A Correlation Exists Between Subchondral Bone Mineral Density
of the Distal Radius and Systemic Bone Mineral Density
Seung Hwan Rhee MD, PhD, Goo Hyun Baek MD, PhD
Received: 21 June 2011/Accepted: 24 October 2011/Published online: 3 December 2011
? The Association of Bone and Joint Surgeons1 2011
common and risk articular congruity owing to disruption of
the subchondral bone. Studies regarding microstructure and
mechanical properties of the distal radius, however, focus
only on the cortical and trabecular bones in the metaphysis
and not on the subchondral bone.
(1) quantify the regional bone mineral density of the sub-
chondral plate in the distal radius; (2) analyze the
topographic distribution pattern of the subchondral bone
clinical factors of age, height, weight, BMI, systemic bone
Intraarticular distal radius fractures are
mineral densities, socio-occupational classification, and
hand osteoarthritis grading.
Eighty postmenopausal women with a mean age
of 68 years (range, 52–88 years)were enrolled inthisstudy.
by conventional CT and processed to provide the regional
bone mineral density of the subchondral plate using a CT
osteoabsorptiometry technique. The estimated subchondral
bone mineral density was analyzed to evaluate the topo-
graphic pattern and its correlation with various clinical
factors, including age, height, weight, BMI, degree of hand
osteoarthritis, socio-occupational class, and systemic bone
mineral density measured in the lumbar spine and hip.
During topographic analysis of a densitometric
map, a bicentric distribution of the subchondral bone
mineral density was found. Among the clinical factors,
only the systemic bone mineral density measured by dual-
energy x-ray absorptiometry in the femur neck and lumbar
spine had a significant correlation with the subchondral
bone mineral density of the distal radius.
Systemic bone mineral density correlates
substantially with the subchondral bone mineral density of
the distal radius as a constitutional factor, whereas other
local factors arising from the gravitational load or joint
reaction force are not associated with the subchondral bone
mineral density of the distal radius.
Level of Evidence
Level II, prognostic study. See
Guidelines for Authors for a complete description of levels
Distal radius fractures are representative fragility fractures
but their relationship with systemic bone mineral density
One of the authors (SHR) has received funding from the Seoul
National University Hospital Research Fund (04-2010-0620).
All ICMJE Conflict of Interest Forms for authors and Clinical
Orthopaedics and Related Research editors and board members are
on file with the publication and can be viewed on request.
Each author certifies that his or her institution approved the human
protocol for this investigation, that all investigations were conducted
in conformity with ethical principles of research, and that informed
consent for participation in the study was obtained.
This work was performed at the Department of Orthopedic Surgery,
Seoul National University College of Medicine, Seoul, Korea.
S. H. Rhee
Department of Orthopedic Surgery, Seoul National University
Boramae Medical Center, 39 Boramae-gil Dongjak-gu,
Seoul 156-707, South Korea
G. H. Baek (&)
Department of Orthopedic Surgery, Seoul National University
College of Medicine, 101 Daehak-ro Jongno-gu,
Seoul 110-744, South Korea
Clin Orthop Relat Res (2012) 470:1682–1689
and Related Research®
A Publication of The Association of Bone and Joint Surgeons®
(BMD) has not attracted much concern compared with ver-
tebral fractures [2, 10, 14, 21]. However, numerous studies
reported that systemic osteoporosis affects the incidence,
fracture stability, and treatment outcome of distal radius
fractures in the elderly [9, 18–20, 38]. Although this corre-
radius fractures has been reported, another concern regard-
ingwhetherthe systemic BMD couldsubstantially represent
the regional BMD of the distal radius or whether other
clinical factors except for systemic BMD also can affect the
regional bone density of the distal radius using quantitative
CT techniques provided precise and sometimes quantitative
information regarding the structure and mechanical proper-
ties of the distal radius, they focused fundamentally on just
the trabecular bone and its surrounding cortical bone in the
metaphysis and not on the subchondral plate of the distal
radius [3, 11, 24, 34, 36].
Considering that an intraarticular extension of the distal
radius is common (70%–88%) [1, 17, 22] and has been
reported to be related to poor treatment outcome including
radiocarpal arthrosis, limited motion, and poor functional
outcome [13, 22, 23, 31], knowledge of the relationship
between systemic BMD and that of the subchondral plate is
needed. Because distal radius fractures frequently are
caused by falls on an outstretched hand, the major
deforming vector of this injury consists of an axial com-
pressive force and dorsal bending force. This load is
normally delivered to the subchondral bone and adjacent
calcified cartilage and then to the articular cartilage .
