Full text of DOI:10.1359/jbmr.2002.17.9.1629

JOURNAL OF BONE AND MINERAL RESEARCH
Volume 17, Number 9, 2002
©
2002 American Society for Bone and Mineral Research
Radius Bone Strength in Bending, Compression, and
Falling and Its Correlation With Clinical Densitometry
at Multiple Sites
1
,2
3,4
1,5
3
¨
EVA-MARIA LOCHMULLER, CHRISTOPH A. LILL, VOLKER KUHN, ERICH SCHNEIDER,
5
and FELIX ECKSTEIN
ABSTRACT
This study comprehensively analyzes the ability of site-specific and nonsite-specific clinical densitometric
techniques for predicting mechanical strength of the distal radius in different loading configurations. DXA of
the distal forearm, spine, femur, and total body and peripheral quantitative computed tomography (pQCT)
measurements of the distal radius (4, 20, and 33%) were obtained in situ (with soft tissues) in 129 cadavers,
aged 80.16 ؎ 9.8 years. Spinal QCT and calcaneal quantitative ultrasound (QUS) were performed ex situ in
degassed specimens. The left radius was tested in three-point bending and axial compression, and the right
forearm was tested in a fall configuration, respectively. Correlation coefficients with radius DXA were r ؍
0
.89, 0.84, and 0.70 for failure in three-point bending, axial compression, and the fall simulation, respectively.
The correlation with pQCT (r ؍ 0.75 for multiple regression models with the fall) was not significantly higher
than for DXA. Nonsite-specific measurements and calcaneal QUS displayed significantly (p < 0.01) lower
correlation coefficients, and QUS did only contribute to the prediction of axial failure stress but not of failure
load. We conclude that a combination of pQCT parameters involves only marginal improvement in predicting
mechanical strength of the distal radius, nonsite-specific measurements are less accurate for this purpose, and
QUS adds only little independent information to site-specific bone mass. Therefore, the noninvasive diagnosis
of loss of strength at the distal radius should rely on site-specific measurements with DXA or pQCT and may
be the earliest chance to detect individuals at risk of osteoporotic fracture. (J Bone Miner Res 2002;17:
1
629–1638)
Key words: distal radius, bone strength, fracture, densitometry
INTRODUCTION
are fractures, which cause a substantial reduction in the
(1)
quality of life of the elderly and a heavy burden on public
(2)
STEOPOROSIS REPRESENTS a major health problem rele- health care systems.
O
vant to most geographic areas and populations around
the world. The clinical endpoint of osteoporotic bone loss menopause,
years having sustained a clinical fracture at this skeletal
The incidence of distal radius fractures rises steeply after
(3,4)
with 20% of all women at the age of 70
(5,6)
The authors have no conflict of interest.
site.
Fractures of the radius represent an early predictive
1
Frauenklinik Innenstadt, Ludwig-Maximilians-Universit a¨ t M u¨ nchen, M u¨ nchen, Germany.
Dr. Lochm u¨ ller and Dr. Lill share first authorship because they have contributed equally to this study.
AO Forschungsinstitut, Davos, Switzerland.
2
3
4
5
Department of Orthopedic Surgery, University of Heidelberg, Heidelberg, Germany.
Musculoskeletal Research Group, Institute of Anatomy, Ludwig-Maximilians-Universit a¨ t M u¨ nchen, M u¨ nchen, Germany.
1
629

¨
LOCHMULLER ET AL.
1
630
TABLE 1. SUMMARY OF IMPORTANT STUDIES ON THE SITE-SPECIFIC CORRELATION OF BONE DENSITOMETRY
SPA, DXA, AND PQCT) WITH FAILURE LOAD OF THE DISTAL RADIUS
(
Load
type
No. of
specimens
Method of
densitometry
Author
Horsman and Currey 1983
Variable
BMC
CrtCNT
BMD
Trab. Dens.
BMD
BMC
BMC
BMC
CrtA
CrtA
BMD
CrtCNT
BMD
CrtA
BMC
CrtA
r
(22)
Axial
Axial
Axial
17
33
9
SPA
0.83
0.87
0.76
0.73
0.87
(23)
Louis et al. 1995
Gordon et al. 1998
pQCT
DXA
pQCT
DXA
SPA
DXA
SPA
QCT
pQCT
DXA
pQCT
DXA
pQCT
DXA
pQCT
(24)
(25)
Wigderowitz et al. 2000
Axial
Fall
Fall
29
12
24
12
(26)
Myers et al. 1991(
0.79
0.35
27)
Myers et al. 1993
Spadaro et al. 1994
(13)
Fall
0.92–0.94
0.84–0.89
0.71–0.89
0.70–0.73
0.72–0.86
0.67–0.75
0.61–0.67
0.78–0.88
0.76–0.82
(
14)
Augat et al. 1996(
Fall
Fall
19
17
15)
Augat et al. 1998
(
28)
Wu et al. 2000
Fall
Fall
13
14
(29)
Njeh et al. 2000
3
r, Correlation coefficient; BMC, in grams; CrtCNT, cortical bone mineral content (g/mm); Trab. Dens., trabecular density (g/cm );
CrtA, cortical area; when ranges of correlation coefficients are given, these refer to measurements at different sites of the radius within
2
the same study; please note that if the coefficient of determination (r ) was given in the respective study, this was transferred into the
correlation coefficient (r) in this table to achieve consistency between studies.
sign of future fractures at other sites such as the proximal
Previous studies have compared mechanical failure loads
(4,7–8)
femur or spine.
