Original and review articles
© Schattauer 2012
The OsteoLaus Cohort Study
Bone mineral density, micro-architecture score and vertebral fracture assessment extracted from a single DXA
device in combination with clinical risk factors improve
significantly the identification of women at high risk of
fracture
O. Lamy1,2; M.-A. Krieg1; D. Stoll1; B. Aubry-Rozier1,3; M. Metzger1; D. Hans1*
1Centre
for Bone Diseases, Lausanne University Hospital, Lausanne, Switzerland; 2Service of internal medicine, Lausanne University Hospital, Lausanne, Switzerland; 3Service of Rheumatology, Lausanne University Hospital, Lausanne,
Switzerland; *for the OsteoLaus Study
Keywords
Trabecular Bone Score (TBS), bone mineral
density, vertebral fracture assessment, DXA
device, osteoporosis
Summary
Indirect micro-architectural (MA) approximation is evaluable in daily practice by the
Trabecular Bone Score (TBS) measure. The aim
of the OsteoLaus cohort is to combine CRF
and the information given by DXA (bone mineral density [BMD], TBS and vertebral fracture
assessment [VFA]) to better identify women
at high fracture risk. We included 631 women:
mean age 67.4 ± 6.7 y, BMI 26.1 ± 4.6. Correlation between BMD and site matched TBS
was low (r2 = 0.16). Prevalence of vertebral
fractures (VFx) grade 2/3, major OP Fx and all
OP Fx was 8.4 %, 17.0 % and 26.0 % respectively. Age- and BMI-adjusted ORs (per SD decrease) were 1.8 (1.2–2.5), 1.6 (1.2–2.1), 1.3
(1.1–1.6) for BMD and 2.0 (1.4–3.0), 1.9
(1.4–2.5), 1.4 (1.1–1.7) for TBS respectively.
Correspondence to
Dr. Olivier Lamy, PD & MER
Centre for Bone Diseases
Lausanne University Hospital (CHUV) – DAL
Avenue Pierre Decker 4
CH-1011 Lausanne, Switzerland
E-Mail: [email protected]
Introduction
Osteoporosis (OP) is a systemic skeletal
disease characterized by a low bone mineral
density (BMD) and a micro-architectural
The TBS ORs (per SD decrease) adjusted for age,
BMI and spine BMD for VFx grade 2/3, major
and all OP Fx were 1.7 (1.1–2.7),1.6 (1.2–2.2)
and 1.3 (1.0–1.7) respectively. Only 35 to 44 %
of women with OP Fx had a BMD < –2.5 SD or
a TBS < 1.200. If we combine a BMD < –2.5 SD
or a TBS < 1.200, 54 to 60 % of women with an
OP Fx are identified. Therefore by using VFA,
BMD, and TBS from a simple and low ionizing
radiation device, the DXA, we can obtain additional informations which are useful for the patient in the daily practice.
Die OsteoLaus-Kohortenstudie – Die Kombination
aus Knochenmineraldichte, MikroarchitekturScore und Wirbelfrakturerkennung, abgeleitet aus
einer einzelnen DXA-Aufnahme, und klinischen
Risikofaktoren verbessert deutlich die Identifizierung von Frauen mit hohem Frakturrisiko
Osteology 2012; 21: 77–82
received: April 23, 2012
accepted after revision: May 29, 2012
lich. Das Ziel der OsteoLaus-Kohorte besteht
darin, klinische Risikofaktoren und Informationen aus der DXA (Knochenmineraldichte
[BMD], TBS und Wirbelkörperfrakturerkennung [VFA]) zu kombinieren, um Frauen mit
hohem Frakturrisiko leichter zu erkennen. Wir
nahmen 631 Frauen im mittleren Alter von
67,4 ± 6,7 J. und mit einem BMI von 26,1 ± 4,6
auf. Es bestand eine schwache Korrelation
zwischen BMD und Zentrums-gematchtem
TBS (r² = 0,16). Die Prävalenz von Wirbelfrakturen (VFx) Grad 2/3, größeren osteoporotischen (OP) Frakturen und allen OP-Frakturen
betrug 8,4 %, 17,0 % bzw. 26,0 %. Alters- und
BMI-adjustierte OR (nach abnehmender SD)
lagen bei 1,8 (1,2–2,5), 1,6 (1,2–2,1) bzw. 1,3
(1,1–1,6) für BMD und 2,0 (1,4–3,0), 1,9
(1,4–2,5) bzw. 1,4 (1,1–1,7) für TBS. Die TBS OR
(nach abnehmender SD), adjustiert nach Alter,
BMI und Wirbelsäulen-BMD, für VFx Grad 2/3,
größere und alle OP-Frakturen betrugen 1,7
(1,1–2,7), 1,6 (1,2–2,2) bzw. 1,3 (1,0–1,7). Nur
35 bis 44 % der Frauen mit OP-Frakturen
hatten eine BMD < –2,5 SD oder einen
TBS < 1.200. Durch Kombination eines
BMD < –2,5 SD oder TBS < 1,200 werden 54
bis 60 % der Frauen mit OP-Fraktur erkannt.
