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Can Metacarpal Cortical Area Predict the Occurrence

of Hip Fracture in Women and Men Over 3 Decades


of Follow-Up? Results From the Framingham
Osteoporosis Study
DOUGLAS P. KIEL,
1
MARIAN T. HANNAN,
1
KERRY E. BROE,
1
DAVID T. FELSON,
2
and
L. ADRIENNE CUPPLES
3
ABSTRACT
The purpose of this study was to determine if a single measurement of metacarpal cortical area could predict
the subsequent risk of hip fracture over a long-term follow-up period. Thirteen hundred eighty-six women and
1014 men (mean age [SD] 61 8 years) underwent posteroanterior hand radiography between 1966 and
1970 as part of the Framingham Study. Measurements of cortical bone width (external width and medullary
width) were made at the midpoint of the second metacarpal with a digital caliper to the nearest 0.1 mm. Hip
fracture occurrence was ascertained on all survivors through December 1995. Surprisingly, in women, there
was no signicant increase in hip fracture according to metacarpal cortical area measurements (per SD
decrease) in either age-adjusted (hazard ratio [HR] 1.13; 95% CI, 0.941.35) or multivariate-adjusted
models (HR 1.06; 95% CI, 0.881.27). The same results were seen when considering only those women who
were >65 years of age at the time of their X-ray or when considering only the rst 10 years of follow-up. When
the type of hip fracture was considered in women, after adjustment for other risk factors, there appeared to
be an association between metacarpal cortical area and intertrochanteric fracture risk (HR 1.24; 95% CI,
0.911.71) but not femoral neck fracture risk (HR 0.93; 95% CI, 0.711.22). In men, the age-adjusted risk
of hip fracture was increased modestly per SD decrease in metacarpal cortical area (HR 1.38; 95% CI,
1.021.87), and this remained true after adjustment for potential confounders. In this prospective cohort study
with up to 30 years of follow-up, metacarpal cortical area in men predicted hip fracture risk. In women, the
only association between metacarpal cortical area and fracture risk was observed for intertrochanteric
fractures and was not signicant when adjusting for multiple potential confounders. We conclude that this
peripheral measure of bone status is not a potent predictor of hip fracture over a long period of follow-up. (J
Bone Miner Res 2001;16:22602266)
Key words: bone density, hip fractures, cohort study, men, women
INTRODUCTION
A
LTHOUGH IT has been well established that measure-
ments of bone mineral density (BMD) can predict hip
fracture risk, a recent meta-analysis
(1)
suggested that very
few studies have examined the predictive ability of bone
mass measurements made between ages 50 and 60 years to
predict subsequent fracture, nor have there been many stud-
ies in men, in whom fractures are less common. Finally, few
studies have followed participants over long periods of
1
Hebrew Rehabilitation Center for Aged Research and Training Institute and Harvard Medical School Division on Aging, Boston,
Massachusetts, USA.
2
Boston University Arthritis Center, Boston University School of Medicine, Boston, Massachusetts, USA.
3
Department of Epidemiology and Biostatistics, Boston University School of Public Health, Boston, Massachusetts, USA.
JOURNAL OF BONE AND MINERAL RESEARCH
Volume 16, Number 12, 2001
2001 American Society for Bone and Mineral Research
2260
time.
(2)
Thus, there are no large-scale prospective studies
examining the ability of a single assessment of bone status
in middle-aged men and women to predict hip fracture
occurring many years later.
Radiogrammetry, an older technique of measuring bone
status available before the development of modern densito-
metric techniques, has the potential to provide insights into
long-term fracture risk prediction. There have been previous
studies evaluating the role of phalangeal bone density using
photodensitometry,
(3)
as well as the role of metacarpal ra-
diogrammetry.
(4,5)
Generally, the number of hip fractures in
these studies was small, results for men were limited, and
the number of years of follow-up ranged from 14 to 16
years.
