Osteoporos Int (2014) 25:243–249
DOI 10.1007/s00198-013-2502-7
ORIGINAL ARTICLE
Added value of trabecular bone score over bone mineral
density for identification of vertebral fractures in patients
with areal bone mineral density in the non-osteoporotic range
K. Nassar & S. Paternotte & S. Kolta & J. Fechtenbaum &
C. Roux & K. Briot
Received: 6 May 2013 / Accepted: 3 September 2013 / Published online: 1 October 2013
# International Osteoporosis Foundation and National Osteoporosis Foundation 2013
Abstract
Summary Detection of patients with vertebral fracture is sim-
ilar for areal bone mineral density (aBMD) and trabecular
bone score (TBS) in patients with non-vertebral fracture. In
non-osteoporotic patients, TBS adds information to lumbar
spine aBMD and is related to an index of spine deterioration.
Introduction Vertebral fractures (VFs) are more predictive of
future fracture than aBMD. The number and severity of VFs
are related to microarchitecture deterioration. TBS has been
shown to be related to microarchitecture. The study aimed at
evaluating TBS in the prediction of the presence and severity
of VFs.
Methods Patients were selected from a Fracture Liaison
Service (FLS): aBMD and vertebral fracture assessment
(VFA) were assessed after the fracture, using dual-energy X-
ray-absorptiometry (DXA). VFs were classified using Genant's
semiquantitative method and severity, using the spinal defor-
mity index (SDI). TBS was obtained after analysis of DXA
scans. Performance of TBS and aBMD was assessed using
areas under the curves (AUCs).
Results A total of 362 patients (77.3 % women; mean age 74.3±
11.7 years) were analysed. Prevalence of VFs was 36.7 %, and
189 patients (52.2 %) were osteoporotic. Performance of TBS
was similar to lumbar spine (LS) aBMD and hip aBMD for the
identification of patients with VFs. In the population with aBMD
in the non-osteoporotic range (n =173), AUC of TBS for the
discrimination of VFs was higher than the AUC of LS aBMD
(0.670 vs 0.541, p =0.035) but not of hip aBMD; there was
a negative correlation between TBS and SDI (r =−0.31;
p <0.0001).
K. Nassar : S. Paternotte : S. Kolta : J. Fechtenbaum : C. Roux :
K. Briot (*)
Rheumatology Department, Cochin Hospital, Paris Descartes
University, Paris, France
e-mail: karine.briot@cch.aphp.fr
Conclusion Detection of patients with vertebral fracture is
similar for aBMD and TBS in patients with non-vertebral
fracture. In patients with aBMD in the non-osteoporotic range,
TBS adds information to lumbar spine aBMD alone and is
related to an index of spine deterioration.
Keywords Bone mineral density . Fracture . Osteoporosis .
TBS
Introduction
Osteoporosis is a skeletal disorder characterized by compromised
bone strength leading to an increased risk of fracture
[1]. Whereas low areal bone mineral density (aBMD) is
among the strongest risk factors for fracture, studies
have shown that up to one half of patients with fragility
fractures have aBMD above the diagnostic threshold of
osteoporosis, i.e. T-score ≤ −2.5 [2–6]. Among post-
menopausal women having risk factors for osteoporosis,
but with T-scores higher than the −2.5 threshold, 20 %
already have vertebral fractures [7]. Vertebral fractures are
the hallmark of bone fragility [8] and are more predictive of
future fracture than aBMD; moreover, the risk of subsequent
fractures increases with the number and the severity of prior
vertebral fractures [9–11]. There is a link between severity of
vertebral fractures and alterations of bone microarchitecture