Thus, the noninvasive diagnosis of of the distal radius in small sets of specimens with site-
loss of strength at the distal radius may be the earliest specific densitometry such as single photon absorptiometry
(13–15,21–29)
chance to detect individuals at risk of osteoporotic bone loss (SPA), DXA, or pQCT
(Table 1), but these usu-
and potential fracture. Because it is easier to prevent bone ally have been performed without soft tissues (except for
(28)
(29)
loss at an early stage than to restore bone strength at a later those performed by Wu et al.
and Njeh et al. ). In
stage of the disease, early diagnosis of reduction in strength recent studies, we have shown that bone failure loads dis-
at the distal radius may be the first chance to identify play only moderate (albeit significant) correlation between
(
7)
patients who profit from treatment.
skeletal sites and that these are predicted more accurately by
(30)
Several methods are available to measure the bone min- site-specific DXA than by nonsite-specific DXA.
We
Currently, DXA is the most also have shown that pQCT measurements at the distal
widely used, but the surrounding soft tissues may introduce radius predict femoral failure loads with the same accuracy
(9,10)
eral status clinically.
(11,12)
relevant measurement errors.
In particular, DXA can- as pQCT analysis at the peripheral lower limb but are
not discriminate between cortical and trabecular bone.
However, geometric parameters of the cortical shell, as femoral neck. However, no previous study has compared
(9)
inferior to pQCT measurements obtained directly at the
(31)
measured with peripheral quantitative computed tomogra- the failure loads of the distal radius with nonsite-specific
(
30)
(28,29)
phy (pQCT), have been suggested to be important for ac- measurements other than DXA or phalangeal QUS,
curate prediction of bone strength.
(13–15)
QCT allows for the and no previous study has compared the correlation of
separate analysis of trabecular and cortical bone and can be densitometric variables of several techniques with both a
(16)
performed with conventional clinical CT scanners. How- fall simulation and the major components of the typical
ever, measurements in the spine may not correlate highly distal radius fracture, namely, dorsal bending and axial
(14,17)
(15,32)
with those at the distal radius,
and they do not allow compression.
for the extraction of geometric parameters of long periph-
The objective of this study was to evaluate comprehen-
eral bones such as the distal radius. Quantitative ultrasound sively the ability of clinically available site-specific and
QUS) at the calcaneus has been shown to display a relevant nonsite-specific densitometric techniques in predicting bone
relationship with trabecular microstructure and mechanical strength of the distal radius in different loading configura-
(
(
18–20)
properties.
This has stimulated hope that QUS may tions in a large set of specimens. We specifically tested the
provide significant independent information for the predic- hypotheses that (1) pQCT allows for an improvement of the
tion of bone strength, beyond that of bone mass or density. prediction of bone strength at the distal radius beyond that
The attractiveness of this technique lies mainly in the com- of bone mass, as measured with DXA under in situ condi-
plete lack of ionizing radiation and in the relatively low tions; (2) nonsite-specific measurements (DXA, spinal
(
19,20)
costs involved.
QCT, and calcaneal QUS) display significantly lower cor-

RADIUS BONE STRENGTH AND DENSITOMETRY
1631
relations with radial failure loads than site-specific DXA or
QCT measurements of the lumbar spine (L2–L4) were
pQCT; (3) calcaneal QUS can, nevertheless, add significant obtained ex situ with a Somatom Plus 4 CT scanner at 80
independent information (to site-specific bone mass) in pre- kV (Siemens, Erlangen, Germany). The standard settings of
dicting bone strength of the distal radius; and (4) the pre- the manufacturer were applied (slice thickness, 10 mm;
dictive ability of the various techniques and parameters in-plane resolution, 0.42 mm), and a phantom with equiv-
3
3
differs for bending and axial compression of the distal alents of 0 mg/cm and 200 mg/cm hydroxylapatite was
radius and, therefore, contribute differently to the prediction used to convert Hounsfield units into density values. To
of the strength that is relevant in resisting a distal radius avoid artifacts from trapped air, the specimens were de-
fracture.
gassed under water at 50 mbar, sealed in thin polyethylene
bags, and measured within an aqueous surrounding. Images
were obtained at the midvertebral level, the trabecular and
cortical density of L2–L4 being determined automatically
by the software. The root mean square (RMS) average CV%
of repeated measurements (4 repetitions in 14 specimens
with repositioning, obtained at different days) was 2.9% for
trabecular and 3.1% for (sub)cortical density. For determi-
nation of the CSAs of the vertebral bodies, the precision
error was 1.2%.
