Download Determining the Prevalence of Osteoporosis and Related Factors

Vol. 161, No. 9
Printed in U.S.A.
DOI: 10.1093/aje/kwi105
American Journal of Epidemiology
Copyright ª 2005 by the Johns Hopkins Bloomberg School of Public Health
All rights reserved
Determining the Prevalence of Osteoporosis and Related Factors using
Quantitative Ultrasound in Vietnamese Adult Women
Vu Thi Thu Hien1,2, Nguyen Cong Khan2, Nguyen Thi Lam2, Le Bach Mai2, DucSon NguyenTrung
Le1,3, Bui Thi Nhung1,2, Masayo Nakamori1, Daisuke Kunii1, Tohru Sakai1, and Shigeru
Yamamoto1
1
Division of International Public Health Nutrition, Institute of Health Biosciences, University of Tokushima Graduate School,
Tokushima, Japan.
2
Vietnam National Institute of Nutrition, Hanoi, Vietnam.
3
Nutrition Center of Ho Chi Minh City, Ho Chi Minh City, Vietnam.
Received for publication June 30, 2004; accepted for publication December 6, 2004.
In 2003, the authors conducted a population-based, cross-sectional survey to determine the prevalence of
osteoporosis and related factors in Vietnamese adult women by using quantitative ultrasound at the heel bone
(calcaneus). A total of 2,232 adult women aged 20 years, living in Hanoi City, and free of illnesses affecting bone
metabolism were randomly selected to participate in the study. Subjects’ bone mass was assessed by speed of
sound at the calcaneus, referred to as quantitative ultrasound measurement. The T-score threshold, defined
as 1.8, was used to identify subjects with osteoporosis. The crude prevalence of osteoporosis in Hanoi City
was 15.4%; after adjustment for age, it was 9.0%. Among premenopausal women, the crude prevalence of
osteoporosis was higher in the urban areas compared with the rural areas. By contrast, postmenopausal women
in the rural areas had a higher prevalence of osteoporosis. Multiple logistic regression analysis revealed that
factors associated with low speed of sound were age, menopause, educational level, lifelong occupation,
recreational weight-bearing exercise, number of births, and height. Results suggest that osteoporosis is
a noteworthy problem in Vietnam, and intervention strategies should be considered to control it, especially in
high-risk populations.
cross-sectional studies; osteoporosis; risk factors; ultrasonics; Vietnam
Abbreviation: QUS, quantitative ultrasound.
Osteoporosis is a growing health problem recognized in
both developed and developing countries (1). Osteoporotic
fractures, especially hip fractures, are related to considerable mortality and increasingly higher costs of health care.
The increasing prevalence of osteoporosis related to more
peripheral and vertebral fractures will lead to increased
socioeconomic burdens because of the high cost of treatment (2, 3). Thus, for the purposes of prevention and
control, there is great interest in conducting epidemiologic
surveys of the prevalence of osteoporosis and related risk
factors in communities (2–4).
The optimal method for diagnosing osteoporosis is to
measure bone mineral density by dual-energy x-ray absorp-
tiometry at the hip and lumbar spine (5). However, it is very
difficult to apply this procedure in community-based studies
because of its lack of portability and its cost. Furthermore,
the procedure exposes subjects to low, but significant doses
of ionizing radiation. Quantitative ultrasound (QUS) measurement, a technique for measuring the peripheral skeleton,
has been proposed because it can be performed quickly, is
relatively inexpensive, is portable, and involves less radiation. Thus, QUS could be an ideal tool to screen for
osteoporosis at the community level (6–12).
Although Asians are thought to have lower bone mass
than Caucasians because of their smaller body size (13), few
population-based studies have been conducted in Asian
Reprint requests to Dr. Shigeru Yamamoto, Division of International Public Health Nutrition, Institute of Health Biosciences, University of
Tokushima Graduate School, 3 Kuramoto, Tokushima, 770-8503 Japan (e-mail: [email protected]).
824
Am J Epidemiol 2005;161:824–830
Osteoporosis in Vietnamese Women
countries. In Vietnam, life expectancy is increasing as the
economy improves (14), and, with a longer lifespan, there is
concern about an increased prevalence of osteoporosis.
