Forearm Bone Mineral Density by Age in 7,620 Men and Women The Tromsø Study, a Population-based Study
Gro K. Rosvold Berntsen1,
Vinjar Fønnebø1,
Anne Tollan2,
Anne Johanne Søgaard3 and
Jeanette H. Magnus1
1 Institute of Community Medicine, University of Tromsø, Tromsø, Norway.
2 Department of Gynecology, Central Hospital of Hedmark, Hamar, Norway.
3 Ullevåll University Hospital, Center for Preventive Medicine, Oslo, Norway.
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ABSTRACT
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Population-based studies of adult forearm bone mineral density (BMD) by age are scarce, and standardized reference values are lacking. In this cross-sectional study, men aged 5574 years, women aged 5074 years, and representative 510% samples of remaining age groups between 25 and 84 years living in Tromsø, Norway, were invited for forearm BMD measurement in 19941995. The authors measured 3,062 men and 4,558 women (response rate, 78%) by single x-ray absoptiometry at distal and ultradistal forearm sites. Up to age 50, the mean BMD difference was 0.1% per 1-year age group in both sexes. After age 50, the mean BMD difference per 1-year age group was -0.6% in men and -1.3% (distal) and -1.5% (ultradistal) in women. The BMD by age curve was linear for men throughout senescence, but women had a slope change to -0.7% (distal) and -0.8% (ultradistal) per 1-year age group from the 65- to 69-year age group. BMD levels and BMD by age association in the general population (n = 7,620) and in the population without bone-threatening diseases or medication (n = 5,179) were similar. Only longitudinal studies can clarify whether cohort effects or longitudinal BMD development patterns explain these cross-sectional results.
bone density; cross-sectional studies; densitometry; X-ray; forearm; men; menopause; reference values; women
Abbreviations:
BMD, bone mineral density;
BMD, mean BMD difference.
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INTRODUCTION
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The ability of the forearm bone mineral density (BMD) to predict any fracture in women is believed to be as good as that for other measurement sites (1
), and wrist BMD has been shown to predict male fragility fractures better than other anatomic sites (2
). Forearm single x-ray absorptiometry is one of the most precise bone densitometric methods (3
), and it is easy, readily standardized, and cheaper than dual energy x-ray absorptiometry measurements at axial sites. Therefore, single energy x-ray absorptiometry measurements of the forearm are a good candidate for any BMD screening (4
, 5
).
Study of the BMD distribution in a general population is needed to compile representative age- and sex-specific reference values. Only two studies of forearm BMD in the general population have previously been published, one from a Japanese-American population (6
) and the other from an elderly upper-middle-class retirement community (7
). Both studies included only middle-aged and elderly subjects. Thus, population-based studies describing the adult life-span BMD distribution are wanting.
As BMD values are not standardized, reference ranges from previous publications are generally not comparable with results from other densitometers (8
). To achieve comparability, BMD results from both densitometers need to be translated to a common scale. A golden BMD standard, against which all other densitometers can compare their results, has proven difficult to produce and has up to now been lacking for the forearm. Ruegsegger and Kalender (9
) have recently developed the European forearm phantom, which is a forearm bone imitation, with a standard bone density. It is currently under evaluation by the International Committee of Standards in Bone Densitometry (K. Engelke, Institut fur Medizinische Physik, Universitat Erlangen, personal communication, 1999). No other standardized BMD reference ranges have been presented up to now.
Most presentations of normal BMD reference ranges are based on highly selected populations believed to be "normal" (i.e., subjects without disease or medication known to affect bone health). However, the selection criteria used to define such populations depend on the current and often fleeting views of "normality" with respect to bone health. Such a selection process could have profound effects on reference values and possibly explain reference range disparities among manufacturers (10
). To our knowledge, a comparison of reference ranges betwen a general population and a selected population without disease or medication known to affect bone health has not yet been published.
The aim of this paper is thus to:
- characterize the forearm BMD distribution by age in a general population
- present standardized age- and sex-specific reference values for distal and ultradistal forearm BMD
- compare reference ranges derived from a general population and a selected population without diseases or medication known to affect bone health.
