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cohort of 4292 women over the age of 70, who
were followed for 2 years
4
. During that time,
330 fractures occurred, including 125 risk factors
and 51 hip fractures. The only significant factors
which showed an excess odds ratio (OR) were
previous fracture (OR 2.67, 95% confidence
interval (CI) 2.10–3.40), a fall in the previous 12
months (OR 2.06, 95% CI 1.63–2.59) and
increased age (OR per year increase 1.03, 95%
CI 1.01–1.05). The authors examined separately
significant factors for hip fracture and wrist frac-
ture, and the only factors that were consistent
across both subgroups were previous fracture,
with odds ratios of around 2.3, and falling in the
previous 12 months, which showed ratios of
between 1.6 and 2.92. Age was only a significant
risk factor for hip fracture, as was low body
weight
4
.
Colles’ fractures
Larger studies have reported on the risk factors
for specific fractures. The Study of Osteoporotic
Fractures (SOF) database has been examined to
determine specific factors for Colles’ fracture,
with 527 cases occurring during a follow-up of
9.8 years. Here the relative risk of wrist fracture
was increased: by 80% in those who had decreased
forearm BMD (per 0.1 g/cm
2
); in those who had
recurrent falls, where the increased risk was 60%
compared with subjects who had no falls; and in
those with previous fracture since the age of 50,
Table 2 Predictors for all fractures from the OFELY (Os des Femmes de Lyon) study
3
Variable OR 95% CI p Value
Fracture after age 45 3.33 1.42–7.79 0.006
Total hip BMD ≤ 0.736 g/cm
2
3.15 1.75–5.66 0.001
Physical activity score ≤ 14 2.08 1.17–3.69 0.01
Grip strength ≤ 60 bar 2.05 1.15–3.64 0.01
Age ≥ 65 1.90 1.04–3.47 0.04
Maternal history of fragility fracture 1.77 1.01–3.09 0.04
Past falls 1.76 1.00–3.09 0.05
BMD, bone mineral density; OR, odds ratio; CI, confidence interval
104
Table 1 Risk factors for fracture which are dependent or partially or completely independent of bone mineral
density (BMD). Adapted from reference 2
BMD-related Partly or completely BMD-independent
Female gender age
BMD Asian or Caucasian race
Premature menopause vitamin D deficiency
Primary or secondary amenorrhea cigarette smoking
Prolonged immobilization excessive alcohol consumption
Low dietary calcium intake neuromuscular disorders
family history of hip fracture
poor visual acuity
previous fragility fracture
glucocorticoid therapy
low body weight
high bone turnover
POSTMENOPAUSAL OSTEOPOROSIS
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New risk factors for hip fracture have recently
been described. It is recognized that patients
with homocystinuria have increased skeletal
deformities and osteoporosis
7
. In the Framing-
ham study, in the female population where fol-
low-up was 15 years, patients with a baseline
homocysteine level in the highest quartile of the
population range had a highly significant 90%
increase in hip fracture, compared with those
with the lowest quartile homocysteine levels
8
. In
a study from The Netherlands, three separate
cohorts were also shown to have significantly
increased risk of hip fracture if their serum
homocysteine level was in the highest quartile of
the normative range, compared with the lowest
quartile
9
. In the largest cohort from this study
followed for 8.1 years, the highest quartile had a
doubling of the fracture risk
10
.
A further factor associated with fractures is
increased levels of vitamin A or retinol, which are
present in many foods including liver, kidney and
milk. High levels of retinol stimulate osteoclast
activity and increase bone resorption, and also
increase periosteal bone formation
7
. In a recent
105
where there was a 30% increased risk
5
. Current
oral estrogen reduced the chance of Colles’ frac-
ture by 40%
5
.
Hip fractures
The often quoted work of Cummings from the
Study of Osteoporotic Fractures (SOF) demon-
strated comprehensively how multiple significant
risk factors contribute to hip fracture risk (Table
3). Eleven separate factors increased risk, while
two factors (weight gain and walking for exer-
cise) reduced the risk
6
. In their article, Cum-
mings and colleagues described almost for the
first time how combinations of risk factors plus
low calcaneal bone density could increase risk of
fracture exponentially when considered together.