Somit können wir anhand von VFA, BMD und
TBS aus einem einfachen und strahlenarmen
Röntgenverfahren, der DXA, Zusatzinformationen gewinnen, die für den Patienten im
Praxisalltag von Nutzen sind.
(MA) deterioration, with a consequent increase in bone fragility and susceptibility to
fracture. The gold standard for the diagnosis of osteoporosis is measurement of
BMD by dual X-Ray absorptiometry
(DXA). However, more than 50 % of osteoporotic fractures occur in individuals
whose DXA T-score is higher than the cutoff of –2.5 SD (1). It is accepted that defining osteoporosis on the sole basis of BMD
Schlüsselwörter
TBS-Wert (Trabecular Bone Score), Knochenmineraldichte, VFA (Vertebral Fracture Assessment), DXA-Gerät, Osteoporose
Zusammenfassung
Eine indirekte Beurteilung der Mikroarchitektur
(MA) ist in der täglichen Praxis anhand des TBS
(Trabecular Bone Score) näherungsweise mög-
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77
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O. Lamy et al.: The OsteoLaus Cohort Study
reached its limit. Indeed, the multifactorial
aspect of this disease encourages more
complex risk model based on both Clinical
Risk Factor (CRF) and BMD (2). Taking
into account epidemiological data and the
impact of these CRF on the 10-year absolute probability of fracture, the FRAX®
model was developed (3). The goal of this
model is a better definition of patients at
high risk for fracture, and by that making
them candidates for treatment. However,
FRAX® has several recognized limitations
(4–6).
Some CRF are interpreted as an indirect
MA approximation. Therefore, any more
direct additional information about MA
would probably help to distinguish patients
with and without fracture having the same
BMD (7). Clearly, developing a novel technique for the efficient, non-invasive clinical
evaluation of bone MA remains both crucial and challenging. MA is indirectly and
easily evaluable by the Trabecular Bone
Score (TBS) measure without additional
ionizing radiation. TBS is a novel grey-level
texture measurement that is based on the
use of experimental variograms of 2D projection images (8, 9). It is able to differentiate between two different micro-architectures that exhibit the same bone density,
but different trabecular characteristics
(씰Fig. 1). TBS measures the mean rate of
local variation of grey levels in 2D projection images. TBS cannot be considered as a
direct physical measure but rather as a bone
textural index strongly correlated to bone
microarchitecture (8–10). The TBS is obtained after re-analysis of a DXA exam, and
gives added value to the site matched BMD.
An elevated TBS reflects strong, fractureresistant MA; a low TBS reflects weak, fracture-prone MA. TBS is very simple to obtain, by reanalyzing a lumbar DXA-scan.
TBS is correlated with bone MA parameters: trabecular spacing (r = 0.63–0.65),
trabecular number (r = 0.73–0.76), connectivity density (r = 0.79–0.83) and SMI
(r = –0.6) (9–10). More importantly, previous studies have documented the value of
the trabecular bone score (TBS) in diagnosis and prognosis value, independently
of CRF and BMD (11–14).
Vertebral fractures (VFx) are one of the
most severe fractures in osteoporosis with a
very high morbidity and mortality (15, 16).
However, their clinical diagnosis is low because VFx are asymptomatic in 60–70 % of
cases (17) and their prognostic relevance is
not taken into account in the FRAX® model
(3). Recent generations of DXA systems
provide not only accurate and reproducible
measurements of BMD, but also the opportunity to use high-quality DXA scans in
place of standard X-rays to confirm and
characterize existing vertebral fractures. So
we are yet able to have additional information useful for the patient in the daily practice: VFA, BMD, and TBS from a simple,
low ionizing radiation and inexpensive device: DXA.
As seen previously, the definition of osteoporosis is evolving into a modern definition of fracture risk, including clinical risk
factors and parameters of bone measures.