assessed at the iliac crest [12].
Assessment of patients with vertebral fractures (VF) is
challenging; most of them do not come to clinical attention
[13–15]. Use of conventional radiology is unattractive on the
ground of costs and radiation exposure. Vertebral fracture as-
sessment (VFA) is a radiographic method using dual-energy X-
ray-absorptiometry (DXA) to diagnose vertebral fractures, val-
idated for reproducibility, sensitivity and specificity as compared
244
with spine radiographs, with low radiation exposure [16–19].
However, not all DXA machines are equipped with VFA
software, and coverage of VFA has not been embraced by
health insurance in all countries. Thus, there is a need in
clinical setting for a tool able to predict the presence of
vertebral fracture and to indicate appropriately spine imaging
in selected patients.
The trabecular bone score (TBS) is a bone texture analysis
derived from the DXA image of the lumbar spine [20]. The
ex vivo studies conducted on bone specimens (vertebrae,
radius and femoral neck) show that TBS positively correlates
with 3D bone microarchitecture parameters, such as connec-
tivity, density and trabecular number, and negatively with
trabecular separation [21–24]. In vivo, this texture parameter
analyses the grey-level variations in DXA images, in the same
bone region as in lumbar spine aBMD. In clinical practice,
lower TBS scores indicate greater fracture susceptibility.
Cross-sectional studies showed that TBS was lower in post-
menopausal women with previous fragility fracture compared
to those without fracture [25] and was lower in women with
fractures irrespective of whether their bone mineral density
(BMD) met the criteria for osteoporosis or osteopenia
[26, 27]. Two retrospective historical cohort studies showed
that lumbar spine TBS and aBMD predicted major fractures
similarly; and that the combination of lumbar spine TBS and
aBMD improves fracture risk prediction in women with
aBMD in the non-osteoporotic range [27, 28]. We have shown
previously in patients with rheumatoid arthritis that TBS has a
better discrimination than lumbar spine aBMD for prediction
of the presence of vertebral fractures [29].
Thus, the purpose of our study was to evaluate the value of
TBS, alone or added to aBMD, in the prediction of the
presence and severity of vertebral fractures in a cohort of
patients included in a Fracture Liaison Service.
Patients and methods
Patient selection
Patients were selected from the Fracture Liaison Service
(FLS) of Cochin Hospital. This FLS was established to pro-
vide routine assessment for osteoporosis to all men and wom-
en over the age of 50 years who had sustained a low-trauma
non-vertebral fracture and are hospitalized in the orthopaedic
surgery department. Low-trauma fractures are defined as those
sustained in falls from standing height or less. Exclusion
criteria are pathological and traumatic fractures, outpatients
and severe impaired cognitive functions.
A senior physician, dedicated to the task of identifying
patients with fragility fractures, selects these patients in the
orthopaedic surgery department and prescribes DXA scanning
and VFA.
Osteoporos Int (2014) 25:243–249
Clinical assessment includes demographic data: age,
height, weight, BMI (body mass index) (in kilogram per
square metre), when standing position is possible, and infor-
mation on anti-osteoporotic treatment in the previous year.
BMD and VFA assessment
These measurements are performed 4–90 days after the
hospitalization for fracture. aBMD (in gram per square