However, the prevalence of osteoporosis and its related
factors remains unclear. A pilot study in 2000 measuring the
bone mass of Vietnamese adult men and women living in
Hanoi City estimated that bone density is low in this
population (15). However, data were insufficient to characterize the prevalence. Thus, further studies on the epidemiologic distribution of osteoporosis and associated factors
in Vietnam are required. Although osteoporosis can affect
both men and women of any age, women are four times
more likely than men to develop osteoporosis (16). Thus, the
aim of the present study was to determine the prevalence
of osteoporosis and related factors in Vietnamese adult
women.
MATERIALS AND METHODS
Setting and study subjects
This study was approved by the Research and Ethical
Committee of the Vietnamese National Institute of Nutrition. It was conducted in Hanoi City from April to May
2003.
Hanoi City is the capital of Vietnam, located in the
northern area of the country, and has a population of
approximately 3 million inhabitants (17). There are 228
wards and communes divided into 102 urban wards and 126
rural communes. A multistage sampling method was used to
select subjects. First, 30 of the total 228 wards and
communes were chosen by using a probability proportional-to-size sampling method (18). From each of the
selected wards and communes, 80 women aged 20 years or
older were chosen randomly and were stratified by 5-year
age groups (20–24, 25–29, 30–34, 35–39, 40–44, 45–49,
50–54, 55–59, 60–64, 65–69, 70–74, 75–79, 80–84, and
85 years). To recruit subjects, a list of all families that
included women aged 20 years or older was constructed,
and family codes were created. From this list, the first family
was selected by randomly choosing a family code. In each
family selected, all women aged 20 years or older and free
of bone deformities and acute illnesses were invited to
participate. After selecting the first family, we used the
‘‘random walking’’ method to approach other families,
adding subjects to obtain 80 women stratified by 5-year
age groups (18). From 30 selected wards and communes,
2,400 women were selected to participate.
This survey was carried out at the local health centers of
the selected sites. To maximize participation, the local
health staff visited each household to explain the study,
obtain written consent from each subject, and remind
participants of the time and date of the survey. At the end
of the survey, a total of 2,368 participants had been
included.
Interview
All participants completed a structured questionnaire.
Included was an assessment of subjects’ medical history,
Am J Epidemiol 2005;161:824–830
825
particularly focusing on hyperparathyroidism, gastrectomy,
diseases of the kidney, diabetes mellitus, rheumatoid
arthritis, chronic liver disease, chronic malabsorptive syndromes, cancer, and jejunoileal bypass, as well as current or
past treatment with glucocorticoids and/or thyroid hormone.
Subjects were excluded from analysis if they had at least one
of the above conditions. Use of oral contraceptive pills was
also recorded.
Information on fracture history, family history of fracture
and osteoporosis, socioeconomic status, lifelong occupation, educational level, and recreational weight-bearing
exercise was collected from each subject. The interview
also asked about current age and age at menarche and
menopause, as well as number of children.
Lifelong occupation was defined as the occupation that
the subject engaged in most frequently in her life. It was
classified as heavy work (farmers, manual workers), office
work (office clerks and other sedentary jobs), or domestic
work (housewife). Educational level was categorized in
three groups, by number of years of schooling: low level
(5 years), medium level (6–8 years), and high level (9
years). Recreational weight-bearing exercise was assessed
by inquiring about regular weight-bearing exercise during at
least the past 12 months. The subjects reported the number
of sessions of weight-bearing exercise of at least 30 minutes
per week. Active behavior was defined as engaging in more
than two sessions per week.
Anthropometry measurement
Height and weight were measured while subjects were
standing, wearing light clothing and no shoes. Body mass
index was calculated as the ratio of weight (in kilograms) to
height (in meters) squared. Waist circumference was
measured at the minimum circumference between the
umbilicus and iliac crest, and hip circumference was
measured at the widest circumference around the buttocks.
Bone mass assessment
Bone mass was assessed by speed of sound (m/second)
using a QUS device (CM-100; ELK Corporation, Tokyo,
Japan). This device is small and portable, with a gel-coupled
(dry) system that can measure speed of sound at the
calcaneus. Coefficients of variation for the device were
measured short term in vivo and in vitro. Precision error
(percent coefficient of variation) using the phantom technique was 0.15 percent and, in vivo, was 0.27 percent (19).