Therefore, we analyzed data from a long-standing longi-
tudinal cohort study, the Framingham Heart Study. We
wished to determine the predictive usefulness of metacarpal
cortical area in determining the risk for hip fracture when
measured by radiogrammetry in a group of middle-aged
men and women. We have shown this measurement to be
predictive of breast cancer, colon cancer, and the progres-
sion of vascular calcication.
(68)
MATERIALS AND METHODS
Study population
The Framingham Study began in 1948 with the primary
goal of evaluating risk factors for heart disease in a
population-based sample of the town of Framingham, MA.
The original cohort consisted of 5209 participants who were
2862 years old at the time of the rst examination in
19481951. These individuals (2873 women and 2336
men) have participated in follow-up examinations every 2
years since that time. At each examination, a medical his-
tory is taken and a physical examination and a series of
laboratory tests have been performed.
(9)
Between 1966 and 1970, at the time of biennial exami-
nations 1011, a posteroanterior radiograph of the right
hand was taken as part of an osteoporosis study. Of the 2408
women and 1791 men seen at either of those visits, 1394
and 1018 unsolicited men and women, respectively, under-
went posteroanterior hand radiography. Not all participants
had radiography performed because funding for the original
project in 1967 was limited.
Assessment of bone mass
We used radiogrammetry to measure cortical bone mass
of the second metacarpal on the right hand. We chose the
second metacarpal because it is one of the largest bones of
the hand, has a more constant shape than the other meta-
carpals,
(10)
and is approximately circular at the midshaft,
with the medullary cavity nearly centered in the tubular
bone cylinder.
(10,11)
Two readers who were unaware of the hip fracture status
of the study assessed cortical bone mass according to a
standard protocol. Hand radiographs were placed at on a
lighted viewing box, and measurements of cortical external
width (W) and medullary width (w) were made halfway up
the second metacarpal with a digital caliper. Digital calipers
were calibrated to the nearest 0.01 mm, and measurements
were recorded to the nearest 0.1 mm. To assess intraob-
server and interobserver reliability in the measurement of
cortical width, we gave 25 hand radiographs to each of the
two readers twice for blinded readings. The intraobserver
correlation coefcients for external and medullary width
were 0.99 and 0.94, respectively; the corresponding inter-
observer correlation coefcients were identical. We used the
relative metacarpal cortical area, calculated as 100 (W
2

w
2
) W
2
, as an indicator of bone mass but also examined
combined cortical thickness (W w).
Assessment of hip fracture
Osteoporotic hip fractures were dened as fractures of the
proximal femur occurring as the result of a fall from stand-
ing height or less and not as the result of metastatic cancer
or greater degrees of trauma such as a motor vehicle acci-
dent. Only rst hip fractures occurring after the date of the
radiograph were included. The methods of hip fracture
ascertainment in this cohort have been described in detail
previously.
(12)
Briey, all hip fractures were ascertained
using four sources: chart review completed on all partici-
pants, hospital record reviews, direct questioning of partic-
ipants at biennial examinations from 1988 to 1995, and
telephone contact with participants not attending examina-
tions. Hospital discharge summaries have been used to
conrm fracture in 96% of cases. In the review of hospital
records, the location of the hip fracture is recorded (e.g.,
femoral neck and intertrochanteric). The rates of hip frac-
ture corresponded closely to age-specic rates obtained
from the National Hospital Discharge Survey.
(12)
Other variables
Information was obtained on potential confounders mea-
sured at the time of the radiograph and at previous exams.
Age, weight, and height were taken from the exam at the
time of the radiograph. When this was not available, the
average was taken from the examination before and after
this exam or the closest examination available. Cigarette use
was determined by averaging the number of cigarettes
smoked per day at baseline and previous examinations.
