Correlates of Forearm Bone Mineral Density in Young Norwegian Women

The Nord-Trøndelag Health Study

Gillian A. Hawker1,2,3, Siri Forsmo4, Suzanne M. Cadarette2,3, Berit Schei4, Susan B. Jaglal2,3,5, Lisa Forsén6 and Arnulf Langhammer7

1 Division of Rheumatology, Women’s College Ambulatory Care Centre, Sunnybrook and Women’s College Health Sciences Centre, Toronto, Ontario, Canada.
2 Osteoporosis Research Program, Women’s College Ambulatory Care Centre, Sunnybrook and Women’s College Health Sciences Centre, Toronto, Ontario, Canada.
3 Department of Health Policy, Management and Evaluation, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada.
4 Department of Community Medicine and General Practice, Faculty of Medicine, Norwegian University of Science and Technology, Trondheim, Norway.
5 Department of Rehabilitation Science, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada.
6 National Institute of Public Health, Oslo, Norway.
7 HUNT Research Centre, Faculty of Medicine, Norwegian University of Science and Technology, Verdal, Norway.

Received for publication September 12, 2001; accepted for publication April 24, 2002.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Maximizing attainment of optimal peak bone mineral density (BMD) is a potential osteoporosis prevention strategy. The main objective of this study was to identify correlates of forearm BMD in young adult women. Population-based data derived from standardized questionnaires administered to healthy women aged 19–35 years in Nord-Trøndelag, Norway (n = 963), were collected in 1995–1997. Forearm BMD was assessed by single x-ray absorptiometry. Multiple linear and logistic regression analyses were used to determine correlates of BMD (g/cm2) and lowest quintile of BMD, respectively, at the ultradistal and distal sites. The mean age and weight of the cohort were 29.7 years (standard deviation 4.7) and 68.6 kg (standard deviation 12.5), respectively. Age and weight were positively associated with BMD at both forearm sites. When data were controlled for age and weight, later age at menarche and lack of milk consumption were associated with lower BMD values. In both linear models and logistic models, none of the factors vitamin D intake, physical activity, smoking, alcohol consumption, amenorrhea, oral contraceptive use, number of pregnancies, history of breastfeeding, and family history of osteoporosis were found to be significantly associated with BMD. Prior studies have suggested that calcium supplementation in children is useful for optimizing peak BMD. Further studies exploring the relation between lifestyle factors and BMD are warranted to search for ways to maximize attainment of peak BMD.

bone density; cross-sectional studies; forearm; osteoporosis; women’s health

Abbreviations: Abbreviation: BMD, bone mineral density.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Although peak bone mineral density (BMD) is largely determined by genetic factors, several lifestyle factors also play a role (13). Strategies designed to alter modifiable risk factors for low peak BMD may decrease risk for osteoporosis and fragility fractures in later life. The three most clinically relevant sites for BMD assessment are those of highest risk for fragility fractures, namely the spine, hip, and forearm. Although BMD measurement by dual-energy x-ray absorptiometry at the spine (4) and hip (5, 6) is the most widely accepted technique for the diagnosis of osteoporosis, peripheral bone densitometry is gaining utility as a low-cost and portable alternative to axial measurements (7). While not as strong a measure as site-specific BMD measurements, low radial BMD is a good predictor of fractures at the hip and lumbar spine (8). Recent results from a prospective population-based cohort study found peripheral assessment of low BMD, including low BMD at forearm sites, to be a significant predictor of any osteoporotic fracture, with a rate ratio of 4.03 (95 percent confidence interval: 3.59, 4.53) among women with osteoporosis compared with those with normal BMD (9).

Prior studies have largely examined predictors of peak BMD at the spine and hip (1012), finding age, weight, physical activity, dietary calcium, menstrual dysfunction, and vitamin D receptor genotypes to be significantly associated with peak BMD. To our knowledge, there have been no published studies reporting data on correlates of peak forearm BMD among healthy young adult women. However, low forearm BMD is a good predictor of fractures at the distal forearm, hip, and lumbar spine (8). In addition, distal forearm fractures are recognized as one of the first clinically overt signs of postmenopausal osteoporosis (13), and women with these fractures have a doubled risk of subsequent vertebral or hip fracture (14). The main objective of this study was to use population-based data to identify factors associated with forearm BMD in healthy young adult women.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Study sample
The Nord-Trøndelag Health Study is an ongoing, comprehensive population-based study focusing on many areas of health research, including cardiovascular, respiratory, and bone health, endocrine and mental disorders, chronic pain, hearing, and more. Between August 1995 and June 1997, a comprehensive questionnaire assessing demographic, health, and lifestyle variables and reproductive history was sent to all residents aged 13 years or more in the county of Nord-Trøndelag, Norway. A consent form and an invitation to undergo a health examination were included in the study package. Assessments included measurements of height (without shoes), weight (in light clothing), and blood pressure and the collection of blood samples. Thirty percent of participants aged 30–39 years and 5 percent of participants aged less than 30 years were randomly selected to undergo forearm BMD measurements. At the time of the examination, a second, more detailed questionnaire evaluating demographic factors, medication use, diet, and for women, menstrual history, history of gynecologic surgery, infertility, pregnancy, and breastfeeding was given to participants. Participants were asked to complete the questionnaire at home and return it by mail. The Nord-Trøndelag Health Study protocol received ethical approval from the National Committee on Ethics in Medical Research (Norwegian Data Inspectorate). The present study includes data from healthy women aged 19–35 years who had undergone forearm bone densitometry.