QUS measurements of the calcaneus were performed ex
situ to avoid potential artifacts from gas in the soft tissues of
formalin-fixed cadavers. The calcanei were dissected clean
of the surrounding tissues and degassed as described previ-
ously. Measurements were performed with an Achillesϩ
scanner (GE Lunar) sealed for underwater usage to deter-
MATERIALS AND METHODS
Study sample
One hundred forty specimens were examined from a
course of macroscopic dissection, for which the donors had
dedicated their body several years before death.
biopsy specimens were taken from the left iliac crest and
prepared for histomorphometry as described previously.
Three specimens with signs of malignancy and seven spec-
imens with signs of renal osteopathy were discarded. One
additional specimen was discarded because of an osteolytic
lesion in the QCT scans. Of the remaining 129 specimens,
(30)
Bone
(30)
8
2 were women (age, 82 Ϯ 8.4 years) and 47 were men
mine the speed of sound (SOS), broadband ultrasound at-
(age, 77 Ϯ 11.1 years).
(34)
tenuation (BUA), and stiffness index (SI).
The calcanei
were measured in a temperature-controlled water bath
37°C) at an anatomically defined position and were al-
lowed to equilibrate to temperature before measurement.
DXA measurements were performed before the course The precision with this system was found to be in the range
(
Bone densitometry with DXA, pQCT, QCT, and QUS
(34)
with intact skin and soft tissues, using a DPX-L scanner (GE of in vivo measurements.
Although formalin fixation
Lunar, Madison, WI, USA). The bone mineral content (Ͼ1 year) decreased the SOS and SI, the values after fixa-
(
(
3
BMC; g) and the projected areal bone mineral density tion were highly correlated with those before embalm-
BMD; g/cm ) were obtained for the left forearm (distal, ment.
3%; radius, ulna, and forearm ϭ both bones together), the
2
(34)
lumbar spine (AP direction), the left femur (neck, trochan-
ter, and total proximal femur), and the total body. We have
shown previously that formalin fixation does not critically
Radiographic analysis
The bones were excised after the course and cleaned of
(12)
affect these measurements
and that the precision is sim- muscles and soft tissues. However, in the right forearm, the
(30)
ilar to that reported for in vivo conditions.
soft tissues were left intact, including tendons, ligaments,
pQCT measurements were performed with intact soft and the interosseous membrane. The wrist joint and hand
tissues at the distal radius (4, 20, and 33% from the wrist also were left intact, to allow for the application of loads for
joint), using an XCT 2000 scanner (Stratec Medizintechnik, mechanical testing. The forearms and the spines were
Pforzheim, Germany). Technical details and the precision X-rayed in two planes with a Siemens X-ray system
(31,33)
have been described previously.
In brief, the bone (Polyphos 30 M; Siemens), and all other bones were
mineral content (CNT; g/mm), the cross-sectional bone area X-rayed with a Faxitron Cabinet X-ray system (model
3
(
CSA), and the bone mineral density (g/cm ) were deter- 43885A, Faxitron X-ray systems; Hewlett Packard, McMin-
mined at the 4% site for the entire cross-section as well as nville, OR, USA). The films were evaluated by an experi-
3
for the trabecular (Ͻ400 mg/cm ) and subcortical (Ͼ400 enced radiologist, to exclude fractures or other local bone
3
mg/cm ) compartment. At the 20% and 33% sites, these disorders. Spinal DXA and QCT values were discarded in
parameters were determined for the entire cross-section as cases in which fractures or deformities were detected in
3
well as for the cortical compartment (Ͼ710 mg/cm ). Ad- lumbar vertebrae.
ditionally, geometric properties of the cortical shell were
determined, including the cortical thickness (Crt.Th; mm),
the polar moment of inertia (1 mm ), the minimal and
Mechanical testing
4
(
14)
maximal (bending) moment of inertia,
and the density-
A three-point bending test was performed on the left
3
weighted polar moment of resistance (R; mm ), which also radius, 33% proximal to the wrist joint (Fig. 1A). Five
(
15,21)
has been termed the strain-stress index.