Alcohol consumption, assessed at exam 2 and exam 7, was
determined by averaging the ounces of alcohol consumed
per week at these two assessments (according to a formula
reported by Gordon and Kannel
(13)
). For the 25 participants
missing this information, alcohol information was taken
from the closest examination after the X-ray. In the case of
7 individuals with missing alcohol information, the gender-
specic mean was assigned. Caffeine intake (computed in
units equal to the number of cups of coffee per day 0.5
the number of cups of tea per day) based on previous studies
of caffeine and hip fracture risk
(14)
was based on the average
intake at exam 4 and exam 12 (exams at which caffeine use
was assessed). For subjects with missing caffeine data,
either information from examination 13 was used (2 men
and 5 women) or the gender-specic mean (5 men and 12
women) was used. For estrogen use at the time of the
2261 METACARPAL CORTICAL AREA AND HIP FRACTURE
radiograph, women were categorized into three groups:
never used estrogen, former users, and current users. Be-
cause some of the women included in the analysis had not
yet reached menopause (absence of menstrual periods for 1
year) at the time of the hand radiograph (n 91), we
created a variable that classied women as being postmeno-
pausal or premenopausal. All aspects of this study were
approved by the Boston University Institutional Review
Board.
Statistical analysis
Using t-tests for continuous variables and
2
tests for
categorical variables, we compared the characteristics of the
participants at the time of the baseline hand radiograph
according to whether they later sustained a hip fracture or
not. Incidence of hip fractures per 1000 person-years was
calculated. To examine the association between metacarpal
cortical area and fracture risk, Cox proportional hazards
regression
(15)
was used to model time to fracture, with
censoring due to death, loss to follow-up, or maximal
follow-up time (December 1995). Covariates were included
in proportional hazard models after verifying that the vari-
ables did not violate the proportional hazards assumption.
Models were rst performed for men and women separately.
Metacarpal cortical area was entered into the models as a
continuous variable and as age-specic quartiles. To obtain
better control of age effects, subjects were classied accord-
ing to age-specic quartiles using 2-year age groupings
from age 47 to 80 years. Two models were constructed: age
adjusted, and multivariate adjusted (age, weight, height,
smoking, alcohol intake, caffeine intake, and, for women,
menopause status and estrogen use). Results for fracture risk
were reported as the hazard ratios (HR) with 95% CIs for
each SD decrease in metacarpal cortical area. We also
calculated incidence rates of hip fracture with their SEs
across age-specic quartiles. To determine if the predictive
value of metacarpal cortical area changed with advancing
age at the time of hand radiograph, we performed analyses
stratied into two age groups: 65 years of age and 65
years of age. Finally, to determine if the ability of metacar-
pal cortical area to predict hip fracture differed according to
the type of fracture, we separately examined the risk of
femoral neck fracture and intertrochanteric fracture among
women according to metacarpal cortical area.
RESULTS
Of the 2411 subjects who had hand radiographs, 11 (8
women and 3 men) were not included in this analysis
because of previous hip fracture. This resulted in 1386
women and 1014 men with hand radiographs of whom 162
(6.08/1000 person-years) and 41 (2.38/1000 person-years)
sustained hip fractures, respectively. The median number of
years from the time of the hand X-ray to the time of hip
fracture was 16 years (range, 228 years) for women and 19
years (range, 426 years) for men. As shown in Table 1,
women who had incident hip fractures were older at base-
line, weighed less, and had lower metacarpal cortical width
than women who did not sustain a hip fracture. Men who
fractured were older at baseline and had lower cortical
width than men without hip fracture; however, there were
no other differences.
Surprisingly, in women, there was no signicant increase
in hip fracture according to metacarpal cortical area mea-
surement in either age-adjusted (HR 1.13; 95% CI, 0.94
1.35) or multivariate-adjusted models (HR 1.06; 95% CI,
0.881.27; Table 2). To determine if an association between
metacarpal cortical area and hip fracture risk might be more
apparent in women who were older at the time of baseline
hand X-ray, we stratied analyses into those aged 65
years versus those 65 years of age at the time of hand
X-ray. The ability of cortical area to predict hip fracture risk
was not increased in either age group (HR 1.06; 95% CI,
0.801.42; and HR 1.16; 95% CI, 0.921.46) in the
younger and older age groups, respectively. When we re-
stricted our follow-up to the rst 10 years after hand radio-
graphs, there was still no association between metacarpal
cortical area and the risk of hip fracture. When we repeated
the analyses using combined cortical width (Ww) instead
of metacarpal cortical area, results in men and women were
similar to those using metacarpal cortical area.
