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JOURNAL OF WOMENS HEALTH

Volume 15, Number 9, 2006


Mary Ann Liebert, Inc.

The Association between Body Mass Index and


Osteoporosis in Patients Referred for a
Bone Mineral Density Examination

KOFI ASOMANING, M.B.Ch.B., M.S.,1 ELIZABETH R. BERTONE-JOHNSON, Sc.D.,2


PHILIP C. NASCA, Ph.D.,2 FREDERICK HOOVEN, Ph.D.,3
and PENELOPE S. PEKOW, Ph.D.2

ABSTRACT

Purpose: Osteoporosis affects 46 million (13%18%) postmenopausal white women in the


United States. Most studies to date on risk factors for osteoporosis have considered body mass
index (BMI) only as a possible confounder. In this study, we assess the direct relationship
between BMI and osteoporosis.
Methods: We conducted a cross-sectional study among women aged 5084 years referred by
their physicians for a bone mineral density (BMD) examination at Baystate Medical Center
between October 1998 and September 2000. BMI was determined prior to the BMD exami-
nation in the clinic. Information on other risk factors was obtained through a mailed ques-
tionnaire. Ordinal logistic regression was used to model the association between BMI and os-
teoporosis, controlling for confounding factors.
Results: BMI was inversely associated with BMD status. After adjustment for age, prior
hormone replacement therapy (HRT) use, and other factors, odds ratios (OR) for low, high,
and obese compared with moderate BMI women were 1.8 (95% CI 1.2-2.7), 0.46 (95% CI 0.29-
0.71), and 0.22 (95% CI 0.14-0.36), respectively, with a significant linear trend (p  0.0001) across
BMI categories. Evaluating BMI as a continuous variable, the odds of bone loss decreased
12% for each unit increase in BMI (OR  0.88, 95% CI 0.85-0.91).
Conclusions: Women with low BMI are at increased risk of osteoporosis. The change in risk
associated with a 1 unit change in BMI (58 lb) is of greater magnitude than most other
modifiable risk factors. To help reduce the risk of osteoporosis, patients should be advised
to maintain a normal weight.

INTRODUCTION density at the hip,1 making it the most common


human bone disease.2 Osteoporosis is character-

I T IS ESTIMATED THAT between 13% and 18% (46


million) of postmenopausal white women in
the United States have osteoporosis, and an ad-
ized by low bone density and microarchitectural
deterioration of bone tissue, leading to bone
fragility and an increased risk of fracture. Osteo-
ditional 30%50% (1317 million) have low bone porotic fractures are the most common and seri-

1Harvard School of Public Health, Boston, Massachusetts.


2Department of Public Health, University of Massachusetts, Amherst, Massachusetts.
3University of Massachusetts Medical School, Shrewsbury, Massachusetts.