The subchondral plate is a major shock-absorbing structure
in the periarticular region and attenuates most of the
impulsive axial load [32, 33]. This mechanism of injury
results in an intraarticular fracture if the transarticular load
exceeds the ultimate strength of the subchondral bone. In
view of this, strength of the subchondral bone is critical
and needs to be quantified.
In this study, we (1) quantified regional BMD of the sub-
chondral plate in the distal radius; (2) analyzed the
(3) evaluated the correlation between the subchondral BMD
and potentially related clinical factors such as age, height,
absorptiometry (DXA) at the proximal femur and lumbar
spine, socio-occupational class, and radiographic evidence of
hand osteoarthritis, to provide insight regarding risk factors
for low subchondral BMD in the distal radius.
Patients and Methods
In this study, 80 postmenopausal women aged 52 to
88 years (mean, 68 years) were involved. We excluded
subjects with chronic arthritis, including rheumatoid
arthritis or osteoarthritis, in the radiocarpal joint or other
preexisting musculoskeletal disorders. The protocol was
approved by the Institutional Review Board. Predetermined
clinical factors consisting of systemic and local factors
were recorded for all patients. For the systemic factors,
demographic data including age, height, weight, BMI, and
BMD of the axial skeleton measured by DXA at the lumbar
area (L2-L4) and proximal femur were checked. The mean
T-score in the lumbar area and T-score of the femur neck
were selected as representative systemic BMD values. For
local factors, we evaluated the accumulated intensity of
hand labor using the radiographic grade of osteoarthritis
and socio-occupational classification. This evaluation pro-
tocol of hand labor intensity arose from the idea that
subjects with radiographic evidence of hand osteoarthritis
or heavy manual workers in the socio-occupational clas-
sification are more likely to be involved in high-level
manual labor and long-term joint reaction force around the
wrist, which possibly leads to a high subchondral BMD.
First, we evaluated radiographic evidence of hand osteo-
arthritis using the modified Kellgren-Lawrence scale;
Grade 2 or higher in this scale measured in the metacar-
pophalangeal or basal joint is defined as definite hand
osteoarthritis (Table 1). This is an extension of the
Framingham study, which shows the relationship between
grip strength and hand osteoarthritis [7, 8]. This extension
appears to be valid because grip strength is related to the
action of the muscle-tendon complex around the wrist. All
radiographic reviews were performed by one author (SHR)
to avoid any potential interobserver bias. Second, for the
socio-occupational classification, the scheme described by
Erikson et al.  was used and subjects with Class IVc,
VIIa, or VIIb in the scheme are defined as being heavy
manual workers (Table 2).
All digital images of the distal radii were scanned using
conventional medical CT (Philips Brilliance 64 multislice
CT scanner, Cleveland, OH, USA). The scanning param-
eters included tube voltage, 120 kVp; tube current, 77 mA;
and scan time, 1.0 seconds. The field of view was set to
125 mm and the full area of the articular surface always
was captured completely. The slice thickness was deter-
mined to be 1.0 mm in all cases. Theoretically, a thinner
Table 1. Modified Kellgren-Lawrence grading system for osteo-
0No features of osteoarthritis
2 Unequivocal osteophytes
3Joint space narrowing
Volume 470, Number 6, June 2012Densitometric Analysis in Postmenopausal Women1683
section might produce more enhanced spatial resolution,
but it was reported that enhanced spatial resolution
acquired even by microCT did not produce a significantly
different density pattern . The wrists were scanned with
the rotation of the forearm set to the full pronated position
and with the axis of the forearm being as perpendicular to
the axial cut plane as possible. The digital images acquired
by conventional CT were saved as DICOM files.
The images saved as DICOM files were imported into
image analyzing software (Analyze; Mayo Clinic, Roches-
true orthogonal images to use the true sagittal images in the
next step. The area of the subchondral plate was cropped
from each image in the series. In this step of cropping, some
portion of the trabecular bone under the subchondral plate
will remain in the cropped image because complete deletion
of the trabecular portion in the image is technically impos-
sible. However, the signal intensity of the trabecular bone is
from the residual trabecular bone does not affect the result
during image processing of the maximum intensity projec-
tion. In the next step, cropped images from serial images
were stacked into a three-dimensional (3-D) object, which
then was digitally rotated 90? to reconstruct the subchondral
plate to face forward. To present the densitometric value of
the subchondral plate, a maximum intensity projection
(MIP) map was developed by extracting the highest signal
intensity of each point in the subchondral plate on the
projection line. This is the process of converting and com-
pressing a series of voxels on the projection line in a 3-D
object to a representative pixel in the two-dimensional
densitometric map. The reconstructed image is shown as a
gray-scale image, but actually the saved image has infor-
mation regarding signal intensity with the Hounsfield unit
(HU), which is the attenuation coefficient used in CT. For
better observation, false-color mapping was applied to the
densitometric map by conversion of each range of the HU
into eight colors. The highest ([ 1400 HU) and lowest
(\ 200 HU) ranges of density values were set to black
and white, respectively, and six more colors were set to be
distributed evenly between them (Fig. 1).