centimetre) is assessed by DXA (Hologic®, QDR 4500A,
software version 12.6; Bedford, MA) at the lumbar spine
(L2–L4) and hip (total hip and femoral neck). The small
detectable difference (SDD) for the device was 0.034, 0.036
and 0.027 g/cm2 for the lumbar spine, femoral neck and total
hip, respectively [30]. The quality control protocol for the
DXA device includes daily scanning of a phantom.
A single device was used for the whole current study. The
World Health Organization (WHO) classification was used to
define osteoporosis as T-score≤−2.5 at the lumbar spine, total
hip or femoral neck. Vertebral fractures from T4 to L4 were
evaluated using VFA software on the DXA device. They were
classified with the Genant semiquantitative approach [31].
Patients with at least one grade 1 fracture were considered as
fractured. Spinal deformity index (SDI), an assessment tool
for vertebral fracture prediction [10, 32] was calculated by
summing the grade of each fractured vertebra from T4 to L4;
the SDI value can vary between 0 (no fracture) and 39 (all the
assessed vertebrae are grade 3). The diagnosis was directly
assessed on the screen, by one single reader (JF), an expert in
this field.
TBS
TBS (TBS iNsight® Software version 1.8, Med-Imaps,
Pessac, France) was obtained after reanalysis of DXA lumbar
spine (L2–L4) scans. The study was conducted independently
of the manufacturer. The software uses the AP spine raw
image(s) from the densitometer, including the aBMD region
of interest (ROI) and edge detection, so that the TBS calcula-
tion is performed over exactly the same ROI as the aBMD
measurement. For each region of measurement, TBS was
evaluated based upon grey-level analysis of the DXA images
as the slope at the origin of the log-log representation of the
experimental variogram. TBS (L2–L4) was calculated as the
mean value of the individual measurements for vertebrae L2–
L4. A BMI between 15 and 35 kg/m2 is mandatory for TBS
analysis, according to the manufacturer.
Statistical analysis
Characteristics of patients with hip fractures and non-vertebral
non-hip fractures and with and without vertebral fractures
were compared by using chi-square tests or Fisher's exact
Osteoporos Int (2014) 25:243–249
tests, or t tests as appropriate. The discriminative values of
aBMD at all sites, TBS (L2–L4) and their combination for the
presence of vertebral fracture was assessed by determining the
area under the receiving operator characteristic (ROC) curve
(area under the curve, AUC). All the analysis was performed
on SAS 9.1® statistical software.
Results
Patient characteristics
Five hundred and twenty-eight patients were recruited in the
FLS between February 2009 and October 2012. VFA was not
performed in 113 patients for technical reasons (including
inability to raise the upper arm for lateral view of VFA
measurement because of humerus and other upper arm frac-
tures); TBS was not measured in 115 patients because of the
inability to assess height and/or weight (and thus BMI which
is requested for TBS calculation) at the time of the DXA scan.
Thus, 362 patients are the basis of the study (77.3 % women;
mean age 74.3±11.7 years) (Table 1). One hundred and
eighty-six (51.4 %) patients had hip fractures, and 176
(48.6 %) had a non-vertebral non-hip fracture, located at
the humerus (n =25 (14.2 %)), pelvis (n =16 (9.3 %)), wrist
(n =85 (49.4 %)) and other sites (n =50 (28.4 %)). For 296 of
them, the non-vertebral fracture was a major fracture
(hip, wrist, humerus) according to the FRAX®. Their char-