For all subjects, speed of sound was measured at the right
calcaneus. The measurement was taken in a temperaturecontrolled environment and was performed by a trained
medical technician only. Standardization and calibration
with standards were performed before the first measurement
of each survey day.
The T-score for each subject was calculated by
using the peak speed-of-sound value for a defined
population of young adults, and its standard deviation,
with the following equation (20): T-score ¼ speed of
soundsubject speed of soundpeak value for young adults/
standard deviationpeak value for young adults.
826 Hien et al.
We calculated the peak speed-of-sound value for young
adults (speed of soundpeak value for young adults) by estimating
peak bone mass, which was itself defined as the average
maximum bone mass achieved by young, healthy, sex- and
race-matched adults (21). For our own population, we
defined the young adult population by identifying the age
range at which speed of sound reached peak value.
Speed of soundpeak value for young adults and standard
deviationpeak value for young adults were determined as the
mean speed-of-sound value for the young adult population
and its standard deviation, respectively.
A person was classified as having osteoporosis if her
T-score was 1.8 and as normal if the score was >1.8.
Statistical analysis
In this paper, data are presented as percentage and as
mean (standard deviation). Student’s t test (two sided) was
applied to examine differences in age, number of children,
anthropometric indicators, and speed-of-sound values between women in rural and urban areas. Bonferroni’s t test
was used to identify significant differences in speed-ofsound values for 5-year age groups to define the age range
for young adults and their peak speed-of-sound value. Chisquare testing was used to examine differences in the
prevalence of osteoporosis, active weight-bearing exercise,
lowest educational level, and heavy lifelong occupation
between women in the rural and urban areas.
Multiple logistic regression analysis was used to test
several models for the associations between osteoporosis
assessed by speed of sound and other variables. Here, data
are presented as odds ratios and 95 percent confidence
intervals. Associations were considered statistically significant at the p < 0.05 level.
All statistical procedures were performed by using SPSS
software for Windows, version 10.0 (SPSS, Inc., Chicago,
Illinois).
RESULTS
TABLE 1. Characteristicsy of Vietnamese adult women living
in urban and rural areas of Hanoi City in 2003 who participated
in a survey of the prevalence of osteoporosis and related
factors
Urban (n ¼ 1,237)
Variable
Rural (n ¼ 995)
Age (years)
48.8 (16.3)
48.0 (16.6)
Weight (kg)
50.7 (7.7)
47.6 (7.1)**
Body mass index (kg/m2)
22.0 (3.1)
20.9 (2.7)**
Waist/hip ratio
0.83 (0.06)
0.81 (0.06)*
Speed of sound at the
calcaneus (m/second)
1,516 (33)
1,518 (35)
Premenopausal women
153.3 (5.0)
153.1 (4.9)**
Postmenopausal women
150.0 (5.5)
148.5 (5.2)
Premenopausal women
9.3
11.3
Postmenopausal women
34.8
67.5**
Premenopausal women
18.8
67.5**
Postmenopausal women
29.1
51.4**
Premenopausal women
1.5 (0.8)
1.6 (0.9)
Postmenopausal women
3.6 (1.9)
4.5 (2.1)**
Premenopausal women
31.8
38.1*
Postmenopausal women
60.8
57.7
Height (cm)
Lowest educational
level (%)
Heavy-work lifelong
occupation (%)
No. of children
Active weight-bearing
exercise (%)
* p < 0.05; ** p < 0.001 (two sided).
y Unless otherwise noted, values are expressed as mean (standard deviation). Rural values were compared with urban values by
using Student’s t test or the chi-square test.
children and a lower educational level than those in the
urban areas.
Characteristics of the subjects
After we reviewed the medical histories, data on 136
subjects with illnesses deemed to affect bone metabolism
were excluded from analysis. Thus, data on a total of 2,232
women (1,237 in urban and 995 in rural areas) were
available for analysis. Premenopausal women accounted
for 46.5 percent of the population (n ¼ 1,038).