When the type of hip fracture was considered in women,
there appeared to be an association between metacarpal
cortical area and intertrochanteric fractures that was only
statistically signicant at the p 0.05 level in the age-
adjusted models (Table 2). Incidence rates across age-
specic quartiles are shown in Fig. 1. In contrast, there were
no suggestions of an association between metacarpal corti-
cal area and femoral neck fractures. There were too few hip
fractures in men to examine types of hip fracture.
In men, the age-adjusted risk of hip fracture was in-
creased modestly per SD decrease in metacarpal cortical
area (HR 1.38; 95% CI, 1.021.87; Table 2), and this
remained true after adjustment for potential confounders.
Hip fracture incidence among men in the lowest quartile of
metacarpal cortical area was 36% higher than among men in
the highest quartile (Fig. 2). The risk ratio for hip fracture
for men in the two lower age-specic quartiles of metacar-
pal cortical area was 2.64 (95% CI, 1.345.21) compared
with men in the two upper quartiles.
DISCUSSION
In this population-based prospective cohort study of men
and women with up to 30 years of follow-up, a single
measurement of metacarpal cortical area had only a very
modest ability to predict later occurrence of hip fracture in
men. In women, metacarpal cortical area was not predictive
of hip fractures overall; however, there was a suggestion
that it may be predictive of intertrochanteric hip fracture but
not femoral neck fracture. To our knowledge, this is the
longest prospective study to examine a peripheral measure-
ment of bone status and the risk of hip fracture and is the
largest study sample of men with such a long follow-up and
large number of hip fractures.
It is well established that measurements of BMD can
predict fracture risk
(1,3,1637)
; however, the majority of stud-
2262 KIEL ET AL.
ies have measured areal BMD, focused on women with
mean age older than our population, and have relatively
short follow-up periods. The longest cohort study reported
in the literature had up to 25 years of follow-up and reported
a relative risk of hip fracture of 1.66 (95% CI, 1.132.46)
per 1 SD decrement in BMD at the forearm at baseline.
(21)
This cohort of 410 women with areal bone mineral mea-
surements made in the early 1970s were followed for all
types of fracture up to 1994. Of the 213 fragility fractures
that occurred during follow-up, 43 were hip fractures. An-
other study of 131 Roman Catholic nuns, almost half of
whom were premenopausal at the time of initial bone mineral
content measurement, recorded 31 incident fractures during
follow-up, and none of the fractures were hip fractures.
The only prospective study in men with long-term
follow-up involved the First National Health and Nutrition
TABLE 1. CHARACTERISTICS OF 1014 MEN AND 1386 WOMEN IN THE FRAMINGHAM STUDY ACCORDING TO THE PRESENCE OR
ABSENCE OF HIP FRACTURE BETWEEN 1966 AND 1995
Characteristics
Women with hip fracture
(n 162; mean SD)
Women without hip fracture
(n 1224; mean SD)
Women
Age at exam of X-ray (year) 65 7.24 60 8.08*
Height at exam of X-ray (in) 62.40 2.78 62.15 2.38
Weight at exam of X-ray (lb) 136.95 19.88 142.96 24.86*
Cortical width (mm) 3.96 0.75 4.25 0.79*
Cigarettes (no/day) 4.63 8.12 5.85 8.76
Alcohol (oz/week) 2.57 4.01 2.44 3.60
Caffeine (2 cups/day) 65% 60%
Menopausal 97% 93%
Estrogen use:
Never 79% 74%
Former 11% 11%
Current 10% 15%
Men with hip fracture
(n 41; mean SD)
Men without hip fracture
(n 973; mean SD)
Men
Age at exam of X-ray (year) 64 7.23 60 7.95*
Height at exam of X-ray (in) 67.46 3.30 67.26 2.69
Weight at exam of X-ray (lb) 170.83 25.35 172.21 25.47
Cortical width (mm) 4.93 0.67 5.22 0.80*
Cigarettes (no/day) 13.64 11.66 11.10 12.31
Alcohol (oz/week) 7.39 6.78 6.43 8.00
Caffeine (2 cups/day) 59% 61%
*p 0.05.