However these tools are poorly validated in
daily routine and require ideally long term
prospective follow up. It is therefore important to have a cohort with a maximum tool
and clinical outcomes. The OsteoLaus
study is a population-based study with a
sample of approximately 1400 women, extensively phenotyped and genotyped, 50 to
80 years old. All these women have in particular a DXA with BMD, VFA and MA
evaluation. The global aim of our study is
to compare transversally and then prospectively (10 years follow-up) different models
to predict the fracture risk and to see how
information on MA could enhance either
model or explain the differences between
these models. Preliminary results of the
transversal phase are reported in this paper.
Method
Colaus Study (18)
Fig. 1 The principle of trabecular Bone Score with two examples (patients with the same BMD)
Colaus is an abbreviation for “Cohort Lausanne”. Briefly, recruitment took place in the
city of Lausanne in Switzerland, a town of
117,161 inhabitants, of which 79,420 are of a
Swiss Nationality. The complete list of the
Lausanne inhabitants aged 35–75 years
(n = 56,694 in 2003) was provided by the
population register of the city and served to
sample the participants to the study. All sub-
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O. Lamy et al.: The OsteoLaus Cohort Study
jects living in the city of Lausanne in 2003 for
more than 90 days have their name included
in this register. Of the initial 19,830 subjects
sampled, finally 6,188 men and women
agreed to participate and were eligible for all
the parts of the Colaus Study (an extensive
phenotyped and genotyped characterization). The aim of the Colaus Study is to assess the prevalence of cardiovascular risk
factors (CVRFs) in the Caucasian population of Lausanne and to determine new
genetic determinants associated with
CVRFs. In addition, sub-studies were designed to assess other aspects of this population and were nested onto this study. The
Colaus study is designed to be followed for
more than 10 years.
Table 1
OsteoLaus. Patient’s
characteristics at
baseline (preliminary
results for the first
631 patients); BMI:
body mass index; Fx:
fracture; OP: osteoporotic; SD: standard
deviation; Major OP
Fx = vertebral, hip,
shoulder, wrist
Lumbar spine
Bone mineral
density
Patients (n)
631
Age ± SD
Trabecular
bone score
67.4 ± 6.7
26.1 ± 4.6
2)
BMI (kg/m
BMD/TBS mean ± SD
0.943 ± 0.168
BMD T-score (mean)
–1.4
–
Correlation BMD – TBS (r2)
0.16
Vertebral Fx (grade 2/ 3)
8.4 %
Adjusted ORgr2/3 (for age and BMI)/SD
1.8 (1.2–2.5)
Major OP Fx (grade 2/3)
1.271 ± 0.103
2.0 (1.4–3.0)
17.0 %
Adjusted ORgr2/3 (for age and BMI)/SD
1.6 (1.2–2.1)
1.9 (1.4–2.5)
26.0 %
All OP Fx (grade 2/3)
ORgr2/3 adjusted for age and BMI
1.3 (1.1–1.6)
1.40 (1.1–1.7)
OsteoLaus (19)
OsteoLaus is a sub-study of Colaus which
started five years later. OsteoLaus was proposed to all women 50–80 years old who
participated at the second Colaus visit
between September 2009 and September
2012. At this time, near 85 % of the women
(seen at the second visit in Colaus, with five
years follow-up) accepted to participate in
the OsteoLaus Study. We expected to include
1400 women. Results for the first 631 included women are given below. The Study
was approved by the Institutional Ethic's
Committee of the University of Lausanne.
Major exclusion’s criteria are the following:
1. any disease known to affect bone metabolism,
2. drugs taken by the subjects known to
have a negative or a positive effect on
bone metabolism and
3. a BMI less than 16 and above 40.
At baseline, each patient would have:
1. a questionnaire about their potential
clinical risk factors of fracture/osteoporosis (including Swiss FRAX® assessment), and about any conditions which
could have an effect on bone metabolism,
2. one spine (L1 to L4) and one femur
measurements using the Discovery A
System (Hologic, USA),
3. one heel measurement using the
Achilles Insight System (GE Healthcare
Lunar, USA),
Fig. 2
Covariate adjusted
area under the curve
(AUC) from ROC
statistics for lumbar
spine BMD, TBS and
TBS adjusted for
BMD
4. a blind (from prevalent clinical conditions) central processing of TBS (TBS
iNsight v1.9, medimaps, France) based
on a previously acquired AP spine DXA
scan, and
5. one VFx assessment using the semiquantitative approach of HK. Genant (20).
The global aims of our study are:
1. to compare retrospectively different
models to predict the fracture risk and
to see how information on MA could
enhance either model or explain the differences between these models,
2. to assess the relationship between osteoporosis and cardiovascular diseases. We
then hope to follow this cohort for ten
years.
Descriptive analysis included means and
percentages with standard deviations (SD).