For example, calcaneal BMD in the lowest third
of the normal range associated with the presence
of more than five risk factors increased the risk of
hip fracture about 25-fold, when compared with
those with calcaneal bone density in the highest
third of the normative range and with 0–2 risk
factors
6
.
Table 3 Risk factors for hip fractures from the Study of Osteoporotic Fractures
6
Factor Relative risk 95% CI
Relative deficit
Age (per 5-year increase) 1.5 1.3–1.7
History of maternal hip fracture 2.0 1.4–2.9
Height at age 25 (per 6 cm) 1.2 1.1–1.4
Self-related health (per 1 point decrease)
*
1.7 1.3–2.2
History of hyperthyroidism 1.8 1.2–2.6
Current use of long-acting benzodiazepines 1.6 1.1–2.4
Current use of anticonvulsants 2.8 1.2–6.3
Current caffeine intake (per 190 mg/day) 1.3 1.0–1.5
On feet less than 4 h/day 1.7 1.2–2.4
Inability to rise from chair 2.1 1.3–3.2
Lowest quartile for distance depth perception 1.5 1.1–2.0
Low frequency contrast sensitivity (1 SD decrease) 1.2 1.0–1.5
Resting pulse > 80 beats/min 1.8 1.3–2.5
Relative benefit
Increase in weight since age 25 (per 20%) gain 0.6 0.5–0.7
Walking for exercise 0.7 0.5–0.9
*
Health was rated as poor (1 point), fair (2 points), or good to excellent (3 points); CI, confidence interval
DIAGNOSIS: CLINICAL, HORMONAL AND BIOCHEMICAL EVALUATION
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CLINICAL RISK FACTORS FOR
OSTEOPOROSIS
The multiple risk factors associated with low
BMD have been examined and described as part
of guidelines preparation in both the UK
14
and
the USA
15
as the indicators allowed for bone
density assessment. The similarities and differ-
ences between these guidelines can be seen in
Table 4. As will be appreciated, the conceptual
approach between the UK and North American
guidelines differs fundamentally, and this will
give rise to differences in the populations that
can be identified for assessment and, thus, treat-
ment
16
. The validity of the Royal College of
Physicians criteria for the diagnosis of osteoporo-
sis has recently been described by Kayan and col-
leagues
17
, and compared with population norms.
The presence of an indication as approved by the
Royal College of Physicians guidelines for bone
density measurement is associated with approxi-
mately half a standard deviation difference in
bone density. The strongest association with
bone density is radiological osteopenia, followed
by estrogen lack, presence of secondary disorders
and previous fracture. The use of corticosteroids
in referred patients did not increase the risk of
osteoporosis, compared with the population
norm, nor did kyphosis, although it was not clear
whether the kyphotic patients also had vertebral
fractures. Nevertheless, these criteria performed
rather better than non-Royal College of Physi-
cians criteria, such as perimenopausal women,
those with back pain and those who were treated
Table 4 Risk factors for osteoporosis approved as indications for bone mineral density measurement
Royal College of Physicians, UK
14
National Osteoporosis Foundation
15
Radiographic osteopenia All women aged 65 and older regardless of risk factors
Vertebral deformity Younger postmenopausal women with one or more risk factors
Previous fragility fracture Postmenopausal women who present with fractures
Prolonged corticosteroids
Premature menopause
Prolonged amenorrhea
Primary hypogonadism
Other diseases associated with osteoporosis
Maternal history of hip fracture
Low body mass index (<19 kg/m
2
)
POSTMENOPAUSAL OSTEOPOROSIS
study, those who had the highest quintile of vita-
min A intake amounting to more than 3 mg per
day had an increased relative risk of hip fracture,
compared with those of the lowest quintile, of
almost 50% (95% CI 1.05–2.07)
10
, and at least
in men higher serum retinol levels are associated
with excess fracture risk
11
.
