh,
The assessments were blinded for fracture status. N.Y., USA). The optical density is a measure of the darkening of the
exposed and processed radiograph. When the bone mass is reduced
Table 1 optical density increases. The optical density was assessed at a loca-
Trabeculation and incident fractures of “fracture-free” women examined 1968/69 and tion between the first and second premolar if possible or as close to
1980/81 with sufficient bone for evaluation of mandibular trabeculation and included that location as possible. The locations were positioned at least 3 mm
in the three Cox proportional hazards regression analyses.
apical to the crestal lamina dura, avoiding roots, lamina dura, and
Women included 1968/69 n (%) Incident fractures during 38 years apical area. The radiographs from 2005/06 and 1992/93 were chosen
Age 38–54 years because the quality was excellent and the processing procedures
Sparse group 1968 133 (18.2) 91 better controlled than 1968/69.
Mixed group 1968 371 (50.8) 114
Dense group 1968 227 (31.0) 17 Reproducibility
Total 731 222a,b

Women included 1980/81 Incident fractures during 26 years Three dentists, one experienced in classifying the trabecular
pattern in oral radiographs in earlier research (observer A), an
Sparse group 1980 143 (27.6) 85
Mixed group 1980 253 (48.8) 49 oral and maxillofacial radiologist (B), and one general practi-
Dense group 1980 122 (23.6) 2 tioner (C) from a department of oral and maxillofacial radiology,
Total 518 136b performed a study of the intra and inter-individual agreement
a
Self-reported, incident fractures. concerning the assessment of the pattern of the bone trabecula-
b
Hospital-verified, incident fractures. tion for panoramic radiographs using a test-retest evaluation. A

Please cite this article as: Jonasson G, et al, A prospective study of mandibular trabecular bone to predict fracture incidence in women: A low-
cost screening tool in the dental clinic, Bone (2011), doi:10.1016/j.bone.2011.06.036
4 G. Jonasson et al. / Bone xxx (2011) xxx–xxx

Fig. 2. Reference images presenting the trabecular pattern as dense trabeculation in a woman with small intertrabecular spaces (left), mixed dense plus sparse trabeculation in a
woman with small intertrabecular spaces cervically and larger spaces more apically (middle), and sparse trabeculation in a woman with large intertrabecular spaces (right). The
radiographs are intra-oral radiographs with better sharpness than panoramic radiographs; note that in the investigation we had only panoramic radiographs available.

total of 30 panoramics were evaluated twice 4 weeks apart by #3: dental examinations in 1968/69 and self-reported fractures
the three observers. 1968–1980 plus verified fractures 1980–2006 (Fig. 1, Tables 1 and 2).

Assessment of potential confounders
At each examination, all women answered questions concerning
smoking, physical activity, and alcohol consumption (all three discrete
numerical variables). Anthropometric measurements were taken
including height and weight. Descriptions of these procedures have
been published previously, including group means and prevalences
for these potential confounders in 1968/69 [19–21]. All hazard ratios
are adjusted for these variables, as described below. Another known
risk factor for future fracture is previous fracture, but we only used the
first fracture. Cortisone medication was noted in 2.4% of the women
(constant during the period), and none received other medication for
osteoporosis than calcium supplementation, which increased from 5%
to 20% during the period, whereas hormone replacement therapy
decreased from 22.8% to 13.6%.
Statistical analysis
The time from the 1968/69 baseline examination to first fracture
or censoring (until 2006) was calculated for each individual. Cox
proportional hazards regression was used to model the dependence of
time to fracture on the exposure (sparse, mixed sparse plus dense, and
dense trabecular pattern) and confounding factors for “fracture-free
survival” by censoring at date of death or at the end of 2006. Three
different proportional hazards regression analyses were performed
based on:
#1: dental examinations in 1968/69 and self-reported, dated fractures
1968–1980;
#2: dental examinations in 1980/81 and hospital-verified fractures
1980–2006;
In all Cox proportional hazards analyses, mixed dense plus sparse
trabeculation was used as a reference group because approximately
50% of the women had this mixed trabecular pattern. Time to fracture
was the dependent variable, and the independent variables were
trabeculation (categories 1 and 3, versus 2), age, smoking, physical
activity, drinking habits, and body mass index (BMI).
Kappa-statistics was used to calculate the intra and inter-
individual agreements. The statistical program SAS version 9.2 (SAS
Institute Inc., Cary, NC) was used.
Results
Radiographic mandibular alveolar trabecular pattern in 1968/69 and
1980/81
In 1968/69, sparse trabeculation was observed in 18.2% of the
women with sufficient trabecular bone for inclusion (Table 1). Twelve
years later, in 1980/81, a larger fraction, 27.6%, now had sparse tra-
beculation. Somewhat fewer had dense trabeculation in 1980/81
compared to 1968 (23.6% versus 31%). In 1980/81, the majority of
subjects were re-examined, new participants were added, and
previous fracture cases were excluded. The risk estimates, presented
in three parts below are all based on the same model including
trabeculation, age, and other potential confounders.
Results for 1968–1980
In the first analysis (Tables 1 and 2), only age and dense versus
mixed trabeculation significantly explained the risk time for self-
reported fracture. The hazard ratio was 0.39 (95% CI: 0.18–0.81,