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MATERIALS AND METHODS
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Study population
Bone densitometry was performed on 3,062 men and 4,558 women recruited from the 19941995 survey of the Tromsø Study. This is a population-based multipurpose study where all subjects aged 25 years or more living in the municipality of Tromsø, Norway, were invited to the main survey (phase I, n = 27,159). Upon attendance at phase I, the following preselected groups were invited to an extended examination (phase II) that included bone densi-tometry (n = 10,213):
- all men aged 5574 years
- all women aged 5074 years
- 510 percent samples of the remaining age groups between 25 and 84 years
Two information brochures were provided together with the study invitations to both the main and extended examinations. Participants signed a declaration of consent prior to both examinations. The Regional Committee of Research Ethics and the Norwegian Data Inspectorate approved the study.
Of all preselected subjects, 78 percent (n = 7,948) had a bone mineral density measurement. Especially invited male participants of the Family Intervention Study (11
) were overrepresented in the younger age groups, which is why 328 were excluded to avoid overrepresentation. This left 7,620 subjects whose age- and sex-specific response rates are given in table 1. The study population was dominated by non-Hispanic Whites. The majority have a Norwegian ethnic background, and approximately 1020 percent have Sami, Finnish, or Sami/Finnish ethnic background.
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TABLE 1. Response rates by age and sex for full participants (attended both first and second examination) among 10,213 eligible subjects, Tromsø Osteoporosis Study, 19941995*
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The population was without disease or medication affecting bone health. As there is no consensus on which factors should be viewed as a threat to bone health, we applied an aggregate of all exclusion criteria used in larger studies (n > 150) that had sought to exclude subjects with diseases and/or medication affecting bone health (8
, 10
, 12




18
). We retained any criteria representing diseases or medication shown to be associated with BMD (table 2), while lifestyle factors and nondisease condtions such as premature menopause, little physical activity, smoking, excessive weight loss, low body mass index, and calcium supplementation were not used as exclusion criteria. We had no information on anorexia, recent hyperthyroidism, hypogonadism, oophorectomy, neurologic disease, recent immobilization, rickets, adrenal disease, or vertebral fractures. The selected subset included 68 percent (n = 5,179) of the original study population. The proportion with one or more exclusion criteria rose from 5 percent in those aged 2029 years to 50 percent among those aged 7079 years (p < 0.001), and more women than men were excluded (p < 0.001) (table 2).
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TABLE 2. Exclusion criteria that defined the population without disease or medication known to affect bone health, from the total study population (n = 7,620), Tromsø Osteoporosis Study, Norway, 19941995*
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Menopause and use of estrogen
Women were asked to report whether they still menstruated and, if not, their age at menopause. Women who had stopped menstruating over a year ago or, if menopause data were missing, were
55 years of age were defined as postmenopausal (n = 3,631). Women who had stopped menstruating within the last year were considered perimenopausal (n = 76). Information on the cause of menopause (natural or surgical) was not available. The mean, median, and 95th percentile ages at menopause were 48 years, 49 years, and 55 years, respectively. Pregnant women and women who were still menstruating and reported a menstruation within the last 6 months were classified as premenopausal (n = 647). Menopausal status was left undefined in 204 women because of missing or conflicting values.
A total of 2, 15, and 84 percent of all premenopausal and 6, 20, and 74 percent of all postmenopausal women answered that they were previous, current, or never users of tablets/patches containing estrogen (not contraceptives), respectively. We excluded current and previous estrogen users and women with undefined menopausal status from analyses by menopausal status. However, 772 women had answered other questions on reproductive issues but left the estrogen question open. Although plausible, we could not be certain that these were estrogen nonusers who found the question irrelevant. Therefore, postmenopausal BMD distribution by age was analyzed with and without the 772 women with missing estrogen data. The results were virtually identical (data not shown), which is why women with missing estrogen data were included in the final analyses.
Bone densitometry
Bone densitometry was performed on the nondominant forearm at distal and ultradistal sites with two single x-ray absorptiometric devices (DTX-100; Osteometer MediTech, Inc., Hawthorne, California). The distal site, which contains 1020 percent trabecular bone (19
), includes both the radius and the ulnae from the 8-mm point (point where the ulnae and radius are separated by 8 mm) and 24 mm proximally. The ultradistal site contains 5070 percent trabecular bone (19
), includes only the radius, and stretches from the 8-mm point up to the radial endplate. The dominant arm was measured in 1 percent of the subjects when the nondominant arm was ineligible because of wounds, plaster casts, and so on.