acteristics are shown in Table 1. One hundred and eighty-nine
(52.2 %) patients had aBMD in the osteoporotic range
(T≤−2.5 at least one the three sites); 110 (30.4 %) patients
received calcium and/or vitamin D, and 49 (13.5 %) reported
receiving an anti-osteoporotic treatment in the year before the
fracture. Prevalence of vertebral fractures by VFA was 36.7 %
Table 1 Characteristics of the population (n =362)
Variables
Age (years) (mean ± SD) 74.3±11.7
Female (n, %) 280 (77.3 %)
History of low trauma fracture N (%) 112 (31.4 %)
BMI (kg/m2) (mean ± SD) 23.5±4.3
Lumbar spine T-score (mean ± SD) −1.48±1.69
Femoral neck T-score (mean ± SD) −2.30±1.03
Total hip T-score (mean ± SD) −1.79±1.13
Osteoporosis (T≤−2.5 at least one site) (n, %) 189 (52.2 %)
≥1 Vertebral fracture (n, %) 133 (36.7 %)
Number of vertebral fracture (mean ± SD) 0.6±1.1
Spinal deformity index (SDI) (mean ± SD) 1.1±2.2
Lumbar spine TBS (mean ± SD) 1.201±0.113
245
(n =133); the mean number of vertebral fractures was 1.7±
1.2. The characteristics of patients according to the presence
of vertebral fractures were in Table 2.
Half of our population recruited in the FLS had hip frac-
ture. Compared to patients with non-hip non-vertebral
fractures, patients with hip fracture were older (77.3±10.9 vs
71.3±11.7 years, p ≤0.0001), had frequently more vertebral
fractures (44.5 vs 28.9 %, p =0.002) and osteoporosis
(T≤−2.5 at least one the three sites) (62.6 vs 41.7 %,
p ≤0.0001). They had lower femoral neck and hip aBMD than
patients without hip fractures (0.580±0.11 vs 0.639±0.12 g/cm2
and 0.600±0.15 vs 0.769±0.15 g/cm2, p <0.0001).
TBS
TBS was weakly correlated with lumbar spine (r =0.51) and
total hip (r =0.34) aBMD. TBS was lower in patients with
vertebral fractures than in patients without vertebral fractures
(1.156±0.108 vs 1.227±0.107, p <0.0001). Mean values of
TBS were 1.159±0.115 and 1.153±0.099 in patients with one
VF and at least two VFs, respectively.
Vertebral fracture discrimination using TBS
In the whole population, AUC of TBS (0.677) was similar to
AUC of lumbar spine (LS) aBMD (0.669, p =0.80) and hip
aBMD AUC (0.692, p =0.68) (Fig. 1) for the presence of VF.
Combination of TBS and LS aBMD (AUC=0.707) improved
VF discrimination as compared to LS aBMD alone (p =0.043)
but not to hip aBMD alone (p =0.327). Combination of TBS
and hip aBMD (AUC=0.713) did not improve VF discrimi-
nation as compared to LS aBMD alone (p =0.088) and to hip
aBMD alone (p =0.327). Results were similar in patients with
major fracture according to the FRAX®.
Negative predictive value for vertebral fracture discrimina-
tion was 0.76, 0.79, 0.81, 0.84 and 0.82 for LS aBMD, hip
aBMD, TBS, combination of TBS with LS aBMD and com-
bination of TBS with hip aBMD, respectively. Positive pre-
dictive value was 0.43, 0.41, 0.46, 0.47 and 0.42 for LS
aBMD, hip aBMD, TBS, combination of TBS with LS
aBMD and combination of TBS with hip aBMD, respectively.
TBS according to the severity of vertebral fractures
Among patients with vertebral fractures, 57 (42.9 %), 47
(35.3 %) and 29 (21.8 %) had only grade 1 fracture, at least
one grade 2 (without grade 3) and at least one grade 3 fracture.
Thus, in our cohort of patients older than 50 years with a
recent non-traumatic fracture, 21 % (n =76) have moderate
and/or severe vertebral fractures. There was no statistically
significant difference of TBS among these three subgroups:
1.168±0.115 in only grade 1 group, 1.154±0.104 in patients
246 Osteoporos Int (2014) 25:243–249