Table 2
Hazard ratios for fracture risk calculated from Cox proportional regression analysis for those with dense trabeculation, mixed dense and sparse trabeculation, and sparse
trabeculation in three periods.

Dense Mixed Sparse

Analysis 1: 1968/1980
n = 731, cases 65a n = 227, cases = 9 n = 371, cases = 37 n = 133, cases = 19
Hazard ratio (95% CI) 0∙386 (0.184–0.807)* 1∙0 1∙453 (0.816–2.59)

Analysis 2: 1980/2006
n = 518; cases = 136b n = 122, cases = 2 n = 253, cases = 49 n = 143, cases = 85
Hazard ratio (95% CI) 0∙07 (0∙017–0∙ 292)*** 1∙0 3∙63 (2∙54–5∙18)****

Analysis 3: 1968/2006
n = 731, cases = 222a,b n = 227 cases = 17 n = 371, cases = 114 n = 133, cases = 91
Hazard ratio (95% CI) 0∙21 (0∙13–0∙36)**** 1∙0 2∙87 (2∙17–3∙80)****

*p b 0∙05, ***p b 0.001, ****p b 0∙ 0001.

Included variables in the model besides trabeculation: age, smoking, physical activity, drinking habits and body mass index.
a
Self-reported fractures.
b
Hospital-verified fractures.

Please cite this article as: Jonasson G, et al, A prospective study of mandibular trabecular bone to predict fracture incidence in women: A low-
cost screening tool in the dental clinic, Bone (2011), doi:10.1016/j.bone.2011.06.036
 G. Jonasson et al. / Bone xxx (2011) xxx–xxx 5

p = 0.0115) for those with dense trabeculation compared to those
with mixed trabeculation. Sparse versus mixed trabecular pattern was
not significant in this initial observation period .The hazard ratio for
age was 0.93 (95% CI: 0.89–0.97, p = 0.0005, Table 2) but the other
independent variables were not statistically significant.
Results for 1980–2006
In the second analysis, 518 women with 136 verified incident
fractures from 1980 to 2006 were included. Again, age and trabecular
pattern explained the risk time for fracture (Table 2). The hazard ratio
for a fracture of sparse trabeculation compared to mixed trabeculation
was 3.63 (95% CI: 2.54–5.18, p b 0.0001). Consistent with the first
observation period, we also observed a significant protective asso-
ciation for dense versus mixed trabeculation, with hazard ratio for
fracture of 0.07 (95% CI: 0.02–0.29, p = 0.0003, Table 2). The hazard
ratio for age was 0.92 (95% CI: 0.89–0.95, p b 0.0001).
Results for 1968–2006
Finally, in the third analysis including the same variables, 731
women with 222 reported and/or verified incident fractures were
included. Again, age and trabecular pattern explained the risk time
for fracture (Table 2). The hazard ratio for a fracture with sparse
trabeculation compared to mixed trabeculation was 2.87 (95% CI:
2.17–3.80, p b 0.0001), and 0.21 (95% CI: 0.13–0.36, p b 0.0001) for a
fracture of dense versus mixed trabeculation (Table 2). The Kaplan–
Meier curve for risk time for fracture during the combined obser-
vation period is shown in Fig. 3, where a graded effect of dense, mixed,
and sparse trabeculation is illustrated. The hazard ratio for age was
0.92 (95% CI: 0.90–0.94, p b 0.0001).
Densitometric measurements
Significant differences were found between the optical density of
radiographs from individuals with sparse trabeculation (1.78, 95% CI:
0.96–2.60), mixed trabeculation (1.42, 95% CI: 0.70–2.20), and dense
trabeculation (1.25, 95% CI: 0.60–1.80, p b 0.0001).
Reproducibility
Inter-observer agreement was at least good (Kappa: 0.73, 0.72,
and 0.84, Table 3) and so was intra-observer agreement (Kappa: 0.65,
0.76, and 0.92, Table 3).
Discussion
The results of the present investigation indicated that mandibular
trabeculation was a powerful predictor of fracture risk. The percent-
age of women with sparse trabeculation increased considerably with
age as did the fracture rate. The regression analyses, confirmed with
Kaplan–Meier survival curve, clearly show the protective effect of
dense trabeculation and the excess risk for sparse trabeculation.
Despite variations in bone mass and trabecular pattern in different
regions within a single mandible, it seems that mandibular trabecular
pattern in the premolar region is a useful predictor of post-cranial
fractures [13]. The hazard ratio for fracture with sparse trabeculation
relative to mixed trabeculation was highest in the second period from
1980 to 2006 compared to the first period (1968–1980). This can be
explained by the higher age of participants in the second period
compared to the first, or alternatively could be due to longer follow-
up time and better ascertainment of endpoints available after 1980.
The higher age in the second period implies that fractures were more