Quality control with respect to precision, long-term stability, detection, and correction of artifacts has been described elsewhere (3
, 20
). Briefly, the coefficients of variation were 0.79 percent and 0.98 percent at the distal and ultradistal sites, respectively. All scans were reviewed and, if necessary, reanalyzed. Serious movement artifacts, region-of-interest outside scan, metallic objects in the region of interest, or bad quality by other causes led 136 distal and 150 ultradistal scans to be excluded, leaving 7,484 distal and 7,470 ultradistal scans for analysis. The systematic BMD difference between the two densitometers was adjusted before analyses (3
).
Standardized BMD values
The European forearm phantom (EFP) (QRM (Quality Assurance in Radiology and Medicine) GmbH, Moehrendorf, Germany) had three hydroxyapatite bone imitations (inserts) with differing densities. We performed 20 measurements of each insert on both densitometers and used regression analysis to model the best-fitting equation between the given and observed BMD values (21
). We tested both a linear and a quadratic term in the model. Both terms were significant, but as the R-squared values for the models were similar (R2 linear model, 0.990; R2 quadratic model, 0.991), we adhered to the simpler linear model:
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Previous fractures in forearm
Distal forearm fracture is associated with a BMD increase at the ultradistal site (22
), low BMD at other sites (23
, 24
), and increased risk for fractures (25
, 26
). Therefore, ultradistal BMD in 637 subjects who reported a distal forearm fracture in the measured hand was corrected according to the results from a substudy of fracture and nonfracture cases. Briefly, 50 subjects with distal forearm fracture were age and sex matched to 115 subjects without fracture. The ultradistal BMD was on average 0.038 g/cm2 higher on the fracture side in cases as compared with that in noncases, whereas there was no effect of fracture on distal BMD.
Data analysis
Plots of BMD life curve. BMD means for each 5-year age and sex stratum were plotted against age to produce BMD life curves. To dissociate the effects of loss of endogenous estrogen production at menopause from other age-related factors, we made an additional plot of the mean BMD for each 5-year age stratum since menopause and 10-year age stratum for postmenopausal women.
BMD by age curves. The BMD by age curves is described in terms of slope and changes of slope. The slope is calculated in one of two ways: 1) the difference between age-specific BMD means, divided by the number of years between the midpoints of the age groups in question. For example, the BMD difference between two consecutive 5-year age groups is divided by five to yield the average BMD difference per 1-year age group. 2) Each linear segment of the BMD life curves was also described with linear regression by age. The regression beta-coefficient expresses the mean BMD difference per 1 year of age increase.
Because age is a time-related variable, a description of BMD by age in terms of change per year may easily be mistaken for a measure of longitudinal development. We have therefore chosen to use the following terminology: mean BMD difference (
BMD) per 1-year age group. The slope is given either as an absolute number or as a percentage of the mean BMD in the youngest age group in the age span.
Mean BMD differences between age groups were tested by one-way analysis of variance. Beta-coefficients were tested for difference to zero by one-sample t tests and for difference between each other by partial F tests. The level of statistical significance was set at p = 0.05.
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RESULTS
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Women
The association between BMD and age in women was nonlinear with marked changes of slope around 5054 years of age and a less marked change at age 6569 years (figure 1). The BMD by age curve in young adults (2549 years of age) was slightly negative but not significantly different from zero at both sites (figure 1; tables 3
5). The highest mean BMD level was found in women aged 3034 years (distal site), but their values did not differ significantly from other young adult BMD values before the age of 50.

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FIGURE 1. Mean forearm bone mineral density (BMD, g/cm2) by age, sex, and measurement site in a population-based study (n = 7,620) (left panel) and a subset of subjects without disease or medication known to affect bone health (n = 5,179) (right panel), Tromsø, Norway, 19941995. Subjects were from a non-Hispanic White population of Norwegian, Sami, or Finnish ethnic background.