Table 1 shows the characteristics of subjects; their mean
age was 48.5 (standard deviation, 16.5) years. In the rural
areas, anthropometric indicators such as weight, body mass
index, and waist/hip ratio were significantly lower in both
premenopausal and postmenopausal women, while height
was significantly lower only in postmenopausal women
compared with those in the urban areas.
Compared with urban women, most of the women in the
rural areas had a lifelong occupation involving heavy work
and engaged in more weight-bearing exercise in their leisure
time. Postmenopausal women in the rural areas had more
Prevalence of osteoporosis
Speed-of-sound value reached its peak at age 30–34
years, started to decline at age 35–39 years, and declined
significantly from age 45 to 49 years. Because mean speedof-sound values at ages 35–39 years and at ages 40–44 years
were similar or even higher than for the age group 20–24
years, we defined women aged 20–44 years as young
adults to calculate peak speed-of-sound value (speed of
soundpeak value for young adults) and its standard deviation
(standard deviationpeak value for young adults) for our own
population. The peak speed-of-sound value for the young
adults was determined to be 1,536 (standard deviation, 30)
m/second. On the basis of this value, the crude prevalence of
osteoporosis was estimated at 15.4 percent in the study
population. Table 2 shows that the prevalence of osteoporosis in the age groups increased with age (v2 ¼ 669.7; p <
0.001, two-sided). After we adjusted for age (using 1999
Am J Epidemiol 2005;161:824–830
Osteoporosis in Vietnamese Women
TABLE 2. Crude prevalence of osteoporosis, by age group,
among Vietnamese adult women living in Hanoi City in 2003
who participated in a survey of osteoporosis and related
factors
Normal
(%)
Osteoporosis
(%)
Age group
(years)
No.
20–29
369
99.2
0.8
30–39
383
97.9
2.1
40–49
407
96.3
3.7
50–59
405
91.6
8.4
60–69
403
69.5
30.5
70–79
217
43.8
56.2
48
20.8
79.2
2,232
84.6
15.4
80
Total
Hanoi census data), the estimated prevalence of osteoporosis was 9.0 percent.
The prevalence of osteoporosis among premenopausal
women was higher in the urban areas than in the rural areas
(figure 1). By contrast, among postmenopausal women, it
was higher in the rural areas than in the urban areas.
Risk factors associated with low speed-of-sound value
Multiple logistic regression analysis showed that age,
menopause, number of children, height, educational level,
lifelong occupation, and recreational weight-bearing exercise acted as significant predictors for osteoporosis (table 3).
These associations were adjusted for age at menarche,
weight, body mass index, waist/hip ratio, family history of
osteoporosis, previous fracture, and oral contraceptive use.
Age and number of children were positively related to the
risk of osteoporosis, while height was negatively related to
827
TABLE 3. Significant predictors of osteoporosis,* assessed
by speed of sound at the calcaneus, for Vietnamese adult
women living in Hanoi City in 2003 who participated in a survey
of the prevalence of osteoporosis and related factors
Age (1-year increment)
Odds ratio
95% CIy
p value
1.15
1.12, 1.17
<0.001
2.07, 5.52
<0.001
Menopause status
Premenopausal
1.00
Postmenopausal
3.38
Educational level
Lowest
1.00
Medium
0.54
0.29, 0.98
0.04
Highest
0.45
0.25, 0.79
<0.01
Lifelong occupation
Heavy work
1.00
Office work
2.00
1.32, 3.02
0.01
Housewife
1.95
1.28, 2.95
<0.01
Recreational
weight-bearing
exercise
No
1.00
Yes
0.30
0.21, 0.44
<0.001
No. of children (1-quartile
increment)
1.75
1.11, 2.76
<0.05
Height (1-quartile
decrement)
1.30
1.07, 1.57
<0.01
* Information was obtained by multiple logistic regression analysis.
The model was adjusted for age at menarche, weight, body mass
index, waist/hip ratio, family history of osteoporosis, previous
fracture, and oral contraceptive use.
y CI, confidence interval.
the risk of osteoporosis. Increased educational level was
associated with a significantly reduced risk of osteoporosis.