The densitometric map that finally was acquired through
false-color mapping was used for data analysis. We
assessed the gross topographic pattern using a series of
densitometric maps. To quantize this topographic densito-
metric analysis, the subchondral plate of the distal radius
was divided into four subareas (radial half of the scaphoid
fossa, ulnar half of the scaphoid fossa, interfossa ridge, and
lunate fossa) by analyzing the coronal and axial images of
the radiocarpal joint of each subject and the average sub-
chondral BMD of each area expressed by HU was
determined. In addition, we calculated the mean subchon-
dral BMD of the entire subchondral plate, and its
correlation with the clinical factors consisting of systemic
and local factors, described above, was assessed.
All statistical procedures were performed with SPSS
12.0 (Chicago, IL, USA). For the statistical evaluation, the
mean BMDs of the four subareas in the subchondral plate
were compared using Student’s paired t-test. The correla-
tion of the mean BMD of the entire subchondral plate with
a range of clinical factors including age, height, weight,
BMI, and BMD of the femoral neck and lumbar spine was
evaluated using the Pearson’s correlation model. In addi-
tion, we evaluated the correlation between the mean
subchondral BMD and the degree of hand osteoarthritis and
socio-occupational class using a Mann-Whitney U test and
Student’s independent t-test, respectively. Probability val-
ues less than 0.05 were considered significant.
In the quantification, the mean subchondral BMD of the
subjects was 518 HU (range, 360–720 HU), and the range
of the highest proportion was 400 to 600 HU (36%), fol-
lowed by 200 to 400 (25%), 600 to 800 (22%), 800 to 1000
(8%), less than 200 (6%), 1000 to 1200 (2%), and greater
than 1200 HU (1%) (Fig. 2).
Table 2. Erikson-Goldthorpe-Portocarero scheme for socio-occupa-
I Higher-grade professionals, administrators
and officials; managers in large industrial
establishment; large proprietors
II Lower-grade professionals, administrators
and officials; higer-grade technicians;
managers in small business and
industrial establishments; supervisors
of non-manual employees
IIIRoutine non-manual employees in
administration and commerce; sales
personnel; other rank-and-file service
IVaSmall proprietor; artisans, etc., with employees
IVbSmall proprietor; artisans, etc.,
IVcFarmers and smallholders; self-employed
V/IVLower-grade technician;supervisors of manual
workers;skilled manual workers
VIIaSemi- and unskilled manual workers
(not in agriculture)
(Published with permission of John Wiley & Sons Ltd. from Erikson
R, Goldthorpe JH, Portocarero L. Intergenerational class mobility in
three Western European Societies: England, France and Sweden. Br J
1684Rhee and BaekClinical Orthopaedics and Related Research1
Fig. 1 The flow diagram illustrates digital image processing with CT osteoabsorptiometry (CT-OAM).
Fig. 2 The
distribution of subchondral BMD
of the distal radius. HU = Houns-
Volume 470, Number 6, June 2012 Densitometric Analysis in Postmenopausal Women1685
In the topographic analysis, the gross subchondral
BMDs of the scaphoid and lunate fossae were greater than
those of the interfossa ridge and outer rim of the sub-
chondral plate (Fig. 1). The result acquired by quantization
using division of the subchondral plate by four subareas
also showed this bicentric pattern of subchondral BMD.
The mean subchondral BMD of the ulnar half of the
scaphoid fossa (718 HU) was significantly higher than that
of the lunate fossa (556 HU) and interfossa ridge (483 HU)
(p = 0.002 and p\0.001, respectively). In addition, the
mean subchondral BMD of the lunate fossa was signifi-
cantly higher (p\0.001) than that of the interfossa ridge.
Also, a comparison of the radial half and ulnar half of the
scaphoid fossa revealed the ulnar half of the scaphoid fossa
to have a significantly higher (p = 0.021) BMD than the
radial half of the scaphoid fossa (640 HU) (Fig. 3).