Assessing correlates of forearm BMD
Information on risk factors was obtained through responses to the Nord-Trøndelag Health Study surveys. Data on weight (kg), height (m), and body mass index (weight (kg)/height (m)2) were grouped into quintiles for analysis. Information on intakes of milk (glasses) and cheese (slices) was collected as daily consumption of 0, <1, 1–2, and >=3 servings. Separate dichotomous variables (yes/no) were created to identify each of current milk consumption and current cheese consumption. A calcium composite measure was derived from questions about daily consumption of milk (300 mg per glass), cheese (200 mg per slice), and calcium supplements (500 mg). Preliminary results found that daily use of vitamin D supplements and cod liver oil evaluated separately were similarly associated with BMD, and thus these variables were combined as an indication of any vitamin D supplementation (yes/no).

Cigarette smoking was analyzed as pack-years and separated into three categories: never smoking, past smoking, and current smoking. Childhood exposure to secondhand smoke and current exposure to secondhand smoke were assessed. Information on alcohol drinking was collected as consumption of wine, beer, and spirits per 2-week period. This variable was analyzed both as a continuous variable and as a categorical variable divided into groups based on weekly consumption. A history of alcohol problems was identified by responses to questions on guilt or receipt of criticism about excessive alcohol consumption and use of alcohol in the morning to calm one’s nerves. A caffeine score was created from daily coffee and tea intake, assigning one point for each cup of coffee and one half point for each cup of tea; scores were then grouped into quintiles for analysis.

Data on light and heavy physical activity were collected as none, <1 hour/week, 1–2 hours/week, and >=3 hours/week. We also assessed age at menarche, use of oral contraceptives, number of deliveries, months of breastfeeding, and periods of amenorrhea. Late menarche was defined as starting to menstruate at age 15 years or later. Age was assessed both as a continuous variable and as a categorical variable divided into groups of 19–24, 25–29, and 30–35 years.

Outcome measure
Single x-ray absorptiometry (Osteometer DTX-100; Nordic Bioscience A/S, Copenhagen, Denmark) was performed at the ultradistal and distal sites of the nondominant forearm. Testing was done on the dominant arm among cases reporting a previous fracture in the region of interest. If previous fractures were reported in both arms, measurement was done on the nondominant arm. Densitometers were calibrated daily. In addition to assessment of the outcomes as continuous variables, quintiles of BMD were determined and the lowest quintiles were identified for analyses. Ultradistal and distal sites were analyzed separately.

Statistical analysis
Demographic and other characteristics of the study population were tabulated as mean values and standard deviations or proportions. Because of problems with automated determination of the beginning of the radial endplate or the 8-mm radius-ulna distance, measurements were recalculated after manual determination (15). Pearson correlation coefficients for BMD and Spearman correlation coefficients for lowest quintile of BMD were computed. Linear relations between each risk factor and ultradistal and distal BMD were determined. Pearson and Spearman correlations between all variables were calculated, as applicable, for assessment of potential collinearity. All variables with a p value of 0.1 or less, controlling for weight, were kept in the variable pool for consideration in multiple-variable linear regression modeling. Forward selection and stepwise approaches were used in model building (16). Similar methods were used to identify correlates of low BMD (defined as the lowest quintile) at the ultradistal and distal forearm sites. In bivariate analyses, the Pearson chi-squared test and unadjusted logistic regression were used for all categorical variables, and t tests were used for continuous variables. Odds ratio estimates and 95 percent confidence intervals were calculated to determine the magnitude of the association for categories within each risk factor. Multiple-variable logistic regression was used to identify independent correlates of low BMD. All analyses were completed using SAS, version 8.12 (SAS Institute, Cary, North Carolina), and p values less than 0.05 were considered significant.