TABLE 2. ASSOCIATION BETWEEN RELATIVE METACARPAL CORTICAL AREA AND ALL HIP FRACTURES, INTERTROCHANTERIC
FRACTURES, AND FEMORAL NECK FRACTURES FOR 1386 WOMEN AND ALL HIP FRACTURES FOR 1014 MEN IN THE
FRAMINGHAM STUDY
Risk ratio for fracture (95% CI)
Age-adjusted Multivariate adjusted*
Womenall hip fractures
Relative metacarpal cortical area (per decrease in SD) 1.13 (0.941.35) 1.06 (0.881.27)
Womenintertrochanteric fracture
Relative metacarpal cortical area (per decrease in SD) 1.34 (0.991.81) 1.24 (0.911.71)
Womenfemoral neck fracture
Relative metacarpal cortical area (per decrease in SD) 1.04 (0.801.35) 0.93 (0.711.22)
Menall hip fractures
Relative metacarpal cortical area (per decrease in SD) 1.38 (1.021.87) 1.42 (1.051.92)
*Adjusted for age, weight, height average ounces of alcohol per week, average number of cigarettes per day, caffeine intake (02
cups/day or 2 cups/day), menopause status, and use of estrogen at exam of X-ray (never, former, or current user).
2263 METACARPAL CORTICAL AREA AND HIP FRACTURE
Examination Survey (NHANES I) and the epidemiologic
follow-up to this study. A subsample of this cohort (n
1437) was followed from the time of the radiographic
absorptiometric assessment of phalangeal bone density in
19711975 for up to 21 years. A total of 26 hip fractures
occurred during follow-up, and the risk of hip fracture
increased by about 70% for each 1 SD decrease in BMD.
This is slightly greater than our estimate of 1.42; however,
the 95% CIs for both estimates overlap with each other.
Thus, there are limited data regarding the predictability of
areal bone density measurements to predict hip fracture in
men and women beyond 20 years. The longest duration
study using absorptiometric methods involved the forearm
site that is largely cortical bone and found that bone density
predicted fragility fractures in general. We also measured
cortical bone in our study and were unable to show an
overall association between cortical width and hip fracture
in women. We conclude that measurements of cortical
width using radiographic morphometry of the metacarpal
are not as useful as radial absorptiometric measurements
although both sites consist of primarily cortical bone.
Whether longer-term follow-up of cohorts who have had
dual-energy absorptiometry (DXA) measurements will
yield results similar to our own is speculative.
Two prospective studies have specically examined the
relation between metacarpal morphometry and hip fracture
risk.
(4,5)
In the rst,
(4)
535 of 771 elderly persons aged 65
years and having had X-rays performed in 19731974 were
able to be traced for the occurrence of hip fracture. Sixteen
hip fractures in women and 7 hip fractures in men occurred
during 14 years of follow-up. Considering men and women
together, metacarpal cortical index tended to predict hip
fracture in this sample (p value for trend 0.08 across
tertiles of metacarpal cortical width). The second study used
data from the NHANES and its three follow-up studies and
found that in 1489 white women followed for an average of
13 years, external cortical width predicted hip fracture.
(5)
Our study differed from these two in several important
ways. First, we had data from a larger cohort of both men
and women, were able to examine longer duration of
follow-up, had complete case ascertainment conrmed by
medical records, and were able to perform gender-specic
analyses as well as looking at the type of hip fracture in
women.