For subjects who engaged in weight-bearing exercise at
least three times a week, the prevalence of osteoporosis was
three times lower than for those who did not. Regarding
menopause status, postmenopausal women had a threetimes higher risk of osteoporosis than premenopausal
women. On the basis of lifelong occupation, office workers
and housewives had double the risk of osteoporosis
compared with women engaged in heavy work.
DISCUSSION
FIGURE 1. Comparison of the prevalence of osteoporosis among
premenopausal and postmenopausal women living in urban and rural
areas of Hanoi City, Vietnam, in 2003.
Am J Epidemiol 2005;161:824–830
Recently, use of QUS at peripheral sites has been
proposed for measuring bone density in large populations
(3, 22). In the current study, we attempted to identify the
prevalence of osteoporosis and related factors in Vietnamese
adult women by using QUS at the calcaneus with our dataderived T-score and by defining osteoporosis as a T-score of
1.8. By using this method, we estimated the prevalence
of osteoporosis in Vietnamese adult women in rural and
urban communities of Hanoi City. The age-adjusted prevalence of osteoporosis for our participating Hanoi subjects
828 Hien et al.
was 9.0 percent. In addition, we found contrasting distributions of osteoporosis between urban and rural areas.
Speed-of-sound measurements at the calcaneus can
identify persons at risk of osteoporotic fracture as reliably
as bone mineral density measurements (23–26) and could be
an ideal tool to screen for osteoporosis at the community
level (6–12). However, it also has been demonstrated that
the T-score threshold of 2.5 may lead to underestimation
of the prevalence of osteoporosis when QUS is measured at
the heel (21). Recent studies on the Hologic Sahara and the
Hologic UBA575þ (Hologic, Bedford, Massachusetts) and
on the Osteometer DTUone (Osteometer MediTech, Inc.,
Hawthorne, California) QUS devices indicate that a T-score
threshold of 1.8 identifies the same percentage of persons
with osteoporosis as the World Health Organization threshold for bone mineral density measurements (27). The CM100 device used in our study is very similar to the Sahara
device and is also used to measure QUS parameters at the
calcaneus. The device comes with a manufacturer’s recommended cutoff value for diagnosing osteoporosis, validated
by dual-energy x-ray absorptiometry (28). In addition, we
found excellent agreement between the manufacturer’s
cutoff and our data-derived T-score in classifying osteoporosis (kappa ¼ 0.967, p < 0.001). Therefore, we felt it was
reasonable to apply a T-score threshold of 1.8 to define
osteoporosis in our population.
The age at peak bone mass depends on skeletal sites or
technologies used (20). Evidence from previous studies
indicates that QUS parameters start to decline from the age
of 40–45 years and fall steadily thereafter (29, 30). Our
study showed similar results, with the peak value of speed of
sound occurring from 20 to 44 years of age, followed by
a significant decline thereafter. For these reasons, we
concluded that defining peak speed-of-sound value as the
mean for women aged 20–44 years and defining osteoporosis by using a T-score threshold of 1.8 is reasonable in
screening for osteoporosis in our population when the CM100 device is used.
In this study, the prevalence of osteoporosis in Vietnamese women was found to be lower than that in Japanese
women in the age group 50–79 years (29.5 percent vs. 51.2
percent) (31) but was similar or higher in comparison to
nearby countries such as China (3.7 percent vs. 3.7 percent
in the age group 40–49 years, 8.4 percent vs. 3.9 percent in
the age group 50–59 years) (32) and Korea (12.8 percent vs.
11.8 percent in women aged 50 years) (33) when the same
age range was compared or when the same method was used
to classify osteoporosis. When we put the information into
context, Japanese women aged 50–79 years were infants and
young children during World War II. Their nutrition was
poor, and calcium intake in 1946 was only 253 mg per day
(34). Therefore, the prevalence of osteoporosis in that age
group is very high. In Vietnam, women who are aged 50–79
years were also exposed to war and had poor nutrition. Thus,
it is reasonable to compare the prevalence of osteoporosis
between Vietnamese and Japanese women aged 50–79
years. The Vietnamese women aged 40–49 years were born
when the war had just ended. The situation may be the same
with Chinese women in the same age range. This factor
might explain why the prevalence of osteoporosis is
comparable in Vietnamese and Chinese women aged 40–
49 years. When classified on the basis of the T-score
threshold of the World Health Organization, the prevalence
of low bone mass among Vietnamese women aged 20 years
or older in 2003 increased compared with that in 2000
(6.4 percent vs. 5.7 percent) (15). These comparisons may
be slightly weakened by the difference in the measurement,
calibration, and standardization methods used in these
studies, but our findings indicate that osteoporosis is
becoming a noteworthy problem in Vietnam.