1028
ASSOCIATION OF BMI AND OSTEOPOROSIS 1029

ous consequence of osteoporosis and are also an tober 1998 and September 2000. We first excluded
important cause of disability and mortality in el- those with a missing address or invalid address
derly people. or for whom only single BMD scores were
Body mass index (BMI), a measure of body recorded. We then selected 100% of the remain-
composition, may be associated with risk of os- ing osteoporotic women and selected every other
teoporosis.3 Individuals with low BMI typically patient within the normal and osteopenic cate-
have low stores of body fat and lower circulating gories, after sorting women alphabetically to en-
estrogen levels, which help prevent loss of bone sure an adequate number of osteoporotic women
tissue.46 Because body fat also acts as a cushion, in our population.
low BMI may increase the risk of fracture as a re- Questionnaires were mailed to a total of 958 se-
sult of a fall.7,8 lected patients. Respondents were divided into
Limited epidemiological research has been BMD categories based on the T-score from their
done on the direct relationship between BMI and BMD examination, using National Osteoporosis
osteoporosis. Most previous studies have evalu- Foundation and World Health Organization
ated other risk factors, including age, weight, (WHO) definitions.1,21,22 Two BMD measure-
race, maternal history of fractures, use of calcium ments, one at the hip (proximal femur) and one
supplements, and menopausal history,913 and at the lumbar spine, were performed at a single
developed indices based on age and weight (in visit. Osteoporosis was defined as one bone mass
addition to other risk factors) to help identify wo- measurement falling below 2.5 standard devia-
men at risk. The easiest index to calculate is the tions (SD) from the mean for adult women of the
Osteoporosis Self-assessment Tool (OST), which same race. Osteopenia was defined as bone mass
is based on age and weight.14 Dargent-Molina et between 1 and 2.5 SD below the same mean. Nor-
al.15 showed that low weight is predictive of low mal bone density was defined as bone mass mea-
bone mineral density (BMD) (defined as a T-score surement greater than 1 SD below the mean.1,21,22
3.5 in that study). Compared with women If a subject was osteoporotic at either the hip or
with weight 66 kg, women with weight 5966 spine, we classified them as osteoporotic. If they
kg had a 3-fold increase in the risk of low BMD were not osteoporotic at either site but were os-
(crude OR  2.87, 95% CI 1.73-4.74). Other stud- teopenic at least at one site, they were classified
ies14,1620 have shown results of similar magni- as osteopenic. If they were normal at both sites,
tude and direction for weight as a risk factor for they were classified as normal.
osteoporosis. BMI is likely to be more predictive BMD was measured by dual x-ray absorp-
of osteoporosis than weight alone because it ad- tiometry (DXA), a standard bone densitometry
justs for differences in height and is more reflec- study. Measurement of BMD using the DXA ma-
tive of body composition. To examine the associ- chine is the most commonly used and accepted
ation between BMI and osteoporosis, we standard for measuring bone mass.20
conducted a cross-sectional study among patients BMI was assessed by measuring the weight
who had been referred by a physician for a BMD and the height of the patients during their first
examination at Baystate Hospital, a large tertiary referral visit. This was done by a single nurse be-
care hospital in western Massachusetts. fore the BMD examination. Weight was measured
with a standardized weight column scale. Height
was measured with the patient standing and us-
MATERIALS AND METHODS ing a stadiometer. The exact measurement of
height in the elderly person is very difficult to de-
In order to obtain a population at high risk for termine because of frailty and spinal deformity,
osteoporosis and who were capable of accurately but Kirk and Hawke23 have demonstrated that
recalling relevant information, while also mini- using the stadiometer has good agreement with
mizing the number of eligible women who might the more accurate assessments using knee height
be lost to follow-up because they had been insti- or demispan (sternal notch to finger roots with
tutionalized or died between the BMD examina- arms outstretched laterally). We then calculated
tion and questionnaire mailing, subjects were BMI as weight in kilograms divided by height in
limited to women aged 5084. Study participants meters squared.
were selected from among the 1769 patients aged Information on medication use and other risk
5084 who had a BMD examination between Oc- factors for osteoporosis at the time of the BMD
1030 ASOMANING ET AL.