We were surprised that overall, metacarpal cortical area
did not predict hip fracture in women and only modestly
increased risk in men. One possibility is that the ability of a
single measurement of bone mass loses its predictive value
over a long duration of follow-up. However, even when we
restricted our analysis to older women or to the rst 10 years
of follow-up, metacarpal cortical area was still not associ-
ated with an increased risk of fracture. There was a modest
ability to predict intertrochanteric hip fractures compared
with femoral neck fractures. The reasons for the difference
in the ability of a measurement of cortical bone to predict
the two different types of hip fractures are not entirely clear
but have been described by other investigators.
(38,39)
Fur-
thermore, in a study of the structural signicance of cortical
and trabecular bone in the proximal femur, using nite
elements analysis, Lotz and colleagues showed that cortical
bone in the intertrochanteric region carried 80% of the load
during gait and during a fall to the side, compared with only
50% at the midneck.
(40)
In fact, there was a gradual transi-
tion from the femoral head, where the majority of load was
carried by trabecular bone, to the trochanteric region, where
the majority of load was carried by cortical bone. These
ndings may help to explain the ability of cortical bone
measurements to predict intertrochanteric hip fractures bet-
ter than neck fractures. Because the percentage of men
sustaining intertrochanteric hip fractures (51%) was greater
than that in women (39%), this may explain why we were
able to show a signicant association between cortical area
and hip fracture in men but only in women sustaining
intertrochanteric fractures.
Our study also raises questions about the predictive abil-
ity of a single measurement of cortical bone in a peripheral
site to predict hip fracture risk up to 30 years later. Simple
radiogrammetric measurements of the second metacarpal do
not appear to perform as well as other measurements such as
radiographic absorptiometry in the prediction of long-term
hip fracture risk in women. In men, there is a modest
increase in risk for each decrement in metacarpal cortical
area. Because many of the recommendations about bone
densitometry screening are based on short-term follow-up
FIG. 2. Incidence rates (and their SEs) of hip fracture by age-
adjusted quartiles of relative metacarpal cortical area in 1014 men in
the Framingham Study.
FIG. 1. Incidence rates (and their SEs) of intertrochanteric hip frac-
ture by age-adjusted quartiles of relative metacarpal cortical area in
1278 women in the Framingham Study.
2264 KIEL ET AL.
of women of advanced age, further long-term studies such
as this one are needed to be able to evaluate the use of bone
mass testing in middle age to predict late-life fractures of
the hip.
ACKNOWLEDGMENTS
We thank Dr. Harry Genant and Lisa McAllister for their
assistance in the measurement of metacarpal cortical thick-
ness on the hand radiographs. This work was supported in
part by the National Institutes of Health (NIH) grant RO1
AR/AG 41398, and AR 20613; NIH/NHLBI Contract N01-
HC-38038; and an unrestricted grant from Merck Human
Health.
REFERENCES
1. Marshall D, Johnell O, Wedel H 1996 Meta-analysis of how
well measures of bone mineral density predict occurrence of
osteoporotic fractures. BMJ 312:12541259.
2. Stegman MR, Recker RR, Davies KM, Ryan RA, Heaney RP
1992 Fracture risk as determined by prospective and retrospec-
tive study designs. Osteoporos Int 2:290297.
3. Mussolino ME, Looker AC, Madans JH, Edelstein D, Walker
RE, Lydick E, Epstein RS, Yates AJ 1997 Phalangeal bone
density and hip fracture risk. Arch Intern Med 157:433438.
4. Cooper C, Wickham C, Walsh K 1991 Appendicular skeletal
status and hip fracture in the elderly: 14-year prospective data.
Bone 12:361364.
5. Huang Z, Himes JH 1997 Bone mass and subsequent risk of
hip fracture. Epidemiology 8:192195.
6. Zhang Y, Kiel DP, Kreger BE, Cupples LA, Ellison RC,
Dorgan JF, Schatzkin A, Levy D, Felson DT 1997 Bone mass
and the risk of breast cancer among postmenopausal women.
N Engl J Med 336:611617.