Fig. 3. Kaplan–Meier survival curve showing cumulative survival and risk time for fracture in three different trabeculation groups; 1: survival of women with sparse
trabeculation, 2: mixed trabeculation and 3: dense trabeculation. Risk time represents the time interval between baseline assessment and the fracture event. All 731
participants included, started “fracture-free” at baseline (1968) and experienced 222 first, incident fractures during the period 1968–2006.

Please cite this article as: Jonasson G, et al, A prospective study of mandibular trabecular bone to predict fracture incidence in women: A low-
cost screening tool in the dental clinic, Bone (2011), doi:10.1016/j.bone.2011.06.036
6 G. Jonasson et al. / Bone xxx (2011) xxx–xxx
Table 3
Kappa values for intra and inter-observer agreement for trabecular pattern.
Observer A Observer B Observer C
Observer A 0.92
Observer B 0.84 0.76
Observer C 0.73 0.72 0.65
likely osteoporotic than fractures at a younger age. In all three periods,
regression models consistently show significant protection in the
dense trabeculation group, regardless of whether endpoints are
reported or verified. It is likely that secondary causes of osteoporosis
may influence fracture rate, but in our investigation physical activity,
medication, alcohol consumption, or smoking were neither confounders
nor significant predictors.
A number of strengths and limitations of this study may be con-
sidered. The advantage of this study is the prospective design, the
relatively large, representative study population, and a high participa-
tion rate. Fractures were carefully checked from questionnaires and
hospitals and as far as we know it is the first longitudinal study using
mandibular trabecular pattern as a predictor of future fracture. The
limitations are mainly that panoramic radiographs are less sharp than
intra-oral radiographs and BMD measurements were not available.
Very few private medical practices in Sweden possess X-ray equipment
which means that nearly all fracture treatments require hospital
contact. The advantage of using a hospital register is that a precise
date is obtained, which is seldom the case when using questionnaires.
However, most studies involving osteoporotic fractures have similar
limitations since all persons who sustain a fracture do not automatically
have contact with health care, especially concerning vertebral osteopo-
rotic fractures. Further studies are needed using BMD measurement and
objective methods on intra-oral radiographs, in order to further clarify
whether mandibular trabecular pattern can perform as well or even
better than BMD measurements for fracture prediction.
Panoramic radiographs are not ideal for assessing trabecular
pattern; they cannot be taken at all dental clinics and fail to show
clearly the fine details of the trabeculation, compared to “ordinary”
dental intra-oral radiographs available at all dental clinics. How-
ever, they show approximately the same features as the intra-oral
radiographs [22]. The densitometric measurements were the only
objective method we could use on the trabecular bone. The objective
methods used previously in our research [11–13] were developed
using intra-oral radiographs. Similarly, advanced imaging techniques
[9,23–26], were not initially designed for trabecular bone in pano-
ramics though images of the mandibular ramus has been analyzed in
one study [26].
We have studied the degree of erosion of the inner endosteal
compact bone using Klemettis index [27,28], and the results are not
published yet. Due to the erosion of the endosteal compact bone we
found it difficult to measure accurately the thickness of the compact
bone on the panoramics of the oldest participants. Other researchers
have developed and validated an automated measurement of cortical
thickness concerning osteoporosis [29], and compared this automated
assessment together with clinical variables with the FRAX index
without BMD [30].
When comparing our results with other studies, we observe
that the rates of sparse trabeculation observed in 1968/69, when the
population was 38–54 years old, are similar to rates observed in more
recent studies [10–12]. Thus, although the baseline data are over
4 decades old, they may be relevant to contemporary middle-aged
female populations. Our results are supported by findings from cross-
sectional studies, using computed tomography, showing that im-