examination was collected through question- model. Factors included in the final model were
naires mailed to study subjects in December 2002. age, use of calcium and vitamin D supplements,
We asked participants to report information on use of HRT and bone active medications (e.g.,
their age, race, education, menopausal status, cig- alendronate, risedronate, calcitonin, and ralox-
arette smoking, use of calcium and vitamin D ifene), and current health status. Other factors
supplements, family history of osteoporosis, evaluated but not included in the final model
medication use, and history of oophrectomy or because they were not associated with either
hysterectomy. The survey did not include any BMI or BMD included race, marital status,
questions on the secondary risk factors for osteo- smoking, and maternal history of osteoporosis
porosis, such as such as prior treatment with or fracture.
steroids, chronic kidney disease, and parathyroid A test for trend over increasing BMI categories
and thyroid disease. The survey was designed was performed where each category median was
specifically for this study and included a number modeled as a continuous variable in the regres-
of questions derived in whole or in part from the sion. We also assessed whether the relationship
Behavioral Risk Factor Surveillance System between BMI and BMD differed in subgroups of
(BRFSS), National Health and Nutritional Exam- participants by stratifying by age group (60 vs.
ination Survey (NHANES), and National Health 60 years old), use of calcium/vitamin D (never
Interview Survey. vs. current or past users), use of HRT (never vs.
The Statistical Analysis System (SAS Institute, current or past users), use of bone active drugs
Cary, NC), version 8.2, was used to complete all (never vs. current or past users), and current
data analyses. We divided women into four cat- health status (excellent/very good/good vs.
egories of BMI: low (19 kg/m2), moderate fair/poor/very poor). Interactions between vari-
(1925), high (2530), and obese (30). Wo- ables and BMI were considered statistically sig-
men were also divided into categories based on nificant if the Wald 2-sided p value for the inter-
levels of other factors potentially associated with action term in the multivariable model was 0.05.
both BMI and BMD, including age, current health
status, and prior use of hormone replacement
therapy (HRT) (Table 1). RESULTS
We evaluated the relationship between risk fac-
tors and BMD categories using the Pearsons chi- Completed questionnaire responses were re-
square test. Ordinal logistic regression analysis ceived from 155 women classified as having os-
was used to model the relationship between BMI teoporosis (60% of eligible participants), 182
and three categories of BMD. The proportional (58%) with osteopenia, and 169 (56%) women
odds logistic model with maximum likelihood es- with normal BMD. Responders and nonrespon-
timate was fit to the ordinal response of BMD cat- ders did not differ by age group, osteoporosis sta-
egory (normal, osteopenia, and osteoporosis), tus, or BMI category. Age, calcium/vitamin D,
and 95% confidence intervals (CI) for the odd ra- HRT, and health status categories appeared sig-
tios (OR) were calculated. Two cumulative logits nificantly different and related to BMD status
were obtained for the three response levels of (Table 1). For women in the oldest age category
normal, osteopenia, and osteoporosis. Hence, the (7584), a lower proportion had normal (7%) or
ORs presented are those comparing osteoporosis osteopenic (16%) rather than osteoporotic (30%)
vs. osteopenia/normal and osteoporosis/osteo- bone density, whereas a reverse trend of more
penia vs. normal status of bone density. The score normal (64%) and fewer osteopenic (33%) and os-
test was used to evaluate the assumption of pro- teoporotic (36%) was observed for women in the
portional odds, and the models were evaluated youngest (5064) category (Table 1). A similar
for goodness of fit. We calculated age-adjusted trend across BMD categories was observed for
ORs using BMI as a categorical variable and also calcium/vitamin D when nonusers were com-
as a continuous variable. pared with users. Among users of HRT, 57% of
We then evaluated the relationship between women had normal BMD status, 48% were os-
BMI and BMD categories, adjusting for the effects teopenic, and 31% were osteoporotic. For non-
of other factors, using backwards stepwise elim- HRT users, the percentages were 43%, 52%, and
ination. We used a cutoff for the Wald statistic of 68% for the same BMD categories.
0.15 to retain a variable in our multivariable Age-adjusted and multivariable ORs showing
ASSOCIATION OF BMI AND OSTEOPOROSIS 1031

TABLE 1. DISTRIBUTION OF RISK FACTORS FOR OSTEOPOROSIS BY BMD CATEGORY:


THE BAYSTATE OSTEOPOROSIS STUDY, 19982000

Normal Osteopenic Osteoporotic


(n  155)b (n  181)b (n  168)b
BMD category n (%) n (%) n (%) p valuea

Age (years) 0.0001


5064 93 (64) 91 (33) 55 (36)
6574 42 (29) 52 (31) 52 (34)
7584 11 (7) 27 (16) 44 (30)
Race 0.11
White/non-Hispanic 136 (91) 154 (88) 135 (83)
Other 13 (9) 22 (12) 27 (17)
Education 0.03
 High school graduate 18 (12) 29 (17) 35 (22)
High school graduate 71 (48) 90 (51) 87 (54)
College graduate 60 (40) 56 (32) 39 (24)
Marital status 0.0001
Married 89 (60) 106 (61) 70 (43)
Divorced, separated, single 39 (26) 36 (20) 34 (21)
Widowed 21 (14) 33 (19) 58 (36)
Maternal history of osteoporosis 0.15
No 61 (39) 68 (46) 53 (43)
Yes 17 (11) 34 (23) 25 (20)
Dont know 77 (40) 79 (31) 90 (37)
Maternal history of fracture 0.02
No 83 (54) 112 (62) 87 (52)
Yes 10 (6) 23 (13) 18 (11)
Dont know 62 (40) 46 (25) 63 (37)
Smoking 0.41
Never 74 (51) 74 (43) 83 (52)
Former 60 (41) 82 (48) 61 (38)
Current 11 (8) 16 (9) 16 (10)
Calcium/vitamin D 0.0001
No 136 (88) 141 (78) 109 (65)
Yes 19 (12) 40 (22) 59 (35)
Bone active drugs 0.01
No 65 (42) 77 (43) 95 (57)
Yes 90 (58) 104 (57) 73 (43)
HRT 0.0001
No 66 (43) 94 (52) 115 (68)
Yes 89 (57) 87 (48) 53 (31)
Lives alone 0.001
No 109 (72) 129 (72) 90 (54)
Yes 41 (28) 52 (28) 76 (46)
Current health status 0.003
Excellent/very good/good 119 (82) 133 (78) 104 (65)
Fair/poor/very poor 27 (18) 38 (22) 55 (35)
ap value derived from chi-square statistics.
bNumbers may not sum to 155 normal, 181 osteopenic, and 168 osteoporotic women because of missing data.

the relationship between BMI and BMD cate- pare osteoporosis vs. osteopenia/normal and os-
gories are presented in Table 2. ORs were deter- teoporosis/osteopenia vs. normal. Adjusted ORs
mined for BMI in categories and as a continuous for low, high, and obese BMI compared with
measure. After adjustment for age, use of cal- women of moderate BMI were 1.76 (95% CI 1.2-
cium/vitamin D, HRT, bone medications, and 2.7), 0.46 (95% CI 0.29-0.71), and 0.22 (95% CI 0.14-
other factors, BMI was inversely associated with 0.36), respectively. The odds of osteopenia/os-
BMD categories, with evidence of a significant teoporosis decreased 12% for each unit increase
linear trend (p  0.0001). The ORs presented com- in BMI (OR  0.88, 95% CI 0.85-0.91).
1032 ASOMANING ET AL.

TABLE 2. AGE-ADJUSTED AND MULTIVARIATE ODDS RATIO

Age-adjusted Multivariate
BMI category n ORa ORb 95% CI

BMI
Low (19 kg/m2) 22 3.06 1.76 1.16, 2.68
Moderate (1925) 192 1.00 1.00
High (2530) 166 0.54 0.46 0.29, 0.71
Obese (30) 123 0.28 0.22 0.14, 0.36
0.0001*
BMI (continuous, kg/m2) 505 0.90 0.88 0.85, 0.91
aSingle odds ratios estimate for two cumulative logits of osteoporosis vs. osteopenia/

normal and osteoporosis/osteopenia vs. normal for BMI.


bAdjusted for age (5064, 6574, 7584), prior use of calcium/vitamin D (yes, no), prior

use of HRT (yes, no), prior use of bone active drug (yes, no), and current health status
(excellent/very good/good, fair/poor/very poor).
*p value for trend using category medians as a continuous variable in the regression
model.