These param- specimens could not be tested because of osteosynthetic
eters originate from engineering principals for estimating material or suspect of previous fracture. To test identical
(14)
the torsional and bending strength of structures.
anatomic regions in all specimens, the shaft was fixed at

¨
1
632
LOCHMULLER ET AL.
vidual moment arms, the failure moment (Nm) was deter-
mined. Five specimens were excluded after testing because
of fracture at a site other than the 33% location. From the
distal end of the same radius, a 10-mm planoparallel axial
slice was removed adjacent to the joint surface (Fig. 1B),
using a diamond band saw (Exact Trennschleifsystem, Nor-
derstedt, Germany). The CSA of both sides of the slice were
measured on scaled paper to allow for the calculation of the
failure stress after testing (peak load divided by CSA
2
[
N/mm ]). An axial compression test was performed at a
0
.8-mm/s loading rate (Fig. 1B), recording the initial peak
(
failure load) of the load-displacement curve with a subse-
quent drop of Ͼ10%.
On the right forearm, a fall was simulated.
(13,26)
The test
was performed with an Instron testing machine (model
302; Instron, High Wycombe, UK). The ulna and radius
4
were embedded in plaster (True Rock; Benzer Dental AG,
Z u¨ rich, Switzerland), with the hand in 70° dorsiflexion and
1
1
0° radial abduction and with the forearm in pronation (Fig.
C). The load was applied through a wedge (the loading
rate, 3.3 mm/s). Failure loads were recorded as the peaks of
the load-displacement curves and were only considered if a
distal radius fracture occurred that could be classified ac-
cording to the Arbeitskreis Osteosynthese Fragen (AO)
(35)
classification.
Briefly, fractures were classified into type
A (extraarticular), B (partly articular), and C (intraarticular),
with increasing complexity from 1 to 3. The type of fracture
was determined from two X-rays (two planes) and from
surgical preparation of the fracture zone. We observed 42
A2 fractures, 19 type A3, 1 type B1, 14 type B2, 2 type B3,
8
type C1, 14 type C2, and 2 type C3 fractures. Twenty-
seven specimens were discarded because they could not be
classified as one of these types of fractures (e.g., shaft
fractures, ulnar fractures, or isolated scaphoid fractures).
Statistical analysis
Differences between genders were assessed using the
unpaired t-test. Simple linear regression analysis was used
to determine the correlation of failure strength between
different loading configurations and with the densitometric
parameters. Fisher z-transformation was used to assess
whether certain coefficients were significantly higher than
others.
Stepwise multiple regression models (forward mode)
were used to identify whether a combination of pQCT
parameters from the metaphyseal (4%) and shaft location
(
20%) allowed for improved prediction of mechanical
strength versus single variables. In the first model (model 1)
we combined the total CSA and total density at the 4% and
2
0% site as well as all parameters describing specific prop-
erties of the trabecular (4% site) and cortical compartment
20% site). The total, cortical, and trabecular BMC were not
FIG. 1. Drawings showing the mechanical testing conditions (A)
three-point bending (left radius), (B) axial compression (left radius),
and (C) fall simulation (right forearm).
(
entered at this step, because these represent direct products
of the density and CSAs. In a second multiple stepwise
regression model (model 2), we included the total content
(
but not the total area and density) at the 4% and 20% site,
6.5% and 49.5% of the individual bone length, using two as well as the parameters describing specific properties of
elements that were able to rotate and translate freely (Fig. the trabecular and cortical compartment. In this way we
A). From the failure load at 6.5 mm/s and from the indi- determined whether certain parameters could improve the
1
1

RADIUS BONE STRENGTH AND DENSITOMETRY
1633
TABLE 2. DESCRIPTIVE DATA OF THE MECHANICAL TESTS WITH MEAN VALUES (ϮSD) FOR MEN AND WOMEN,
RESPECTIVELY
Fall
Three-Point bending
Axial load
(kN; n ϭ 124)
Axial stress
(N/mm ; n ϭ 124)
configuration
(kN; n ϭ 102)
2
(kNmm; n ϭ 119)
Men
31.3
3.41
6.66
2.23
Women
15.5
Ϫ50%
p Ͻ 0.001
1.87
Ϫ45%
p Ͻ 0.001
4.85
Ϫ27%
p Ͻ 0.001
1.21
Ϫ46%
p Ͻ 0.001
a
%
Difference
b
Significance
a
Percent difference between both genders (women related to men).
Level of statistical significance of gender difference (unpaired t-test).
b
prediction of bone strength beyond that of total (cross-
sectional) content alone. Stepwise regression models also
trabecular area at 4% as well as cortical area and polar
moment of resistance at 20%);
were used to determine whether calcaneal QUS was able to (3) Axial compression failure stress: r ϭ 0.70 for models
contribute significant independent information to the site-
specific bone mass (DXA) in predicting failure strength.
1 and 2 (trabecular density at 4% and cortical thickness
at 20%);
(
4) Fall simulation failure load: r ϭ 0.72 for model 1 (total
density at 4% and polar moment of resistance at 20%)
and r ϭ 0.75 for model 2 (total content and trabecular
area at 4% and polar moment of resistance at 20%).
RESULTS
The bone failure loads and moments in bending were
significantly higher in men than in women, and this also
applied for the failure stress in axial compression (Table 2).