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TABLE 3. Mean distal forearm bone mineral density (BMD), given in standardized European forearm phantom units, and mean BMD percentage differences per 1-year age groups for 5-year intervals, Tromsø Osteoporosis Study, 19941995*
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TABLE 4. Mean ultradistal forearm bone mineral density (BMD), given in standardized European forearm phantom units, and mean BMD percentage differences per 1-year age groups for 5-year intervals, Tromsø Osteoporosis Study, 19941995*
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TABLE 5. Mean bone mineral density (BMD) differences per 1-year age group for linear segments of the BMD by age curve, Tromsø Osteoporosis Study, 19941995*
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At 5054 and 4549 years of age at distal and ultradistal sites, respectively, the association between BMD and age changed so that the
BMD per 1-year age group was greater than 1 percent. From 6569 years of age, the
BMD per 1-year age group decreased to less than 1 percent (table 5). Neither mean BMD levels nor BMD by age curves differed significantly between subjects without disease or medication known to affect bone health and the overall study population (figure 1).
The role of menopausal status was considered. The
BMD per 1-year age group in premenopausal women who had never used estrogen hormone replacement therapy was slightly negative but now differed significantly from zero (distal, 0.11 percent, p = 0.008; ultradistal, -0.19 percent, p = 0.0011). Pre- and perimenopausal mean BMD levels did not differ significantly, but women in their first postmenopausal year had 3.8 percent (distal, p = 0.0008) and 5.9 percent (ultradistal, p < 0.001) lower BMD than did premenopausal women. The mean BMD differences observed among the following five 1-year since menopause groups ranged from -0.3 percent to -1.9 percent (distal) and from 2.1 percent to -3.9 percent (ultradistal).
The
BMD per 5 years since menopause groups seemed to diminish in the late postmenopause within all age strata, whereas the average BMD difference between age groups was remarkably constant within all strata of years since menopause (figure 2). However, we could not separate the effect of age and years since menopause in a regression analysis, because of the high collinearity between the two variables (r = 0.82).

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FIGURE 2. Postmenopausal mean distal bone mineral density (BMD, g/cm2) by age and years since menopause (YSM) in 2,530 women from a population-based study, Tromsø, Norway, 19941995. All women were postmenopausal and had never used hormone replacent therapy. Bars represent 50 subjects or more unless otherwise indicated. Bars representing less than 10 subjects were excluded because of the uncertainty of the estimate. BMD by YSM, linear association, within age strata: 5059 years, p < 0.0001; 6069 years, p < 0.001; and 7079 years, p = 0.15. Between YSM groups, within age strata, bars marked with an asterisk are significantly different (p < 0.05) from neighboring bars. BMD by age, linear association, within YSM stratum: YSM 59, p = 0.043; YSM 1014, 1519, and 2024, p < 0.0001; and YSM 25, p = 0.0019.
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Men
In men also the association between BMD and age was nonlinear, with a change of slope around 5054 years at both sites, although this was most distinct at the distal site (figure 1; tables 3 and 4). At the distal site, no age group displayed higher BMD levels than others before 50 years, whereas at the ultradistal site, subjects aged 3034 years had higher BMD levels. Yet, of all ultradistal BMD means before 50 years, only the 4044 age group mean was significantly lower (p = 0.017) than the peak BMD. The
BMD per 1-year age group before 50 years of age was negative and significantly different from zero at both sites, but the
BMD per 1-year age group was much larger at the ultradistal site (table 5).
From 5054 years of age the
BMD per 1-year age group was -0.6 percent (figure 1; tables 3
5) at both sites. The slopes of the BMD by age, before and after 50 years of age, were significantly different from one another (p < 0.001) at the distal site but of borderline significance at the ultradistal site (p = 0.08). The ultradistal BMD by age curve could alternatively be viewed as linear, from the highest BMD level in subjects aged 3034 years into older age groups. The slopes before and after age 50 would be similar (p = 0.71), and the
BMD per 1-year age group from 30 years up would be -0.47 percent (table 5). The BMD development and BMD levels by age in the subpopulation without diseases or medication known to affect bone were not significantly different from those in the overall study population (figure 1).