paired bone architecture is associated with fracture, partially inde-
pendent of BMD [31,32], and resistance to fracture depends not only
on the total amount of bone but also on the size and distribution of the
trabeculae [33]. The increased distances between adjacent trabeculae
Please cite this article as: Jonasson G, et al, A prospective study of mandibular trabecular bone to predict fracture incidence in women: A low-
cost screening tool in the dental clinic, Bone (2011), doi:10.1016/j.bone.2011.06.036
account for more than twice the age-related bone loss compared to
the decrease in trabecular width, and loss of connectivity has more
deleterious effect on bone strength than thin but well-connected
trabeculae [33].
We excluded cases with severely resorbed edentulous mandibles.
The main observation in the excluded edentulous material was that
the radiographic basal bone was mostly dense. Basal bone seems to
react differently to aging than alveolar bone. It is possible that severe
alveolar resorption is followed by a reinforcement of the remaining
trabecular structures in the basal bone in order to compensate for the
loss in vertical dimension. Our observation is supported by other
investigators [34–36]. Data from questionnaires in 2000 showed that
3–13% of the population was edentulous [37] and fewer have a
severely eroded alveolar process, especially in Sweden where im-
plants are rather common. Our findings are applicable in dentate
individuals and in partial edentulous individuals with well preserved
alveolar bone. The exclusion of non-dated fractures was due to the
selected methods: the Cox proportional hazards modeling and the
Kaplan–Meier survival curve. We were focused on future fractures
and time to fracture.
Previously mentioned prospective research demonstrated that
osteoporotic women have more fractures compared to women with
normal BMD [1], but that the osteoporotic group is small (14.5%) [1].
In fact, women without osteoporosis had 73% of fractures while only
27% occurred in women with osteoporosis [1]. Thus, our results may
make it possible to also identify non-osteoporotic women at future
risk and refer them to medical care. Our previous study showed that
mandibular trabecular pattern is a better correlate of fracture than
BMD, identifying 48% of all previous fractures compared to the 19%
identified using BMD [13].
Conclusions
The unique feature of the present study, compared with most
previous publications, is the long observation period and prospective
design. We found that the trabecular pattern was a highly significant
predictor of future fracture risk both in perimenopausal and in older
women: the older the individual, the more effective the mandibular
trabecular pattern as a fracture predictor. Given that 20% of 38–
54 year old women in this study had sparse trabeculation and sim-
ilar rates are seen today, a large fraction of the population could
potentially benefit from the knowledge that they are at risk. In
conclusion, our findings imply that dentists can use ordinary dental
radiographs as a rough tool to identify women at high risk for future
fractures in mid-life, often many years before the first fracture occurs.
Contributions
LL, CB and GJ designed the study; LL, CB, MA and MH are the
principal investigators of The Prospective Population Study of Women
in Gothenburg; GJ coordinated, and with MA collected the data. VS
and GJ performed the statistical analyses; GJ wrote the first draft of
the report; all authors interpreted the results, revised the text, and
approved the final text.
Funding
This study was funded by research grants from the Health & Medical
Care Committee of the Regional Executive Board, Region Western
Götaland, the Research and Development Councils of Southern Älvsborg
and Göteborg & Southern Bohuslän Counties, the Swedish Council for
Working Life and Social Research (FAS Center EpiLife), and the Swedish
Research Council.
 G. Jonasson et al. / Bone xxx (2011) xxx–xxx
Role of the funding source
The study sponsors had no role in the design, in the collection,
analysis, and interpretation of the data; or in the preparation, review,
or approval of the manuscript. The opinions, results, and conclusions
are those of the authors and all authors have full access to all data.
Conflicting interest
All authors declare no conflict of interest.
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