The correlation of strength in axial compression and three-
point bending was r ϭ 0.81 (p Ͻ 0.001). Axial compression
displayed a somewhat higher correlation coefficient with the
fall configuration (r ϭ 0.77; p Ͻ 0.001) than bending (r ϭ
Although the combination of various pQCT parameters
tended to improve the prediction of failure loads versus
single variables, the multiple regression coefficients were
not significantly higher than those obtained by DXA (Table
3
; Fig. 2).
For three-point-bending moments and axial failure loads,
all nonsite-specific measurements displayed significantly
p Ͻ 0.01) lower correlation coefficients than site-specific
0
.65; p Ͻ 0.001), but the difference was not significant.
(
There were no obvious differences in failure loads in the fall
simulation between groups with different fracture types
DXA or pQCT (Table 3; Fig. 2). For the fall simulation,
nonsite-specific measurements also displayed significantly
lower associations (p Ͻ 0.05 to 0.01). Calcaneal QUS
tended to produce lower correlation coefficients than other
nonsite-specific analysis in three-point bending and axial
compression but was equivalent to nonsite-specific DXA in
the fall simulation. In predicting radial failure stress in axial
loading, QUS tended to display a higher correlation than
other nonsite-specific measurements, with the coefficients
being in the range of those of site-specific analysis (Table
(AO classification).
DXA of the left distal radius BMC displayed correlation
coefficients of r ϭ 0.89 with the failure moment in three-
point bending, r ϭ 0.84 with the failure load in axial
compression, and r ϭ 0.70 with the failure load in a simu-
lated fall (Table 3; Fig. 2). DXA of the ulna or total forearm
displayed slightly lower associations (Table 3).
With pQCT, the highest correlation coefficients in three-
point bending were for the cortical content at 20% (r ϭ
3
). The calcaneal SI was able to contribute significant in-
0
.91), in axial compression for the total content at 20% (r ϭ
dependent information to site-specific DXA in predicting
axial failure stress but none of the QUS parameters were
part of multiple regression models when predicting failure
loads in any of the loading configurations.
The correlation coefficients for site-specific and nonsite-
specific measurements were generally highest for three-
point bending, followed by the axial compression and even-
tually by fall simulation (Fig. 2). Only calcaneal QUS
displayed a higher correlation with axial compression than
with bending.
0
.81), and in the fall simulation for the total content at 4%
or 20% (r ϭ 0.67). However, these coefficients were not
significantly higher than those obtained by DXA. pQCT
measurements at the 33% measurement location were
highly correlated with those at 20% and did not display
higher correlation coefficients than those at 20% (data not
shown). Stepwise regression models with variables from the
4
% and 20% measurement site produced the following
results for the various loading configurations:
(1) Three-point bending failure moment: r ϭ 0.90 for
model 1 (cortical area at 20%) and r ϭ 0.91 for model
2
(total content at 4% and cortical content at 20%);
DISCUSSION
(
2) Axial compression failure load: r ϭ 0.84 for model 1
(cortical area at 20% and polar moment of resistance at
In this study we tested the hypotheses that (1) pQCT
2
0%) and r ϭ 0.87 for model 2 (total content and allows improvement of the prediction of bone strength at the

¨
LOCHMULLER ET AL.
1
634
TABLE 3. CORRELATION BETWEEN BONE STRENGTH AT THE DISTAL RADIUS IN THREE-POINT BENDING, AXIAL COMPRESSION,
AND A FALL CONFIGURATION WITH DENSITOMETRIC DATA
Three-point
bending
Axial
stress
(n ϭ 124)
Fall
configuration
(n ϭ 102)
Axial load
(n ϭ 124)
(
n ϭ 119)
DXA
Radius
distal 1/3)
Ulna
distal 1/3)
Forearm
distal 1/3)
BMC
BMD
BMC
BMD
BMC
BMD
CNT (Dens*)
Trab. CNT (Dens*)
CNT (Dens*)
Crt.CNT (Dens*)
Crt.Th.