Vertebral fractures
A recent study from van der Klift and col-
leagues
12
reported the risk factors for vertebral
fracture in a 6.3-year follow-up of 1624 women
aged more than or equal to 55, in whom 113
morphometric vertebral fractures were detected.
The significant positive clinical risk factors lead-
ing to excess risk of morphometric fractures
included body mass index, walking-aid use, age
at menopause and current smoker; the most
prominent clinical risk factor for vertebral frac-
ture was a prevalent vertebral fracture, where
relative risk rose by over 500% compared with
no prevalent fracture. Bone density was also pre-
dictive of fracture, with a one-standard-
deviation reduction in either lumbar spine or
femoral neck BMD being associated with an
almost doubling of risk
12
. The only significant
clinical risk factors for incident vertebral
fracture in the small number of only 34 cases as
recently reported by Papaioannou and col-
leagues
13
were femoral neck BMD and the phys-
ical functioning domain of the Short Form 36-
item (SF-36) questionnaire.
106
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without densitometry, where the bone density
was on average more than one standard deviation
above the age-matched mean
17
.
Diseases and medications associated
with osteoporosis
There are multiple medications, including gluco-
corticoids, gonadotropin releasing hormone
antagonists, methotrexate, heparin and warfarin,
that have all been associated with low bone den-
sity. These drugs and their associated disorders
are listed in Table 5. As will be noted, they
include hereditary skeletal and connective tissue
diseases, endocrine and metabolic disorders, mar-
row disease including multiple myeloma, sys-
temic lupus erythematosus (SLE) and rheu-
matoid arthritis. There are also a number of
miscellaneous conditions, which include renal
insufficiency and chronic hepatic disease.
Recently, further evidence has become available
that disorders such as celiac disease
18
, Crohn’s
disease
19
, peptic ulcer disease
20
and breast cancer
treated with the aromatase inhibitor
21
are all
associated with low bone density, and some
disorders may also be associated with fracture.
Even patients who have already had a fall and
who have two or more risk factors have been
found to have increased incidence of osteoporo-
sis
22
, although this may simply be due to frailty.
Risk factor scores
This bewildering complex list of risk factors for
fracture or low bone density has led to the devel-
opment of assessment tools that combine many
of these risk factors in a single score, which could
be used to identify those individuals either who
should have bone density testing or, in some
cases, who are considered to be at such risk as to
indicate the need for treatment directly. One of
the most prominent of these indexes, which has
been widely used, is the fracture index, as
described by Black and colleagues
23
. A high-risk
score of between 5 and 9 using the index is asso-
ciated with a 5-year hip fracture risk of 8.2%
without BMD as a risk factor, and adding BMD
only marginally increases the fracture risk pre-
diction at the hip. Similar data were described by
Black and colleagues for non-vertebral and ver-
Table 5 Medications and diseases associated with secondary osteoporosis
Medications
Glucocorticoids, gonadotropin releasing hormone agonists, loop diuretics, methotrexate, thyroid replacement,
heparin, depo-medroxyprogesterone acetate, anti-neoplastic agents, cyclosporin
Hereditary skeletal/connective tissue diseases
Osteogenesis imperfecta, rickets, hypophosphatasia, Marfan's syndrome
Endocrine and metabolic
Hypogonadism, hyperparathyroidism, hyperthyroidism, Cushing syndrome, acidosis, Gaucher's disease,
hemochromatosis, insulin-dependent diabetes, androgen insensitivity
Marrow diseases
Myeloma, mastocytosis, thalassemia, leukemia
Rheumatologic diseases
Systemic lupus, ankylosing spondylitis, rheumatoid arthritis
Miscellaneous
Renal insufficiency, hypercalciuria, chronic hepatic disease, chronic obstructive pulmonary disease, depression,
spinal cord injury, anorexia nervosa, malabsorption or malnutrition, cystic fibrosis, organ transplantation,
pregnancy
New causes
Coeliac disease, peptic ulcer, Crohns’ disease, breast cancer treated with aromatase inhibitor
DIAGNOSIS: CLINICAL, HORMONAL AND BIOCHEMICAL EVALUATION
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POSTMENOPAUSAL OSTEOPOROSIS
tebral fractures, where again fracture risk
increased only slightly by the addition of BMD
as a risk factor in the SOF study population
23
.