Percentage change in BMD at each site and
in TBS was calculated for each subject as
the absolute change over the duration of
follow-up divided by the baseline value.
Pearson correlation coefficients were calculated comparing site-specific BMD and
TBS. Odds ratios (OR) were calculated to
estimate the risk of a prevalent fracture,
using age and BMI-adjusted logistic regression. Age- and BMI adjusted Area under the
Receiver operator characteristic (AUC)
values were calculated.
Finally, women were categorized into
two groups according to the WHO classification: non osteoporotic and osteoporotic
and stratified above and below 1.200
threshold of TBS. Chi2 test were used to
compare fracture incidence below and
above the BMD/TBS thresholds. For all inferential tests, the threshold for statistical
significance was set at p < 0.05, and all tests
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79
80
O. Lamy et al.: The OsteoLaus Cohort Study
Sensitivity Specificity
Single models
Combined
models
FRAX® All fracture
(Swiss threshold ([age])
23.8 %
92.4 %
FRAX® All fracture
(20 % threshold)
28.6 %
93.4 %
BMI 20 threshold
4.8 %
93.9 %
Spine BMD
(–2.5 T-score threshold)
33.3 %
74.1 %
Spine TBS (–1.200
threshold)
42.9 %
74.6 %
Spine BMD or TBS
thresholds
59.5 %
59.2 %
Spine BMD or FRAX®
thresholds (age)
45.2 %
70.4 %
Spine TBS or FRAX®
thresholds (age)
52.4 %
70.9 %
Spine TBS or BMD or
FRAX® thresholds (age)
66.7 %
56.2 %
were two-tailed. Statistica (Version 8.0,
StatSoft, Inc., Tulsa, OK, USA) was used for
all statistical analyses.
Results
The characteristics of the 631 women are
given in 씰Table 1. The Age- and BMIadjusted ORs (per each BMD SD decrease)
were 1.8 (1.2–2.5) for VFx grade 2/3, 1.6
(1.2–2.1) for major OP fractures, and 1.3
(1.1–1.6) for all OP fractures. The age- and
BMI-adjusted ORs (per each TBS SD
decrease) were 2.0 (1.4–3.0), 1.9 (1.4–2.5),
1.4 (1.1–1.7) respectively, for each type of
fractures. The age- and BMI-adjusted AUC
for lumbar spine BMD, TBS and TBS adjusted for BMD was between 0.61 and 0.68,
lower for all OP fractures and higher for
VFx grade 2/3 and major OP fractures
(씰Fig. 2). The AUC for the TBS adjusted
for age, BMI and BMD remained significant for all the categories of fracture. The
TBS ORs (per each SD decrease) adjusted
for age, BMI and spine BMD for VFx grade
2/3, major and all OP Fx were 1.7
(1.1–2.7),1.6 (1.2–2.2) and 1.3 (1.0–1.7) respectively.
Using a triage approach, only 35 to 44 %
of women with one type of OP fractures
had a BMD < –2.5 SD or a TBS < 1.200. If
Table 2
Comparison between
single versus combined models in regard to sensitivity
and specificity using
the vertebral fracture
sub group
we combine a BMD < –2.5 SD and a TBS <
1.200, 54 to 60 % of women with an osteoporotic Fx are identified (Chi2 trend were
all significant). The Comparison between
single versus combined models in regards
to sensitivity and specificity using the vertebral fracture sub group can be found in
씰Table 2. TBS as a stand-alone approach
displayed a sensitivity of 42.9 % and specificity of 74.6 % versus 33.3 % and 74.1 %
Conclusion
In agreement with published studies, these
preliminary results confirm:
1. the partial independence between BMD
and TBS, demonstrating that TBS is
measuring different bone entities, and
2. and that a combination of BMD and TBS
increases significantly the identification
of women with prevalent OP fractures.
We therefore are able to have complementary information about fracture (VFA), BMD
and TBS with a simple, low ionising radiation
and an inexpensive device: DXA. The combination of TBS and FRAX® would be worth to
be further evaluated. As most fractures occur
in women with osteopenia, identifying individuals most likely to fracture can facilitate
more efficient utilization of health care resources.
for Spine BMD respectively while the
FRAX® outcome was in the range of 23.8
and 92.4 % respectively. The combination
of TBS and FRAX® seems to be the best
comprise in sensitivity (52.4 %/specificity
(70.9 %).