7. Zhang Y, Felson DT, Ellison RC, Kreger BE, Schatzkin A,
Dorgan JF, Cupples LA, Levy D, Kiel DP 2001 Bone mass and
the risk of colon cancer among postmenopausal women: The
Framingham Study. Am J Epidemiol 153:3137.
8. Kiel DP, Kauppila LL, Cupples LA, Hannan MT, ODonnell
CJ, Wilson PWF 2001 Bone loss and the progression of aortic
calcication over a 25 year period: The Framingham Study.
Calcif Tissue Int 68:271276.
9. Dawber TR, Meadors GF, Moore FE 1951 Epidemiological
approaches to heart disease: The Framingham Study. Am J
Pub Health 41:279286.
10. Garn S, Rohmann C, Wagner B, Sascoli W 1967 Continuing
bone growth throughout life: A general phenomenon. Am J
Phys Anthropol 26:313317.
11. Garn S, Rohmann C, Nolan P Jr 1964 The developmental
nature of bone changes during aging. In: Birren JE (ed.)
Relations of Development and Aging. Charles C. Thomas,
Springeld, IL, USA, pp. 4161.
12. Kiel DP, Felson DT, Anderson JJ, Wilson PW, Moskowitz
MA 1987 Hip fracture and the use of estrogens in postmeno-
pausal women. The Framingham Study. N Engl J Med 317:
11691174.
13. Gordon T, Kannel WB 1983 Drinking habits and cardiovas-
cular disease: The Framingham Study. Am Heart J 105:667
673.
14. Kiel DP, Felson DT, Hannan MT, Anderson JJ, Wilson PW
1990 Caffeine and the risk of hip fracture: The Framingham
Study. Am J Epidemiol 132:675684.
15. Cox DR 1972 Regression models and lifetables. J R Stat Soc
B34:187220.
16. Schott AM, Cormier C, Hans D, Favier F, Hausherr E,
Dargent-Molina P, Delmas PD, Ribot C, Sebert JL, Breart G,
Meunier PJ 1998 How hip and whole-body bone mineral
density predict hip fracture in elderly women: The EPIDOS
Prospective Study. Osteoporos Int 8:247254.
17. Pluijm SM, Graafmans WC, Bouter LM, Lips P 1999 Ultra-
sound measurements for the prediction of osteoporotic frac-
tures in elderly people. Osteoporos Int 9:550556.
18. Huang C, Ross PD, Wasnich RD 1998 Short-term and long-
term fracture prediction by bone mass measurements: A pro-
spective study. J Bone Miner Res 13:107113.
19. Huang C, Ross PD, Yates AJ, Walker RE, Imose K, Emi K,
Wasnich RD 1998 Prediction of fracture risk by radiographic
absorptiometry and quantitative ultrasound: A prospective
study. Calcif Tissue Int 63:380384.
20. De Laet CE, Van Hout BA, Burger H, Weel AE, Hofman A,
Pols HA 1998 Hip fracture prediction in elderly men and
women: Validation in the Rotterdam study. J Bone Miner Res
13:15871593.
21. Duppe H, Gardsell P, Nilsson B, Johnell O 1997 A single bone
density measurement can predict fractures over 25 years. Cal-
cif Tissue Int 60:171174.
22. Mussolino ME, Looker AC, Madans JH, Langlois JA, Orwoll
ES 1998 Risk factors for hip fracture in white men: The
NHANES I Epidemiologic Follow-up Study. J Bone Miner
Res 13:918924.
23. Gardsell P, Johnell O, Nilsson BE 1991 The predictive value
of bone loss for fragility fractures in women: A longitudinal
study over 15 years. Calcif Tissue Int 49:9094.
24. Gardsell P, Johnell O, Nilsson BE, Gullberg B 1993 Predicting
various fragility fractures in women by forearm bone densi-
tometry: A follow-up study. Calcif Tissue Int 52:348353.
25. Cheng S, Suominen H, Era P, Heikkinen E 1994 Bone density
of the calcaneus and fractures in 75- and 80-year-old men and
women. Osteoporos Int 4:4854.