A number of other instruments have been
derived in an attempt to detect those who will
have low bone mineral density with increased
specificity and sensitivity, compared with the
simple one-off risk factors as described in the
Royal College of Physicians and the National
Osteoporosis Foundation guidelines. The sensi-
tivity and specificity of these composite risk fac-
tor scores have been compared and contrasted in
a recent publication
24
. Overall, these scores have
a high sensitivity of around 90% in detecting
those who have low bone density, but somewhat
conservative specificity of no more than 50%
indicating that many people with low bone den-
sity will be missed by using composite risk
scores.
BIOCHEMICAL AND HORMONAL
TESTING
In subjects who have presented with osteoporosis
or indeed fracture, biochemical and hormonal
testing is mainly used to detect secondary osteo-
porosis. The indications for testing and the tests
used are described in Table 6, and have been
described previously in guidelines
14,25
.
USE OF BONE TURNOVER
MARKERS
Bone turnover markers have been derived to
reflect both bone resorption and bone formation.
Formation markers can arise from matrix pro-
teins such as osteocalcin or the procollagen type
I propeptide from the C-terminal (PICP) or the
N-terminal (PINP), or can be enzymatic such as
the bone isoform of alkaline phosphatase.
Resorption markers are derived from either
collagen type I degradation, specifically the
pyridinium cross-links of collagen from the C- or
N-telopeptide region (CTX, NTX), or the cross-
link protein, deoxypyridinoline (DPD). An enzy-
matic-derived bone marker associated with bone
resorption is tartrate-resistant acid phosphatase
type 5. These markers can be used in a variety of
situations.
They have been used to predict spine bone
loss where, in the individual patient, they have
only moderate correlations with change in bone
mineral density explaining just over 40% of the
variability, rather similar to that explained by
years since the menopause
26
. Perhaps a more
promising use of the markers, however, is to
enhance the predictive capacity of bone density
for risk of hip or other fractures. Garnero and
colleagues demonstrated in the EPIDOS
(Epidémiologie de l’Ostéoporose) study that the
risk of hip fracture with low hip bone density was
increased 2.9-fold, while, if subjects had baseline
urinary CTX above the upper limit of the young
normal range, they had an increased risk of just
over 2, and if both factors were combined the
increased risk rose to around 4
27
. Kanis and asso-
ciates proposed that including measurement of
markers in a 10-year risk factor assessment for
hip fracture would lead to a substantial increase
in the relative risk of those who had a combina-
tion of low BMD, high CTX and a prior fracture,
108
Table 6 Biochemical and hormonal tests used in the
assessment of osteoporosis
Hematological disease and malignancy
Full blood count, erythrocyte sedimentation rate
(ESR) or C-reactive protein (CRP)
Serum protein electrophoresis ± urinary
Bence-Jones proteins
Chronic liver disease
Liver function tests – albumin, aspartate
aminotransferase (AST), gamma glutamyl
transferase (γGT)
Metabolic bone diseases
Serum calcium, phosphate, alkaline phosphatase
Chronic renal disease and malabsorption
Serum creatinine
Antiendomysial antibody
Endocrine disease
Serum thyroid stimulating hormone (TSH),
parathyroid hormone (PTH), 25OH vitamin D
Serum estradiol, follicle stimulating hormone (FSH),
testosterone, sex hormone binding globulin (SHBG)
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DIAGNOSIS: CLINICAL, HORMONAL AND BIOCHEMICAL EVALUATION
increasing the 10-year probability to over 50% if
all three markers were present
28
.