Of the 14,181 women aged 19–35 years who were invited to participate, 8,824 (62 percent) enrolled, and 1,125 (13 percent) were included in the Osteoporosis Study and thus had bone densitometry measurements. Among these women, 995 (88 percent) completed the second, more detailed questionnaire. Women were not excluded if they did not complete the second survey. However, women who had had a fracture in the forearm tested (n = 2), who were missing data on weight (n = 5), or who were pregnant (n = 56) were excluded. A further 99 women were excluded for having one or more comorbid conditions that might affect BMD (six who had undergone surgical or natural menopause, one who had never menstruated, six who were severely physically disabled, 20 with epilepsy, 13 with rheumatoid arthritis, five who had had thyroid surgery, 12 with high metabolism, four with other thyroid diseases, 19 with cancer, and nine in self-reported poor health) and/or for taking medications known to affect BMD (17 taking daily corticosteroids and 18 taking thyroxin). This left a total sample of 963 healthy young women. The 99 women excluded because of a chronic health condition and/or use of medication known to affect BMD were significantly older (difference = 1.09 years, p = 0.027) than the 963 women included in the study and had a lower BMD at the ultradistal site (difference = –0.01 g/cm2, p = 0.049); weight, height, body mass index, calcium intake, and milk consumption were similar in the two groups.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Table 1 shows the characteristics of the study population. The mean age of the sample was 29.7 years (standard deviation 4.7), and the mean and median body mass indices were 24.8 (standard deviation 4.1) and 24.0 (range, 15.7–42.1), respectively. The majority of the subjects were single (58 percent), had a postsecondary education (54 percent), and were employed (88 percent). Ten percent were students. Mean BMD was 0.386 g/cm2 (standard deviation 0.048) for the ultradistal forearm and 0.478 g/cm2 (standard deviation 0.042) for the distal forearm. The two measures of forearm BMD were highly correlated (r = 0.81). Age, anthropometric measures, and calcium intake assessed as continuous variables were positively associated with both ultradistal BMD and distal BMD (p < 0.05). Age at menarche, however, was negatively associated with these outcomes (ß = –0.003 (p = 0.024) and ß = –0.003 (p = 0.008) for ultradistal and distal BMD, respectively).


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TABLE 1. Demographic and other characteristics of women aged 19–35 years (n = 963) in the Osteoporosis Study of the Nord-Trøndelag Health Study, Norway, 1995–1997
 
Table 2 shows the results of bivariate linear regression analysis, displaying mean BMD in categories of osteoporosis risk factors. Values for ultradistal forearm BMD were statistically similar in all age groups. For distal BMD, mean values were significantly higher among women aged 30–35 years than among women aged 19–24 years but were similar to values among women aged 25–29 years. In general, mean BMD increased with increasing weight, height, and body mass index. Although the calcium composite measure was associated with BMD, most of the association was due to milk consumption, and thus milk intake was used in model building. Milk drinkers had significantly higher BMD at both sites (p < 0.05). There was no association between quintiles of caffeine intake and BMD. Caffeine intake was correlated with age (r = 0.42), such that older women were more likely to drink more coffee/tea; however, after adjustment for age, caffeine intake did not reach statistical significance. None of the factors cheese consumption, vitamin D intake, physical activity, smoking, alcohol consumption, amenorrhea, oral contraceptive use, number of pregnancies, history of breastfeeding, and family history of osteoporosis were found to be significantly associated with BMD.


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TABLE 2. Distribution of the study sample and mean bone mineral density values (g/cm2) according to risk factors for low bone mineral density among women aged 19–35 years (n = 963), Nord-Trøndelag Health Study, Norway, 1995–1997
 
In multiple-variable linear regression analysis (table 3), current weight, age (continuous), current milk consumption (yes/no), and age at menarche were independent correlates of BMD at both forearm sites. Weight was the most important factor associated with BMD. The amounts of variance explained by the models were 6.3 percent and 8.0 percent for ultradistal and distal BMD, respectively. Weight alone accounted for 67 percent of the variance explained by these models. Women with late menarche weighed significantly less (64.9 kg, 95 percent confidence interval: 62.9, 66.9) than women who had reached menarche before age 15 years (69.1 kg, 95 percent confidence interval: 68.2, 69.9).