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DISCUSSION
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Main findings
The forearm BMD association with age was slightly negative (-0.1 percent between 1-year age groups) in both sexes up to 50 years of age, after which the BMD by age slope became clearly negative, with a
BMD per 1-year age group of -0.6 percent at both sites in middle-aged and elderly men. In middle-aged women, the
BMD per 1-year age group exceeded 1 percent but decreased to -0.7 percent and -0.8 percent from 65 to 69 years of age. The effect of time since menopause on BMD levels seemed to wane off in the late postmenopause. The subset of the study population without disease or medication known to affect bone did not differ from the study population at large with respect to BMD level or BMD by age associations.
Bias considerations
Cross-sectional versus longitudinal BMD change. The cross-sectional estimates of BMD by age associations are not true measures of longitudinal BMD change. They are vulnerable to both cohort effects and selection bias, and patterns of individual BMD change cannot be discerned. Longitudinal studies provide data on individual BMD change patterns, but they are also prone to selection bias and loss to follow-up, and they require repeated measurements that render them costly and time consuming. Thus, cross-sectional studies are attractive ways of establishing BMD distributions by age, but they should be supplemented with longitudinal studies.
Selection bias. Nonresponse may generate selection bias, and in our case the BMD by age curves could be distorted if both BMD level and age were associated with important selection factors. In an effort to characterize response patterns, we compared characteristics for the 10,213 subjects invited to both the first and second examinations by response pattern.
For the 1,151 subjects who attended neither examination (nonresponders), we had only age and sex data. For the 1,114 subjects who attended the first but not the second examination (partial responders), we had data from the first examination and one or two questionnaires. For the 7,948 subjects who attended both examinations (full responders), we had a complete data set. These comparative analyses were stratified by sex and by the following age groups: <45 (young), 4564 (middle aged), and 65 years and over (elderly).
Disease and disability are linked to low BMD (27
, 28
), and nonresponders are known to be less healthy than responders (29
31
), especially among those >55 years of age (32
). However, our full responders were not healthier than partial responders in any age or sex group, as judged by the self-reported prevalence of myocardial infarction, stroke, diabetes, angina pectoris, and asthma. Nonresponders could still be less healthy than partial and full responders. This may explain the lower response rates in subjects aged >75 years (table 1).
Smoking and physical activity are known to affect BMD results (33
, 34
). The elderly and middle-aged partial responders were more often daily smokers (44 vs. 32 percent, p < 0.001) and were more often sedentary in their leisure time (31 vs. 23 percent, p < 0.001) than were full responders. Elderly male and female smokers had 3 percent and 6 percent lower distal BMD than did nonsmokers (data not shown), respectively, whereas the BMD level differed by physical activity only in elderly men in our study (data not shown). These biases may have led to BMD overestimations in the range of 0.30.6 percent in the middle aged and elderly. This is by any standard a negligible adjustment of the BMD by age results.
Analyses of the partial responders gave no clues to the cause of the low response rates in the young (<45 years). Previous studies of young nonresponders found "being too busy" and "perceiving no personal benefit of attending" as important reasons for nonresponse in the young (32
, 35
). Such selection factors would probably not affect the observed associations between BMD and age in this age group.
Misclassification of menopausal status. Women with hysterectomies but intact ovaries and estrogen users who failed to report use would be classified as postmenopausal even though they had premenopausal sex steroid levels. Such misclassification would mitigate any observed effect of time since menopause on BMD in postmenopausal women.
Other limitations. The study population was dominated by non-Hispanic Whites of Norwegian, Sami, or Finnish ethnic background. Whether this represents a barrier to comparability with other ethnic groups and/or representation is currently unknown. The BMD distribution by age is quite similar to that of other unselected populations as judged by visual comparison of BMD curves, but there are currently no data that allow comparisons of BMD levels because of the lack of BMD standardization.
Female BMD life curve
Young adult female BMD. Most (36

39
) but not all (40
, 41
) previously published studies of forearm BMD in self-selected and/or healthy populations find no evidence of premenopausal bone loss. We found a nonsignificant decline in analyses of all young women and a significant decline in analyses restricted to premenopausal BMD never users of estrogen. Perimenopausal estrogen use probably "erases" the BMD decline in the former group. We found no age groups with substantially higher BMD levels than in other age groups, which questions the concept of a premenopausal BMD peak. Population-based longitudinal studies are required to determine whether BMD does decline in the premenopause.