I polar
R polar
I Minimum
I Maximum
0.89
0.88
0.87
0.86
0.89
0.89
0.75
0.53
0.90
0.91
0.85
0.74
0.81
0.74
0.74
0.91
0.70
0.61
0.66
0.63
0.71
0.64
0.69
0.60
0.77
0.74
0.57*
0.61
0.50
0.54
0.54
0.84
0.78
0.80
0.79
0.83
0.80
0.75
0.55
0.81
0.79
0.73
0.72
0.79
0.70
0.72
0.87
0.65
0.57
0.65
0.61
0.67
0.59
0.62
0.51
0.70
0.68
0.47*
0.56*
0.56
0.60
0.60
0.62
0.65
0.57
0.66
0.60
0.67
0.61*
0.55*
0.63*
0.58*
0.66
—
0.70
0.64
0.65
0.66
0.69
0.66
0.67
(
(
(
‡
†
pQCT
Radius 4%
‡
‡
‡
0.46
Radius 20%
0.67
0.65
0.57
0.58
0.66
0.55
0.57
0.75
0.46
0.42
0.42
0.45
0.48
0.46
0.47
0.42
0.54
0.55
0.41
0.54*
†
‡
‡
a
†
—
—
—
‡
‡
‡
‡
‡
Multiple regression (see text)
Neck
0.70
0.52
0.51
‡
‡
†
DXA
BMC
BMD
BMC
BMD
BMC
BMD
BMC
BMD
BMC
BMD
Density (ϫ CSA*)
Density (ϫ CSA*)
SOS
BUA
SI
‡
‡
‡
‡
‡
†
‡
Trochanter
Total femur
L2–L4
0.46
‡
‡
‡
0.54
0.52
0.54
0.48
‡
‡
‡
‡
‡
‡
‡
‡
‡
‡
‡
†
‡
0.45
‡
‡
†
Total body
Trabecular
0.57
0.61
0.46
‡
‡
†
,
‡
,‡
†
‡
QCT
‡
,‡
†
,‡
Cortical
Calcaneal
Ultrasound
0.46
‡
‡
‡
0.61
0.61
0.63
0.40
0.47
0.46
‡
‡
‡
‡
‡
‡
Please note that the QCT density values were multiplied with the CSA of the lumbar vertebral bodies to obtain correlation coefficients
with the failure loads, but not with the failure stress.
Radius 4%, metaphyseal location 4% proximal to the wrist joint; radius 20%, shaft location 20% proximal to the wrist joint; Mult.
Regress., multiple regression from variables measured at 4% and 20%; L2–L4, lumbar vertebral segments 2–4; BMC, in grams; BMD,
in grams per squared centimeter; CNT, bone mineral content (g/mm); Dens., density; Trab., trabecular; Crt.Th, cortical thickness; I,
moment of inertia; R, moment of resistance; SOS, in meters per second; BUA, in decibels per megahertz.
a
Density weighted.
†
All correlation coefficients were significant at p Ͻ 0.01; correlation coefficient significantly lower ( p Ͻ 0.05) than that with
‡
radius DXA; correlation coefficient significantly lower ( p Ͻ 0.01) than that with radius DXA.
(2)
distal radius beyond that of bone mass (in situ DXA); (2) care system, and their age-related increase in incidence
(36)
nonsite-specific measurements (DXA, spinal QCT, and cal- has been shown to precede that in the hip and spine.
caneal QUS) display a significantly lower association with Experimentally, we have shown that bone failure loads are
radial failure loads than site-specific DXA or pQCT; (3) only moderately, but significantly, associated between the
(30)
(8)
calcaneal QUS can, nevertheless, add significant indepen- distal radius and other sites.
A recent meta-analysis of
dent information to bone mass in predicting bone strength; clinical studies has convincingly shown that patients with
and (4) the predictive ability of densitometric techniques fracture generally suffer from an increased risk of subse-
and parameters differs for bending and axial compression. quent fractures. Specifically, fractures of the forearm were
The forearm (distal radius) has been identified as an associated with a high relative risk of subsequent fractures
(8)
important site of fracture, with a high likelihood of relevant at the hip, spine, and other sites. The increase in relative
attribution to risk from osteoporotic bone loss, particularly risk of fracture at all sites was similar for radius fractures
(1)
in elderly women. Distal radius fractures also cause sub- that had occurred in adolescence compared with those at or
(7)
stantial expenditures (385 million US$/year) to the health after menopause. Cuddihy et al. concluded from a retro-

RADIUS BONE STRENGTH AND DENSITOMETRY
1635
termined in vivo and the bending and compression compo-
nent of distal radius strength cannot be separated in an
analysis of clinical fractures. Moreover, longitudinal studies
into the value of different densitometric techniques require
long time intervals and are complicated by cumulative
X-ray exposure arising from application of multiple mea-
surement techniques in the same subject (usually healthy
volunteers). No previous experimental study has determined
the strength of the distal radius in a fall simulation as well
as in axial compression and bending, has assessed the ability
of site-specific (DXA and pQCT) versus nonsite-specific
X-ray techniques (DXA, QCT, and QUS), and has analyzed
the correlation of calcaneus QUS with distal radius strength
in different loading configurations. In particular, no other
study has reached a comparable sample size (Table 1). In
contrast to specimens obtained from pathological dissec-
tion, our study sample did not include a preselection of
highly pathological cases and thus may be considered rep-
resentative for the elderly population in southern Ger-
(30)
many.