26. Cummings SR, Black DM, Nevitt MC, Browner WS, Cauley
JA, Genant HK, Mascioli SR, Scott JC, Seeley DG, Steiger P,
Vogt TM, and the Study of Osteoporotic Fractures Research
Group 1990 Appendicular bone density and age predict hip
fracture in women. The Study of Osteoporotic Fractures Re-
search Group. JAMA 263:665668.
27. Cummings SR, Black DM, Nevitt MC, Browner W, Cauley J,
Ensrud K, Genant HK, Palermo L, Scott J, Vogt TM 1993
Bone density at various sites for prediction of hip fractures.
The Study of Osteoporotic Fractures Research Group. Lancet
341:7275.
28. Hui SL, Slemenda CW, Johnston CC Jr 1989 Baseline mea-
surement of bone mass predicts fracture in white women. Ann
Intern Med 111:355361.
29. Lester GE, Anderson JJ, Tylavsky FA, Sutton WR, Stinnett
SS, DeMasi RA, Talmage RV 1990 Update on the use of distal
radial bone density measurements in prediction of hip and
Colles fracture risk. J Orthop Res 8:220226.
30. Melton LJD, Atkinson EJ, OFallon WM, Wahner HW, Riggs
BL 1993 Long-term fracture prediction by bone mineral as-
sessed at different skeletal sites. J Bone Miner Res 8:1227
1233.
31. Nordin BE, Chatterton BE, Walker CJ, Wishart J 1987 The
relation of forearm mineral density to peripheral fractures in
postmenopausal women. Med J Aust 146:300304.
32. Porter RW, Miller CG, Grainger D, Palmer SB 1990 Predic-
tion of hip fracture in elderly women: A prospective study [see
comments]. BMJ 301:638641.
33. Wasnich RD, Ross PD, Davis JW, Vogel JM 1989 A compar-
ison of single and multi-site BMC measurements for assess-
ment of spine fracture probability. J Nucl Med 30:11661171.
34. Wasnich RD, Ross PD, Heilbrun LK, Vogel JM 1987 Selec-
tion of the optimal skeletal site for fracture risk prediction.
Clin Orthop 216:262269.
2265 METACARPAL CORTICAL AREA AND HIP FRACTURE
35. Kelsey JL, Browner WS, Seeley DG, Nevitt MC, Cummings
SR 1992 Risk factors for fractures of the distal forearm and
proximal humerus. The Study of Osteoporotic Fractures Re-
search Group. Am J Epidemiol 135:477489.
36. Ross PD, Davis JW, Epstein RS, Wasnich RD 1991 Pre-
existing fractures and bone mass predict vertebral fracture
incidence in women. Ann Intern Med 114:919923.
37. Cleghorn DB, Polley KJ, Bellon MJ, Chatterton J, Baghurst
PA, Nordin BE 1991 Fracture rates as a function of forearm
mineral density in normal postmenopausal women: Retrospec-
tive and prospective data. Calcif Tissue Int 49:161163.
38. Jergas M, San Valentin R, Black DM, Nevitt M, Palermo L,
Genant HK, Cummings S 1995 Radiogrammetry of the meta-
carpals predicts future hip fracture. A prospective study.
J Bone Miner Res 10:S1;S371.
39. Nevitt MC, Johnell O, Black DM, Ensrud K, Genant HK,
Cummings SR 1994 Bone mineral density predicts non-
spine fractures in very elderly women. Osteoporos Int
4:325331.
40. Lotz JC, Cheal EJ, Hayes WC 1995 Stress distributions within
the proximal femur during gait and falls: Implications for
osteoporotic fracture. Osteoporos Int 5:252261.
Address reprint requests to:
Douglas P. Kiel, M.D., M.P.H.
HRCA Research and Training Institute
1200 Center Street
Boston, MA 02131, USA
Received in original form December 11, 2000; in revised form
April 23, 2001; accepted June 15, 2001.
2266 KIEL ET AL.

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