Use of bone markers to diagnose
osteoporosis
Bone turnover markers are increased in only
about 25% of women with postmenopausal
osteoporosis, and hence cannot be used for
diagnosis. Nor have bone markers been proved
to be useful in a selection of patients who would
effectively receive antifracture treatment. Seibel
and colleagues have recently shown that bisphos-
phonates are effective at all levels of bone
turnover in preventing fractures
29
. However, a
high level of bone turnover may indicate the
presence of secondary osteoporosis, such as in
Paget’s disease, secondary hyperparathyroidism,
primary hyperparathyroidism, thyrotoxicosis or
even hypogonadism. It may also be high in
patients with malignancy or in those who have
suffered a recent fracture. On the other hand,
Cushing’s syndrome will be associated with low
osteocalcin levels, and osteogenesis imperfecta
with low PICP
30
.
MONITORING OF TREATMENT
Bone turnover markers have an increasing role in
this situation. It is important to identify non-
responders to hormone replacement therapy
(HRT), for example, as any errors in dosing
instructions can then be considered. Further, the
detection of non-response could lead the clinician
to consider secondary osteoporosis or to change
treatment. Also, bone turnover markers have
been used to encourage adherence with therapy
31
.
Changes in biochemical markers are usually
large, and occur more rapidly than changes in
bone mineral density. Further, an increase in
bone density only explains 4% of the antifracture
efficacy with raloxifene
32
, 17% with alend-
ronate
33
and up to 28% with risedronate
34
. In
contrast, changes in urinary NTX or CTX may
explain as much as two-thirds of vertebral frac-
ture reduction
34
.
CONCLUSIONS
Risk factors are multiple, but can be used in con-
junction with bone mineral density measure-
ments and possibly bone markers to assist in pre-
diction of the risk of incident fractures. The most
persistent risk factors for fracture at all sites are
age and previous fracture, with risk of falls a signif-
icant risk factor for hip and wrist fractures. Bio-
chemical and hormonal testing should be used to
exclude secondary osteoporosis, while bone
turnover markers may be used soon to monitor
therapy. However, to date, the only risk factor
that has been shown to be a suitable target for
effective treatment is bone mineral density.
109
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INTRODUCTION
More than standard bone densitometry
1
, non-
invasive and/or non-destructive techniques are
capable of providing macro- or microstructural
information about bone
2
. While bone densito-
metry provides important information about
osteoporotic fracture risk, numerous studies indi-
cate that bone strength is only partially
explained by bone mineral density (BMD).
Quantitative assessment of macrostructural char-
acteristics such as geometry, and microstructural
features such as relative trabecular volume, tra-
becular spacing and connectivity, may improve
our ability to estimate bone strength.
The methods available for quantitatively
assessing macrostructure include computed
tomography and, particularly, volumetric quan-
titative computed tomography (vQCT). Non-
invasive and/or non-destructive methods for
assessing the microstructure of trabecular bone
include high-resolution computed tomography
(hrCT), micro-computed tomography (
µCT),
high-resolution magnetic resonance (hrMR) and
micro-magnetic resonance (
µMR). Volumetric
QCT, hrCT and hrMR are generally applicable in
vivo, while
µCT and µMR are principally applica-
ble in vitro.
VOLUMETRIC COMPUTED
TOMOGRAPHY
The use of standard QCT has centered on two-
dimensional characterization of vertebral trabec-
ular bone, but there is also interest in developing
three-dimensional, or vQCT, techniques to
improve spinal measurements and to extend
QCT assessments to the proximal femur. These
three-dimensional techniques encompass the
entire object of interest with stacked slices or
spiral CT scans, and can use anatomic landmarks
to define coordinate systems automatically for
reformatting CT data into anatomically relevant
projections.
Volumetric CT (Figure 1) can determine bone
mineral content (BMC) or BMD of the entire
bone or subregion, such as a vertebral body or
femoral neck, as well as provide separate analysis
of the trabecular or cortical components. Since a
true and highly accurate volumetric rendering is
provided, important geometrical and bio-
mechanically relevant assessments such as cross-
sectional moment of inertia and finite element
Advanced imaging assessment of bone quality
H. K. Genant and Y. Jiang
13
Figure 1 Volumetric quantitative computed
tomography (QCT) of the spine may be used to
analyze bone mineral density in bone compartments
and to measure accurately vertebral geometry.
Courtesy of Thomas Lang
113
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