By obtaining X-rays from all skeletal regions and
performing a histomorphometric analysis of the iliac crest,
we were able to apply exclusion criteria similar to clinical
(39)
studies. Regarding the fixation, Edmonston et al.
and
(14)
Augat et al. concluded that mechanical strength of entire
bones is affected only minimally by formalin solution and
that the correlation between BMC and mechanical strength
is not altered. In this context, it also must be noted that the
distribution of types of distal radius fractures (AO classifi-
cation) closely resembled that seen clinically. We are not
2
FIG. 2. Bar graph showing coefficients of determination (r ) between
failure loads in three-point bending, axial compression, and a fall
simulation and site-specific versus nonsite-specific densitometric mea- aware of epidemiological studies into the distribution of AO
surements. BMC, bone mineral content (g); CNT, bone mineral content fracture types in elderly subjects, but a recent analysis of
40)
g/mm); trab, trabecular; cort, cortical; US, calcaneal quantitative snowboard injuries( in Japan (99 distal radius fractures)
(
ultrasound; stiff. ind., stiffness index.
revealed 51% A2, 19% A3, 7% B1, 11% C1, 9% C2, and
% C3 fractures. Apart from the absence of B2 and B3
3
fractures in these Japanese snowboarders, this distribution is
in high agreement with that produced by our biomechanical
test. In addition, we have shown previously that even 10-
month formalin fixation does not significantly affect DXA,
spective study into forearm and subsequent fractures that a
sentinel forearm fracture should not be ignored in men and
that the opportunity for therapeutic intervention (e.g., hor-
mone replacement therapy) at the time of distal radius
fracture was underutilized in women. Regarding the predic-
tive ability of densitometric measurements, Marshall et
(12)
not even under in situ conditions. Moreover, densitomet-
ric measurements of this study are in the range of those
(41)
(
37)
reported in vivo, except for QUS. The SOS and SI of the
calcaneus have been shown to decrease significantly with
fixation, but values were highly correlated with those before
al. maintained, from a meta-analysis of ϳ2000 fractures,
that all DXA measurement sites (including the distal fore-
arm) had similar predictive abilities, with the exception that
spinal measurement was the best predictor for vertebral
fracture and femoral measurement was the best for hip
(34)
fixation in fresh specimens.
Thus, the correlation be-
tween QUS and bone strength is likely not affected by the
use of fixed specimens.
(38)
fracture. It has been shown also
that the long-term pre-
The highest correlation between densitometry and failure
loads in our study generally was observed for three-point
bending and the lowest was for the fall simulation. This is
not surprising because of the more controlled mechanical
diction of bone densitometry at the distal forearm (up to 11
years before fracture) was similar in magnitude compared
with short-term prediction (Ͻ3 years before fracture).
Taken together, these results suggest that the noninvasive
diagnosis of loss of bone mineral at the distal radius may be conditions during bending, in which failure occurs directly
the earliest chance to detect individuals at risk of osteopo- at the site of load application. In axial compression, the site
rotic fracture at this and other sites. Because it is easier to of failure is confined to the cross-sectional specimen but
prevent bone loss at an early stage than to restore bone may vary in location and bone compartment (trabecular or
strength at later stages of the disease, early diagnosis of cortical). Similar correlation coefficients between failure
reduction in strength at the distal radius thus may be the first loads in axial compression and bone densitometry also have
(22–25)
chance to identify patients who profit from treatment.
been reported by other authors.
With a more complex
We have selected an experimental (biomechanical) study failure test such as a fall simulation, the site of failure is
design because bone strength cannot be quantitatively de- more variable. Therefore, it is obvious that it is more diffi-

¨
1
636
LOCHMULLER ET AL.
(13–15,26–29)
cult to predict fracture loads in this loading mode
than in the other loading configurations.
the calcaneus is determined primarily by trabecular proper-
ties. Interestingly, however, calcaneal QUS reached sim-
(43)
The association between failure loads in the fall config- ilar correlations as DXA for axial failure stress and was an
uration and radial DXA in our study (r ϭ 0.70) is in the independent predictor, potentially because calcaneal QUS
(
13–15,26–29)
range of that reported previously,
although pre- carries less information on bone size than DXA.
We expected densitometric measurements at predomi-
vious authors have performed measurements in the same
arm (usually under ex situ conditions), whereas in our case, nantly cortical sites (e.g., DXA of the femoral neck) to be
DXA was performed in the contralateral arm and by main- correlated more highly with the bending component of
taining the soft tissue errors involved in clinical measure- strength at the radial shaft, and measurements at predomi-
(26,27)
ments. Myers et al.
developed a multiple-angle scan- nantly trabecular sites (e.g., greater trochanter or spine) to
ning technique to determine the moment of inertia of the be associated more highly with failure of the radial metaph-
distal radius from DXA scans. With this method, they were ysis in axial compression. However, this did not become
able to improve the correlation coefficients with failure evident in our study. Potential reasons may be that bone
strength versus the BMC in multiple regression models. properties are very heterogeneous between skeletal
(17,33,44,45)
Today, the moment of inertia and other geometric parame- sites,
and that the compressive strength of the
ters of the cortical shell can be determined tomographically distal metaphysis is more strongly determined by the prop-
(
9)
by pQCT. Several authors have identified geometric pa- erties of the (sub)cortical rather than the trabecular com-
rameters of the radial cortex to be important predictors of partment.