The mean age, height, weight, BMI, and DXA T-scores
(range, 52–88 years), 154.0 cm (range, 138–164 cm),
57.8 kg (range, 42–70 kg), 24.3 (range, 19.9–30.3 kg/m2),
?1.8 (range, ?3.8–0.8) and ?2.7 (range, ?4.8 to ?0.6),
respectively. When correlation of the mean subchondral
the femoral neck and lumbar spine were significant factors
correlated with the mean subchondral BMD (r = 0.61,
p\0.001; r = 0.64, p\0.001, respectively) (Fig. 4). The
subchondral BMD was similar regardless of the socio-
occupational classification and radiographic evidence of
hand osteoarthritis (p = 0.11; p = 0.53) (Table 3).
Several studies on BMD or strength in trabecular or cor-
tical bone of the metaphysis of the distal radius have been
published [11, 24, 34, 36]. However, to our knowledge no
reports have focused on the subchondral plate of the distal
radius. We examined the topographic pattern of the sub-
chondral plate of the distal radius and the correlation
between various clinical factors and subchondral BMD of
the distal radius. We assumed that the subchondral BMD of
the distal radius can be affected by (1) systemic or con-
stitutional factors, which include age, height, weight, BMI,
and T-score measured by DXA at the axial skeleton; and
(2) by local factors that are long-term joint reaction forces
represented indirectly by radiographic evidence of osteo-
arthritis and socio-occupational class.
Our study has several limitations. First, we used CT
osteoabsorptiometry, which resulted in densitometric
Fig. 3 The box-and-whiskers plot shows the average BMDs of four
subareas in the subchondral plate. BMD = bone mineral density.
Fig. 4A–B The scatter diagram shows the correlation between the
(A) femoral neck and (B) lumbar spine. BMD = bone mineral density.
1686 Rhee and BaekClinical Orthopaedics and Related Research1
values in HU. Because the HU is the attenuation coefficient
that is calibrated with reference to water and not an absolute
value, the results produced in HU may present different
leading to a lack of reproducibility in measurement. How-
ever, all subjects were evaluated using an identical CT
scanner under the same conditions. Therefore, the topo-
graphic and correlational analysis in this study would not
have substantial problems. Second, the authors used radio-
graphic evidence of osteoarthritis and socio-occupational
class as indirect indicators of the accumulated intensity of
hand labor and long-term joint reaction force exerted on the
distal radius. Although the criteria of osteoarthritis and hard
manual worker were based on previous studies [6, 25, 39],
this type of dichotomous way of division is somewhat arbi-
trary. Third, the estimated densitometric measurement is the
maximum value among a series of voxels that are located on
the trajectory line because we used the MIP technique. The
MIP appears more reasonable, but such a technique is cur-
rently unavailable. Nevertheless, selecting the maximum
value using MIP will not allow substantial error because the
subchondral plate of the distal radius in the elderly is nor-
mally very thin.
In the quantification, the mean subchondral BMD of the
subjects was 518 HU (range, 360–720 HU). In a previous
study, bone quality was categorized into five classes based
on the Hounsfield unit obtained from a CT scan . In this
classification, the BMD range of 360 to 720 HU, as in our
study, corresponds to the D3 class, which consists of the
porous cortical bone and the fine trabecular bone. Con-
sidering this, the quantified results of our study showed that
the subchondral BMD of the distal radius in postmeno-
pausal women usually corresponds to the interim value
between the BMDs of the cortical and trabecular bones,
and is relatively widely distributed through the range (eg,
360–720 HU), depending on the subjects.
In the topographic analysis, the gross pattern of the
densitometric distribution was assessed and a quantified
comparative analysis was performed by dividing the sub-
chondral plate into four subareas (radial half of the
scaphoid fossa, ulnar half of the scaphoid fossa, interfossa
ridge, and lunate fossa). The subarea division like this was
based on the load-bearing situation of each location, ie, the
ulnar half of the scaphoid fossa and lunate fossa bear the
transarticular (radioscaphoid and radiolunate) load directly
but the interfossa ridge does not bear any direct load and
the radial half of the scaphoid fossa bears a range of loads
depending on the posture of the wrist. Statistically, the
areas of the ulnar half of the scaphoid fossa and lunate
fossa have a significantly higher BMD than the interfossa
ridge, as shown in the gross assessment of each densito-
metric image (Fig. 1). This bicentric pattern of the
subchondral BMD can be explained by the hypothesis that
the transarticular load of the wrist is transmitted mainly by
the radioscaphoid and radiolunate joints and the subchon-
dral plate of the distal radius adapted to this long-standing
mechanical strain. This type of densitometric distribution
corresponds well with studies by Carlson and Patel [4, 28].