Analyses stratified by age group, current In our study, each one unit increase in BMI was
health status, and prior use of calcium/vitamin associated with a significant 12% decrease in risk.
D, HRT, or bone active drugs did not suggest that This is consistent with results obtained by Nitzan-
the BMI-BMD association varied over levels of Kaluski et al.,25 who reported a significant 8% de-
these factors, and no interaction term was signif- crease with each one unit increase in BMI. Simi-
icant (p  0.05) when added to the final model. larly, Munasinghe et al.26 observed that women
with osteoporosis had lower BMI compared with
patients with normal BMD (23.7 vs. 28.5 kg/m2,
DISCUSSION p  0.001).
As with other studies,3,10,13,14,1628 results from
In this cross-sectional study of women referred our analysis suggest that the proportion of wo-
for a BMD examination, we observed that women men with bone loss increases with age, with a 4-
with a lower BMI have a significantly higher risk fold higher risk of bone loss in women age 75
of osteoporosis compared with normal weight compared with those 5064 years (data not
women. This association persisted after control- shown). In elderly women, this is explained by a
ling for age, current health status, and prior use gradual loss of BMD, often referred to as age-re-
of calcium/vitamin D, HRT, and bone active lated or senile bone loss, which starts in midlife29
drugs. BMI appears to have the strongest associ- and continues over time. Bone loss occurs more
ation with BMD in this population. rapidly in women in the early years after meno-
Two mechanisms have been proposed to ex- pause. Women who have been postmenopausal
plain how body mass may affect osteoporosis and for more than 5 years lose BMD at a rate of 1%2%
risk of fracture. It has been suggested that body fat per year. The relative amount lost by women dur-
provides an indirect protection from bone loss by ing their 70s is greater than during their 60s, al-
providing a source and depot for the peripheral though the rate of loss decreases.30 Maintaining
conversion of androstenedione to the metaboli- a healthy body mass and not becoming under-
cally active estrogen, estrone.5,6,24 When this es- weight may help reduce the effects of aging on
trogen depot is deficient, there is an increase in the BMD loss.
rate of bone turnover, which results in a faster rates BMI is likely to be a better predictor of osteo-
of bone loss.58 The second potential mechanism porosis than weight alone, as it more accurately
suggests that in early adulthood, heavy individu- measures body composition. In our study, the ini-
als tend to reach a higher peak BMD than thinner tial medical record review did not provide the in-
individuals and exert a greater load on their dividual heights and weights (only the calculated
weight-bearing joints, leading to the development BMI), and we are unable to compare results for
of higher BMD.24 Such heavy individuals are less BMI and weight in our population. We used a sin-
likely to be osteoporotic in their old age. gle measurement of BMI assessed at the same
ASSOCIATION OF BMI AND OSTEOPOROSIS 1033

time as BMD to classify subjects in terms of body osteoporosis in postmenopausal women who are
composition. A single measurement may not be underweight. Interventions are also suggested that
representative of long-term body composition, will enable these patients to build and maintain
does not allow us to evaluate the effects of BMI bone density. Additional advice on changes to
in early adulthood or weight loss or gain over make to reduce the risk of fracture include exer-
time, and may contribute to misclassification. cise to improve balance and lower body strength
Any such misclassification is likely to be nondif- and the removal of home hazards to make the liv-
ferential, and the effect of such a bias will be to ing area safer. Although obesity or excessive
underestimate the true relationship between BMI weight gain should not be recommended as a strat-
and bone density. We were unable to assess the egy to maintain bone density, the strong relation
reason women were referred for a BMD exami- of low bone density with low BMI underlies the
nation. Referred populations may include a large importance of elderly patients not becoming un-
proportion of patients with previously recog- derweight as far as bone density is concerned.
nized risk factors for osteoporosis or other dis-
eases associated with osteoporosis. They could
have been referred for screening for low bone ACKNOWLEDGMENTS
density prior to treatment or for follow-up of
treatment. This could affect the impact and in- We are indebted to Stephen Gehlbach, M.D.,
terpretation of use of therapies, such as cal- M.P.H., for his support of this research. We
cium/vitamin D, HRT, or bone active medica- would also like to acknowledge the assistance of
tions, on bone density status. Information on the Department of Healthcare Quality, Baystate
other exposures, such as maternal history of frac- Health Systems, in completing this study.
ture or osteoporosis, smoking status, and use of
bone active drugs, was collected by self-report
without corroboration from medical records or
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