Menopause and postmenopause. The larger BMD differences between women in their first postmenopausal year and premenopausal women, with smaller differences between the second and fifth postmenopausal years, are supported by other studies (7
) and by the current knowledge of the role of estrogen in bone biology (14
, 36
, 42
44
).
The BMD decline by age in the early postmenopause is steeper than that in the late postmenopause. Several smaller cross-sectional studies of forearm BMD in selected populations also report such a pattern (36
, 38
, 42
, 45
, 46
), but the two other population-based studies of forearm BMD observed no equivalent changes of slope (6
) or a small change at the midradius only (7
). Several explanations could be valid for this observation. 1) One explanation might be that there is an average BMD change identical to the cross-sectional changes. Riggs et al. (47
) suggest that a depletion of cancellous bone surface after many years of increased bone loss causes such an average change in bone resorption in the sixth decade (47
). 2) If small groups experience large BMD changes over shorter periods of time, cross-sectional BMD would decline as long as women continue to enter the swift bone loss phase. This is consistent with longitudinal studies where bone loss levels off 410 years after the menopause (40
, 48
50
). 3) Another explanation might be a cohort effect, where women who are now past 65 years of age generally lose less bone per year than younger women do.
The observed pattern is still an enigma and has so far not been satisfactorily explained. Population-based longitudinal studies of bone loss coupled with studies of the determinants of such loss are needed.
Male BMD life curve
Young adulthood. The young adult BMD by age slope for the distal site was slightly but significantly negative. Two previous studies of distal BMD in selected populations support this (36
, 51
), while one study found a stable distal BMD (42
).
Volumetric ultradistal BMD has been shown to be stable by age up to the age of 50 (46
). Our young adult ultradistal curve was quite irregular, with a high peak and a steep decline. The small numbers in the youngest male age groups probably account for the curve irregularity. Furthermore, if the BMD mean for the 3034 age group is disregarded, the ultradistal young adult curve would become quite similar to the distal curve.
Middle and old age. There was a change to a more negative slope in the male BMD by age curve around age 50 at both forearm sites, although the change was not as clear-cut as in women. With the exception of one study (51
), other studies of smaller selected populations support this observation (36
, 42
, 46
, 52
). The reason for the larger differences is not clear, but the age-related decrease in male estrogen levels might play a role (
). The BMD by age slope after age 50 is negative and linear at both sites up to the seventh decade. This is comparable to the findings in the population-based study of Caucasian men (7
) but not of Japanese-American men whose
BMD per 1-year age group was even more negative (>1 percent) after the age of 60 (6
).
BMD development in healthy versus general populations
Neither the BMD by age association nor BMD levels in the general population differed significantly from those in subjects without disease or medication known to affect bone health. Considering that over 2,000 subjects were excluded, this stability was surprising, as such a systematic selection might be expected to distort results. The explanation may be that the mixture of exclusion factors had no common effect on the BMD, and they therefore to some extent cancelled each other out. This is good news, as we up to now have relied heavily on results from selected groups of so-called "normal" subjects. However, the studies that provided our exclusion criteria (8
, 10
, 12




18
) all applied quite different sets of exclusion criteria effectively rendering the populations incomparable. We fear that the small inconsistencies in our study may be due to a lucky combination of exclusion criteria that cancelled out important effects and that slight changes in the exclusion criteria may produce different results. As long as "normal" and "healthy" with respect to bone status lack operational definitions, we recommend the study of the unselected general population or use of selection criteria that are standardized and easily replicable.
The results presented in this paper bring forth questions that are important for our further understanding of bone biology:
- Does forearm BMD decline in young adulthood in both men and women, and if so why?
- Is the age-related BMD loss parallel for both men and women when the menopausal BMD loss is disregarded?
- What mechanism causes the BMD by age curve to become less steep at 65 years of age in women?
- Does BMD development at male trabecular sites differ from that at male cortical sites and female cortical and trabecular sites?
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NOTES
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Correspondence to Dr. Gro K. Rosvold Berntsen, Institute of Community Medicine, University of Tromsø, N-9037 Tromsø, Norway (e-mail: gro.berntsen{at}ism.uit.no).
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Received for publication November 22, 1999.
Accepted for publication June 22, 2000.