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TABLE 3. Independent correlates of forearm bone mineral density (g/cm2) among women aged 19–35 years (n = 814), Nord-Trøndelag Health Study, Norway, 1995–1997
 
Evaluation of BMD in quintiles produced cutpoints of <0.347 g/cm2 for low ultradistal BMD (n = 188, 19.5 percent) and <0.439 g/cm2 for low distal BMD (n = 190, 19.7 percent). These two measures of low forearm BMD were correlated (Spearman’s r = 0.57). Correlates of low BMD defined in this manner were similar to the results seen in linear regression analysis. In unadjusted logistic regression models (table 4), low forearm BMD was associated with lower weight, lower height, lower calcium intake, and lower age within the range of 19–35 years (distal site only). Factors independently associated with low forearm BMD (table 5) included body weight, milk consumption, and age (distal site only). Similarly to the results of linear regression analysis, weight and milk consumption (yes/no) were independent correlates of low forearm BMD at both sites. Age was not significantly associated with low ultradistal BMD. Neither age at menarche nor late menarche was associated with low BMD at either site. When data were controlled for age and weight, women who did not drink milk daily had twice the odds of low forearm BMD.


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TABLE 4. Unadjusted odds ratio estimates for being in the lowest quintile{dagger} of bone mineral density (g/cm2) among women aged 19–35 years (n = 814), Nord-Trøndelag Health Study, Norway, 1995–1997
 

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TABLE 5. Adjusted{dagger} odds ratio estimates for being in the lowest quintile{ddagger} of bone mineral density (g/cm2) among women aged 19–35 years (n = 832), Nord-Trøndelag Health Study, Norway, 1995–1997
 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The importance of primary prevention of osteoporosis through maximization of peak BMD was highlighted in three recent review articles (3, 17, 18). In general, three classes of factors are thought to influence peak BMD: alterations in hormone concentrations (reproductive, calciotrophic, other), bone-loading (weight, strength, mobility), and lifestyle (nutrition, exposure to alcohol and tobacco) (3, 17). Hormonal factors evaluated in this study included age at menarche, use of oral contraceptives, parity, frequency of breastfeeding, and amenorrhea. Results indicate that among women aged 19–35 years, forearm BMD is negatively associated with increasing age at menarche. Although this finding is consistent with several studies that evaluated correlates of peak BMD (12, 19, 20) and fracture risk among older women (21), other studies have not found an association (10, 22). In fact, a negative but nonsignificant association was found between BMD and age at menarche in a cross-sectional evaluation of forearm BMD among older Norwegian women (22).

The association between later menarche and BMD is thought to be related to lower endogenous estrogen exposure among women with delayed menarche. It is interesting that women with late menarche (age >=15 years) in this study weighed significantly less than those who reached menarche before age 15 (64.9 kg vs. 69.1 kg, p < 0.001). This is similar to findings that girls with a later age at menarche (>14 years) are more likely to be taller and to have less body fat and lower BMD (23). Furthermore, BMD is correlated more highly with fat mass than with lean mass, particularly at skeletal sites high in trabecular bone, such as the forearm and spine (24). It has been suggested that increased fat mass contributes to bone density through the aromatization of androgens to estrogens in adipose tissue.

Similarly, weight was found to be the most important factor associated with BMD in the forearm. Given that the forearm is not a weight-bearing site, unlike the spine and hip, this finding suggests that weight may be a proxy for other factors, such as endogenous estrogen exposure. No associations were found with other variables (parity, breastfeeding, oral contraceptive use, amenorrhea) that are commonly used as proxies for estrogen exposure. This is consistent with findings in older Norwegian women (22) and the current belief that BMD losses during pregnancy and lactation are generally self-correcting (17, 18).

In this study, milk consumption was a significant source of calcium, which was found to be associated with higher BMD values. Retrospective (25) and prospective (26) studies have demonstrated significant increases in BMD among adolescents consuming more milk. Not only is milk beneficial because of its supply of necessary calcium, but milk protein may also suppress osteoclast function (27). Calcium nutrition early in life is important for growth and attainment of peak BMD (11, 2831). A recent cross-sectional assessment found calcium intake to be an important factor associated with radial BMD among girls aged 11–15 years but not among women aged 20–23 years (32), emphasizing the importance of calcium intake during periods of rapid bone accrual. Although current milk consumption was significantly associated with forearm BMD in this study, it was not possible to separate the association for current intake from that for intake during adolescence. Research has found that adult milk consumption is correlated with milk consumption during childhood and adolescence (25). Further research is necessary to evaluate the relative importance of calcium intake in bone mass—that is, the impact of calcium consumption during periods of rapid bone accrual throughout adolescence relative to consumption in young adulthood. Regardless, these data support the notion that developing good habitual milk consumption may lead to increased peak BMD. Paradoxically, Norway has the highest reported rates of milk consumption, yet it also has the highest rates of hip fracture (33, 34).