(
13–15,23)
strength in the distal radius.
al.,
Contrary to Augat et
In conclusion, this experimental study shows that (1) a
(
15)
(13,24,28,29)
however, other investigators
reported that combination of pQCT parameters (specifically geometric
these parameters did not attain higher correlations than the properties of the cortical shell) tends to improve the predic-
BMC from DXA. We observed a trend for multiple regres- tion beyond that of bone mass BMC alone, but correlation
sion models from pQCT parameters to slightly improve the coefficients are not significantly higher than those for site-
prediction of bone strength compared with single pQCT specific DXA; (2) indeed, nonsite-specific measurements
parameters or DXA, but the gain in information was not display significantly lower correlation coefficients with fail-
statistically significant. Therefore, we found no evidence ure loads compared with site-specific analysis, independent
that pQCT is superior to DXA in determining the mechan- on which measurement technique; (3) calcaneal QUS adds
ical strength of the distal radius, even under in situ mea- independent information to site-specific bone mass only in
surement conditions, including DXA soft tissue arti- predicting axial failure stress in axial compression but not in
(
11,12)
facts.
Likely explanations are that soft tissue artifacts predicting failure loads in any other loading configuration;
of DXA at the distal radius are small, the bone mass (4) calcaneal QUS tends to be a superior predictor of the
measured with DXA in the distal radius is predominantly compressive (rather than the bending) component of distal
determined by cortical bone, and the bone mass is distrib- radius strength, whereas all other (site-specific and nonsite-
uted in very similar ways throughout the cross-section in specific) parameters exhibit no obvious tendency to predict
most individuals.
either component of strength with higher accuracy than the
We find pQCT parameters at 20% and 33% radial length other. The noninvasive diagnosis of loss of strength at the
to be of similar value in predicting mechanical strength, distal radius thus should primarily rely on site-specific mea-
even for the three-point bending test, in which failure oc- surements with either DXA or pQCT. Because loss of
curred specifically at the 33% site. Interestingly, the pQCT strength at the radius has been shown to precede that in the
parameters from the shaft also displayed higher coefficients spine and femur, this may be the earliest chance to detect
with failure of the metaphysis (axial compression) than the individuals at risk of osteoporotic fracture and to initiate
parameters from the metaphyseal site itself. Although this therapeutic treatment.
may appear paradox, similar results also have been reported
(14,15)
by Augat et al.,
likely because cortical properties can
be measured more accurately with pQCT at the shaft than at
the metaphysis. However, we found no differences for
pQCT parameters from the shaft or metaphyseal location in
predicting strength in the fall configuration.
ACKNOWLEDGMENTS
We thank G u¨ nther Delling and coworkers (Abteilung
Osteopathologie, Universit a¨ tsklinikum Eppendorf, Ham-
(
28)
(29)
Wu et al.
and Njeh et al.
reported phalangeal QUS burg, Germany) for the histomorphometric analyses, Jan
to display similar correlations with failure as DXA or pQCT Grimm (Medizinische Physik, Klinik f u¨ r Diagnostische Ra-
and to add independent information to site-specific bone diologie, Kiel, Germany) for reading the spinal X-rays, and
mass. In this study, QUS of the calcaneus displayed signif- Horst Russ (Anatomische Anstalt M u¨ nchen) for drawing
icantly lower correlation coefficients with failure loads in all Fig. 1. Albert Albrecht (AO-Forschungsinstitut, Davos),
loading configurations compared with site-specific measure- Markus Bachmeier, Boriana Barth, Hans-J u¨ rgen Becker,
ments and did not contribute to failure load prediction in Gudrun Goldmann, Oliver Groll, and Nadine Krefting
stepwise regression models. Potential reasons for the differ- (Musculoskeletal Research Group, Institute of Anatomy
ent outcomes include the small sample size (Table 1), mea- M u¨ nchen) are acknowledged for their help with radiogra-
surements at the phalanges are closer to the site of interest phy, densitometric measurements, and biomechanical test-
than those at the calcaneus, or phalangeal QUS properties ing. This work has been supported by a grant from the
(42)
depend more strongly on cortical bone,
whereas QUS of Deutsche Forschungsgemeinschaft (DFG LO 730/2–1).

RADIUS BONE STRENGTH AND DENSITOMETRY
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Eva-Maria Lochm u¨ ller, M.D.
Frauenklinik Innenstadt
Ludwig-Maximilians-Universit a¨ t M u¨ nchen
Maistr. 11, D 80337 M u¨ nchen, Germany
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