Table 2 Characteristics of pa-

tients according to the presence of Vertebral fractures No vertebral fractures p value
vertebral fractures
N (%) 133 229
Age (years) (mean ± SD) 80.2 (±10.4) 71.0 (±11.1) <0.0001
Female (n, %) 104 (78.2 %) 176 (76.9 %) 0.769
Parents with hip fracture (n, %) 81 (60.9 %) 101 (44.1 %) 0.002
Lumbar spine T-score (mean ± SD) −2.1±1.7 −1.2±1.6 <0.0001
Femoral neck T-score (mean ± SD) −2.7±1.1 −2.1±1.0 <0.0001
Total hip T-score (mean ± SD) −2.3±1.1 −1.5±1.0 <0.0001
Osteoporosis (T≤−2.5 at least one site) (n, %) 95 (71.4 %) 94 (41.1 %) <0.0001
Lumbar spine TBS (mean ± SD) 1.157±0.108 1.227±0.107 <0.0001

with at least one grade 2, and 1.139±0.104 in patients with at
least one grade 3.
There was a negative correlation between SDI and TBS
(r =−0.31 (p <0.0001)), hip aBMD (−0.32 (p <0.0001)) and
LS aBMD (r =−0.30 (p <0.0001)). TBS was not correlated
with SDI after adjustment for age, hip aBMD and lumbar
spine aBMD.
Seventy-six patients had at least one grade 2 VF. The AUC
for discrimination of these patients as compared to the others
(n =286 having no VF or only grade 1 VFs) were 0.665,
0.679, 0.661, 0.712 and 683 for TBS, LS aBMD, hip
aBMD, TBS + LS aBMD, and TBS + hip aBMD. In this
situation, AUC of TBS for the discrimination of VFs was
similar to LS aBMD (0.665 vs 0.679, p =0.712) and to hip
aBMD (0.665 vs 0.661 p =0.953). Combination of TBS and
LS aBMD or hip aBMD to improve discrimination of patients
having at least one grade 2 VF was not significant (p =0.095
and 0.433, respectively) as compared to these parameters
alone. Results were similar in patients for whom the non-
vertebral fracture was a major fracture according to the
FRAX®.
TBS in patients with aBMD in the non-osteoporotic range
In patients with aBMD in the non-osteoporotic range (n =173)
(T>−2.5 at all sites), TBS was significantly lower in patients
with vertebral fractures than in patients without VF (1.187±
0.121 vs 1.253±0.104, p =0.001). AUC of TBS for the dis-
crimination of VFs was higher than the AUC of LS aBMD
(0.671 vs 0.541, p =0.035) but not of hip aBMD (0.670 vs
0.585, p =0.264) (Figs. 2 and 3). TBS was negatively corre-
lated to SDI (r =−0.25 (p =0.001)). In these patients, LS
aBMD and hip aBMD were not correlated with SDI (−0.07
(p =0.360) and −0.04 (p =0.618), respectively).
In patients for whom the non-vertebral fracture was a major
fracture according to the FRAX® (n =132), TBS was signif-
icantly lower in patients with vertebral fractures than in pa-
tients without VF (1.194±0.112 vs 1.264±0.092, p =0.001).
AUC of TBS for the discrimination of VFs was similar to
LS aBMD (0.697 vs 0.545, p =0.303) and to hip aBMD
(0.697 vs 0.588, p =0.264). TBS was negatively correlated to
SDI (r =−0.29 (p =0.001)). In these patients with aBMD in the
non-osteoporotic range, LS aBMD and hip aBMD were not

Fig. 1 Discriminative value of ROC curves in the whole population

TBS alone and in combination 1
with LS and hip aBMD in the 0.9
whole population
0.8
0.7
Sensitivity

0.6
0.5
0.4
0.3
0.2
0.1
0
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1
1 - Specificity

TBS LS BMD Hip BMD TBS + LS BMD TBS + Hip BMD

Osteoporos Int (2014) 25:243–249 247

Fig. 2 Discriminative value of ROC curves in the patients with aBMD in the non osteoporotic range
TBS alone and in combination 1
with LS and hip aBMD in patients
with aBMD in the non- 0.9
osteoporotic range 0.8
0.7

Sensitivity
0.6
0.5
0.4
0.3
0.2
0.1
0
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1
1 - Specificity
TB LS Hip TBS + LS TBS + Hip