However, the subchondral BMD of the ulnar half of the
scaphoid fossa is significantly higher than the radial half of
the scaphoid fossa and lunate fossa, and there was no sta-
tistical difference in subchondral BMD between the radial
half of the scaphoid fossa and the lunate fossa. This sug-
gests the contact area between the proximal pole of the
scaphoid and the ulnar half of the scaphoid fossa is the
primary load-transmitting location, and the radiolunate
joint and radial half of the radioscaphoid joint are the
secondary load-transmitting locations. In addition, this
topographic distribution of BMD has several clinical
implications. First, when intraarticular extension of the
distal radius fracture or lunate die-punch fracture occurs,
the interfossa ridge, with a relatively low BMD, is nor-
mally involved in fractures. Second, when performing
volar plating to a distal radius fracture, locking screws
produced better support on a relatively dense subchondral
portion of the lunate fossa and the ulnar half of the
scaphoid fossa rather than that of the interfossa ridge.
For correlational analysis, several systemic and local
factors were assumed to be the clinical factors with a
Table 3. Correlation of the subchondral bone density with various
Age (years)68 –0.26 0.11
Height (cm) 154.0–0.120.45
24.3 –0.19 0.25
T-score (femur neck)–1.8 0.61
\0.001 T-score (lumbar spine) –2.70.64
Nonmanual worker 310.11
Hard manual worker 49
*Age, height, weight, BMI, and T-scores measured by dual-energy
x-ray absorptiometry at the lumbar spine and femoral neck were
evaluated statistically using Pearson’s correlation model. Comparison
of the subchondral bone density between the groups determined by
the socio-occupational classification and radiographic evidence of
hand osteoarthritis using a Student’s independent t-test and Mann-
Whitney U test, respectively;?hard manual worker group was defined
as class IVc, VIIa, or VIIb in the Erikson-Goldthorpe-Portocarero
scheme ;?osteoarthritis was defined as above Grade II in meta-
carpophalangealand basal joint by Kellgren and Lawrence
classification; BMI = body mass index.
Volume 470, Number 6, June 2012Densitometric Analysis in Postmenopausal Women1687
potential correlation with subchondral BMD. Among the
systemic factors, only the systemic BMD measured in the
T-score by DXA at the lumbar spine and femoral neck was
related to the subchondral BMD. In general, several
anthropometric variables including age, height, weight, and
BMI are believed to be related to systemic osteoporosis in
postmenopausal women despite some debate [27, 30, 37].
However, our study showed such anthropometric variables
do not correlate with the subchondral BMD of the distal
The local factors represented by the radiographic evi-
dence of osteoarthritis and socio-occupational class also
were found not to correlate with the subchondral BMD of
the distal radius. A mechanical load applied to a joint
includes the weightbearing force and joint reaction force
. Because humans are bipedal animals, the weight-
bearing force applied to the wrist can be negligible and
there remains only a joint reaction force that is made from
the muscle-tendon structure. We assessed the accumulated
intensity of hand labor experienced in the past using the
socio-occupational classification and radiographic evidence
of osteoarthritis to objectively determine the long-term
joint reaction force exerted on the distal radius. We used
the scheme described by Erikson et al.  as a socio-
occupational classification and the Kellgren-Lawrence
scale as an osteoarthritis grading system to objectify and
minimize the arbitrariness. The scheme by Erikson et al.
 has been used to evaluate the socioeconomic factors in
a range of disease situations [5, 6, 25], and the Kellgren-
Lawrence scale has been used to evaluate hand osteoar-
thritis and its impact on the functional status in the study by
Zhang et al. . As a result, the intensity of accumulated
hand labor showed no significant relationship with the
subchondral BMD of the distal radius.
These negative correlations can be explained by Frost’s
mechanostat hypothesis [15, 16]. There is a range of strain
that maintains constant bone turnover. The lowest value of
that range is called the minimum effective strain (MES) for
the remodeling threshold. Bone loss progresses when the
strain applied to the bone is less than the MES, whereas
bone gain progresses when the strain is beyond that range.
Because the wrist is not a weightbearing joint in humans,
gravitational factors such as weight or BMI have little
effect on the wrist. In addition, the joint reaction force
caused by accumulated intense hand labor might not reach
the level of the remodeling threshold. Only the systemic
BMD measured in the axial skeleton was found to correlate
with the subchondral BMD of the distal radius, possibly as
a constitutional factor.
We believe our results provide anatomic and clinical
insights regarding the microstructure and mechanical prop-
been relatively undisclosed. Also, the topographic findings
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