This study was epidemiologic and population-based, which is a strength. However, it had several limitations. The data were cross-sectional, and hence time sequences could not be established. For some of the factors, the lack of association may have been due to the measures used. For example, the type of exercise that confers the greatest increase in BMD involves relatively intense site-specific loading with high impact forces (3, 35). Research has shown that the dominant forearm is larger than the nondominant forearm, a finding attributed to the presence of more cortical bone in the dominant forearm (30, 3638). Unfortunately, information on exercise was not collected at this level of detail. Further research exploring the impact of upper extremity activity on peak forearm BMD and subsequent protection from fracture would be of interest.

Similarly, studies have identified an association between BMD and family history of lower BMD (10). Although women with a family history of osteoporosis had 1–2 percent lower BMD than those with no family history, these differences did not reach statistical significance. The lack of association in this study may be related to the relative timing of the question, which restricted the identification of family history to parents and siblings (not grandparents) of participants. Given that osteoporosis is a silent disease until it manifests as fragility fractures, it may have been premature to identify familial history only among parents, who may have just been entering middle age. These limitations are highlighted by the fact that only 6–8 percent of variance was explained by the regression models.

Furthermore, total calcium intake may have been underestimated in this study, for several reasons: 1) milk and cheese intakes were truncated at responses of three or more servings per day, 2) data on nondairy sources of calcium were not collected, and 3) information on the quantity of calcium supplements taken was not collected. Perhaps "current milk intake" in this study identified women who were presently consuming sufficient amounts of calcium or, more compellingly, women who had consumed adequate calcium during periods of rapid bone accrual (childhood/adolescence).

Although the focus of this study was evaluation of peak BMD among healthy women, it is interesting to note that the 99 women excluded for having health conditions and/or taking medications predisposing them to bone loss were found to have similar weight, height, and milk consumption as the women included but were older and had significantly lower BMD at the ultradistal site. This finding emphasizes the importance of recognizing the impact of health conditions and medication use on the bone health of young women and of ensuring that adequate prevention or treatment is provided.

To our knowledge, this study was the first to evaluate correlates of peak forearm BMD in women. Results identified greater body weight, increasing age, earlier age at menarche, and milk consumption as independent correlates of higher forearm BMD between the ages of 19 and 35 years. These findings are consistent with previous reports evaluating peak BMD at the hip and spine, which identified weight as the best single predictor of BMD (10), and they support the growing body of literature (25, 27) suggesting a beneficial effect of milk consumption on peak BMD.


    ACKNOWLEDGMENTS
 
The Nord-Trøndelag Health Study (The HUNT Study) is a collaboration between the HUNT Research Centre, Faculty of Medicine, Norwegian University of Science and Technology; the National Institute of Public Health; the National Health Screening Service of Norway; and the Nord-Trøndelag County Council. The Osteoporosis Study in the Nord-Trøndelag Health Study (Principal Investigator, Dr. Berit Schei) was supported by grants from the Norwegian Women’s Health Association, the Norwegian Research Council, the Norwegian Osteoporosis Foundation, and the Foundation for Health and Rehabilitation. Through collaboration with the Bronchial Obstruction Study in the Nord-Trøndelag Health Study (Principal Investigator, Dr. Arnulf Langhammer), AstraZeneca Norway (Oslo, Norway) contributed half the cost of taking bone density measurements in a 5 percent sample of participants aged 20–95 years. The National Institute of Public Health and the National Health Screening Service conducted the data collection.

The authors acknowledge the Atkinson Charitable Foundation (Toronto, Ontario, Canada) for funding the Atkinson Chair in Women’s Health Research, which was held by Dr. Berit Schei at the Center for Research in Women’s Health (a partnership of the Sunnybrook and Women’s College Health Sciences Centre and the University of Toronto). Dr. Gillian A. Hawker is a Scientist of the Medical Research Council of Canada. Suzanne M. Cadarette is supported by a Doctoral Research Award from the Canadian Institutes of Health Research, in partnership with the Ontario Ministry of Health and Long-Term Care. Dr. Susan B. Jaglal is a Career Scientist of the Ontario Ministry of Health and Long-Term Care.


    NOTES
 
Correspondence to Dr. Gillian A. Hawker, Women’s College Ambulatory Care Centre, Sunnybrook and Women’s College Health Sciences Centre, 76 Grenville Street, 10th Floor East, Room 1010, Toronto, Ontario, Canada M5S 1B2 (e-mail: g.hawker{at}utoronto.ca). Back


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 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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