Discussion
These preliminary results of our cohort
study confirm the very low correlation between lumbar spine BMD and TBS
(r2 = 0.16). TBS predicts vertebral, major
and all OP fracture equally well than spine
BMD and thus independently of age and
BMD. This prediction ability remained significant even after adjustment for spine
BMD confirming that TBS measures other
bone characteristics than density. TBS is
meant to fulfil the “micro-architectural”
part of the current definition of osteoporosis. We have tested the complementarity of
BMD and TBS in a 2 step triage approach.
Such approach demonstrated the significant added value of TBS in addition to
bone mineral density for the identification
of patients at higher risk of fracture. Moreover the global combination of TBS and
FRAX® (BMD) improves the sensitivity
(52 % versus 33 to 43 % for BMD or TBS
alone), while maintaining an appropriate
level of specificity. Such interesting findings on combining FRAX® and TBS have
never been reported before. However, the
optimum model and threshold has yet to be
further investigated.
It is interesting and reassuring to see that
we obtain the same results in another Swiss
cohort study (Osteo-Mobile, preliminary
results based on 510 women) analysed independently (21). This added value of TBS
has been further documented in cross-sectional, prospective and longitudinal studies
(11–14, 21–35). Indeed, TBS has been
found:
1. to be lower in post-menopausal women
with a past osteoporotic fracture compared with age- and BMD-matched
women without fracture (11),
2. to give an incremental increase in the
odds ratio for spine fracture when combined with spine BMD (12, 21–25),
3. to be lower in women with fractures
compared with women without frac-
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O. Lamy et al.: The OsteoLaus Cohort Study
tures, irrespective of whether their BMD
met the criteria for osteoporosis or
osteopenia (13, 21–25),
4. to prospectively predict fracture as well
as spine BMD (14, 26, 27),
5. to recapture around 1/3 of the patients
who were miss-classified according to
the BMD WHO definition of osteoporosis alone (21–27), and
6. to be responsive to treatment therapy
(28–32).
In the large Manitoba study including
29,407 women > 50 years old and followed
for 4.7 years, TBS was demonstrated to improve the OP fracture identification in a
sequential approach to risk reclassification
using BMD followed by TBS (14). Out of
321 (19 %) major osteoporotic fractures in
women with normal lumbar spine BMD,
93 (30 %) occurred in the lowest TBS tertile, and 203 (63 %) in the lowest two tertiles. In addition, 635 (38 %) major osteoporotic fractures were identified in patients
who had lumbar spine BMD in the osteopenic range, among whom 272 (43 %) had
TBS in the lowest tertile and 501 (79 %) in
the lowest two tertiles. Only 899 of 7,157
(12.6 %) of women with lumbar spine
BMD in the osteoporotic range had TBS in
the highest tertile and only 51 of 712
(7.2 %) of the fracture subjects had TBS in
the highest tertile. TBS would have correctly reclassified 43 % of the fracture subjects found in the osteopenic BMD range
(vs. 30.5 % of non-fractured subjects) and
29 % in the normal BMD range (vs. 20.2 %
of non-fractured subjects). Overall, 365
(38 %) fracture subjects misclassified by
lumbar spine BMD as non-osteoporotic
according to the WHO definition were in
the lowest TBS tertile suggesting poor
microarchitecture. Such results were consistent with our findings and particularly
interesting since we have used the same
TBS lowest threshold at 1.200. This threshold may not be optimal but seems to come
out consistently throughout reported
studies (33).
The risk of fracture is multi-factorial.
Many CRF are independent or partially independent of the BMD to predict the fracture risk. Moreover, BMD does not capture
the 3D micro-architecture of bone tissue,
which constitutes an important additional
factor of bone strength. TBS is a promising
factor to identify patients at high risk of
fracture. What will be in the future the
place of TBS in a model of risk prediction?
Will it be used in addition to the CRF and
BMD as included in the FRAX®, or in place
of some CRF (34)? The TBS seems to be
particularly low (in comparison with
BMD) in some conditions like rheumatoid
arthritis (36), treatment with glucocorticoids (37) or aromatase inhibitors (32). In
the future, a new model, including (eventually) TBS and certainly the identification
of asymptomatic vertebral fractures, will be
necessary to better identify women at high
risk of fracture. We hope that OsteoLaus
will give some answers in testing transversally and prospectively different models.
Acknowledgment
Sincere thanks are due to Prof Peter Vollenweider, Gerard Waeber, and Martin Preisig,
for the access to the CoLaus database.
Thanks go also to the Lausanne University
hospital for their financial support.
Conflict of interest
Didier Hans is co-owner of the TBS patent and has corresponding ownership
shares. The corresponding author ensures
that none of the other authors has any
conflicts of interest.
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Osteologie 2/2012
© Schattauer 2012
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For personal or educational use only. No other uses without permission. All rights reserved.