Factors affecting bone mineral density have been studied
extensively (35–38). Recently, the impact of risk factors on
QUS parameters has also been given more attention. Our
data show that increasing age and postmenopausal status are
predictors of low speed of sound. Increased age was
associated with a significantly increased risk of osteoporosis,
especially when women become postmenopausal. This
finding is consistent with those from other studies (10, 15,
39). Our study also agreed with previous research reporting
that low educational level was related to increased risk
of osteoporosis (40). Low stature and a large number of
children are predictors of low speed of sound. These
associations were demonstrated in previous studies (41–
43) and were also confirmed in our data. In addition, our
survey indicates that engaging in recreational, active weightbearing exercise and having a lifelong occupation involving
heavy work can help protect subjects from osteoporosis.
Our study also revealed contrasting distributions of
osteoporosis between urban and rural areas of the country.
To our knowledge, this finding has not been observed in
other countries and is likely due to socioeconomic characteristics of Vietnamese. In rural areas, most of the people
are farmers and take part in more active weight-bearing
exercise, which might explain why the prevalence of
osteoporosis among rural premenopausal women was lower
compared with that among urban women. However, because
rural postmenopausal women have more children, a lower
stature, and a lower educational level, the prevalence of
osteoporosis among postmenopausal women in the rural
areas was higher. In addition, rural women consume fewer
dairy products, and eggs/milk consumption in the rural areas
was lower than in the urban areas (5.4 g per capita/day vs.
25.5 g per capita/day). Moreover, the postmenopausal
women experienced greater problems with access to enough
food, including calcium-rich foods, when they were teens
and young adults because of war and the early years
thereafter (44). Exposed to a long period of inadequate
calcium intake, rural postmenopausal women are more
likely to suffer from osteoporosis. This finding may partially
explain why the prevalence of osteoporosis among postmenopausal women was higher in the rural areas, and it
should be confirmed by further studies in order to design an
appropriate intervention strategy.
The present study has several limitations. First, the
T-score threshold for diagnosing osteoporosis by QUS or
use of the CM-100 device has not been established.
However, in the context of epidemiologic studies at the
community level in developing countries, we could only
apply QUS and use a T-score threshold of 1.8 to identify
subjects with osteoporosis. Many studies support the view of
Am J Epidemiol 2005;161:824–830
Osteoporosis in Vietnamese Women
using QUS to screen for osteoporosis at the community level
(6–12). A previous study also applied a T-score threshold of
1.8 to define osteoporosis using QUS (45). For these
reasons, we believe that, with a large sample size and
random sampling methods, our data may truly represent the
prevalence of osteoporosis in Hanoi City, or they may even
underestimate its prevalence. Second, this study was a crosssectional survey, and we could not measure all factors
affecting the risk of osteoporosis. Moreover, using a prevalence measure to assess risk factors also has limitations
because the factors associated with osteoporosis may not
reflect the real cause-effect relation. Risk factors assessed by
using prevalence measures can only suggest the hypothesis
for a possible cause-effect relation. Thus, a prospective
study is needed to confirm any association between low
speed of sound and risk factors and to explain the differing
patterns of osteoporosis distribution between urban and
rural areas.
In conclusion, this study shows that the prevalence of
osteoporosis in Vietnamese adult women in Hanoi City,
determined by QUS, is relatively high compared with that in
nearby countries. In addition, our data indicate differing
distributions of osteoporosis between rural and urban areas
of Hanoi City. These findings suggest that osteoporosis is
a problem in Vietnam. Furthermore, using multiple logistic
regression, we assessed associations between low speed of
sound and risk factors, as well as protective factors. Because
osteoporosis is related to considerable mortality and increasingly higher costs of health care, screening for
osteoporosis, particularly in high-risk populations, and
setting up a national program to prevent and control
osteoporosis in Vietnam are urgently needed.
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