correlated with SDI (−0.08 (p =0.344) and −0.06 (p =0.491), subjects with hip fractures, explaining the higher prevalence
respectively). of VFs found in our study as compared to other studies [33]. In
these patients with hip fractures, VFs influence functional
outcomes [34], illustrating the relevance of the identification
Discussion of patients with prevalent vertebral fracture.
Our study confirms previous data showing that TBS had an
This study conducted in a population of patients recruited in a additive value for the discrimination of patients with vertebral
Fracture Liaison Service shows that TBS improves the pre- fracture when combined with lumbar spine aBMD [24–26]. In
diction of the presence of VFs as compared to lumbar spine patients with rheumatoid arthritis (RA), TBS measured at the
aBMD alone, but not to hip aBMD. The same result is lumbar spine has a better discrimination value than lumbar
observed in patients with aBMD in the non-osteoporotic spine aBMD for the prediction of the presence of vertebral
range. However, in this population, TBS is correlated to the fractures. In RA patients with osteopenia, the proportion of
severity of the vertebral fractures, whereas lumbar spine and patients with vertebral fracture was higher in the lowest tertile
hip aBMDs are not. of TBS when compared with the highest tertile [29]. In wom-
Almost 40 % of our patients having a recent non-traumatic en older than 50 years of the Manitoba study (n =29 407,
non-vertebral fracture had at least one vertebral fracture, mean follow-up of 4.7 years) (10.7 % of major fractures
confirming the high prevalence of these VFs not previously excluding clinical vertebral fractures), TBS and LS aBMD
diagnosed in this population [33]. Prevalence of VFs differs predicted similarly incident fragility fractures (including clin-
according to the site of non-vertebral fracture; it is higher in ical vertebral fractures), and the combination was superior to
either measurement alone [27]. In the OFELY cohort (17 %
TBS values (mean)
with prevalent fracture), the assessment of TBS in 560 post-
1.24 menopausal women predicted incident fractures (including
1.22 clinical vertebral fractures), as well as LS aBMD, but the
1.2 combination of TBS and LS aBMD added only limited infor-
1.18
mation in the whole population [28]. In our study on patients
*
1.16
with non-vertebral fractures and in the other studies with a
lower prevalence of non-vertebral fractures, TBS is superior to
1.14
LS aBMD for the identification of vertebral fractures.
1.12
However, in clinical practice, measurement of aBMD at
1.1
two sites including the hip is recommended; our data show
1.08
No VF At least one Grade 1 Grade 2 Grade 3 that TBS does not add information when the hip aBMD is
(n=229) VF (n=133) (n=57) (n=47) (n=29) available.
Fig. 3 TBS values according to the vertebral fractures status. The aster- Identification of subjects with aBMD in the non-osteoporotic
isk indicates that TBS value of patients with at least one VF was lower
range at high risk of fractures is a relevant objective. The
than the TBS value of patients without VF (p ≤0.05). TBS was not
statistically significant among patients with only grade 1, patients with OFELY study showed that the combination of normal and
at least one grade 2 and patients with at least one grade 3 osteopenic T-scores with the lowest range of TBS improved
248
the identification of a significant proportion of women with
aBMD in the non-osteoporotic range with incident fragility
fracture [28]. In our study on patients with aBMD in the non-
osteoporotic range, TBS added information to LS aBMD for the
detection of patients with VFs, but not to hip aBMD. This
discrepancy among two studies may be related to the difference
in clinical fragility, as all our patients already had a non-vertebral
fracture. These results were not confirmed if we performed the
analysis in patients with major non-vertebral fractures (hip,
wrist, humerus).
Detection of patients with VF is not enough for optimal
management, as relevant outcomes (such as risk for subsequent
fractures and mortality) are related not only to the presence but
also to the severity of the vertebral fractures, i.e. their number
and grades [9, 10, 32]. TBS did not add information in this
matter in our population of patients with fracture. However,
correlation between TBS and the number and severity of ver-
tebral fractures assessed by the SDI was significant in patients
with aBMD in the non-osteoporotic range; we did not find such
a correlation with lumbar spine aBMD and hip a BMD. These
results were confirmed for patients with major non-vertebral
fractures according to the FRAX®. This suggests that in pa-
tients with aBMD in the non-osteoporotic range and peripheral
fracture, TBS could reflect the vertebral deterioration, more
than aBMD does. Using transiliac biopsies and measurement
of bone microarchitecture across different grades of VF sever-
ity, Genant et al. showed that vertebral fracture severity is
associated with progressive deterioration of cancellous and
cortical microarchitecture, and that the assessment of VF se-
verity is a surrogate of the microarchitecture status indepen-
dently of age and lumbar spine BMD [10]. We did not test the
predictive value of FRAX® in our population for several
reasons. FRAX® has not been proposed for the prediction of
the risk of radiographic vertebral fractures. Moreover FRAX®
is used to calculate the risk of fracture and is not useful in the
patients who have just made a recent fracture and who are thus
at high immediate risk [35]. In this population, it is the severity
(presence of vertebral fractures) assessment which is important.
The main limitation of our study is the fracture severity of
the population; half of the patients had hip fractures, and these
results have been obtained in a population of patients with a
recent fragility fracture. Our results cannot be applied to a
population with less severe cases, especially patients without
fracture.
This study is the first study which shows a relationship
between TBS and severity of VFs using VFA. Detection of
patients with vertebral fracture is similar for aBMD and TBS
in patients with non-vertebral fracture. In patients with aBMD
in the non-osteoporotic range, TBS adds information to lum-
bar spine aBMD alone (not to hip aBMD) and is related to an
index of spine deterioration.
Conflicts of interest None.
Osteoporos Int (2014) 25:243–249
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