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Effects of projective bone area size of the spine on bone density and the diagnosis of osteoporosis in healthy pre-menopausal women in China

Institute of Metabolism and Endocrinology, The Second Xiang-Ya Hospital, Central South University, Changsha, Hunan 410011, P.R. China

	Abstract

Top Abstract Introduction Methods and subjects Results Discussion References

 
The aim of this study was to understand the effects of projective bone area (BA) size of the spine on bone density and the diagnosis of osteoporosis. Measurements of BA, bone mineral content (BMC), areal bone density (aBMD) and volumetric bone density (vBMD) at the posteroanterior (PA) lumbar spine (vertebrae L2–L4) followed by a paired PA/lateral spine (L2–L4) were made using a dual-energy X-ray absorptiometry (DXA) fan-beam bone densitometer (Hologic QDR 4500A) in 1436 healthy pre-menopausal women aged from 20 to 56-years-old. At the PA and lateral lumbar spine, there was a significant positive correlation between BA and BMC (r=0.762 and 0.762, p=0.000) and aBMD (r=0.370 and 0.352, p=0.000), but not vBMD (r=0.000 and 0.102, p=0.813 and 0.063). When BA at the PA spine changed by one standard deviation (SD), BMC and aBMD correspondingly changed by 12.6% and 4.3% on the basis of their respective means while vBMD indicated no change. When a variation of 1 SD was observed in BA at the lateral spine, BMC, aBMD and vBMD correspondingly changed by 13.8%, 4.4% and 1.73% on the basis of their respective means. Through an intercomparison among large, intermediate and small BA groups, significant differences were found in the means of subject's height, weight, BMC and aBMD at the PA and lateral spine as well as the detection rate of osteoporosis by aBMD (p=0.000). Detection rates of osteoporosis by aBMD at the PA, lateral spine and vBMD in healthy pre-menopausal women aged from 40 years to 56 years were 4.5%, 16.4% and 9.7%, respectively, in the small BA group; 1.3%, 6.4% and 7.3%, respectively, in the intermediate BA group; and 0, 0 and 5.5%, respectively, in the large BA group. No significant differences were found in the detection rates of osteoporosis by vBMD among the groups. The results of multiple linear regression revealed that the major factors influencing BA of the lumbar spine was height. In healthy pre-menopausal women of the same race and age, the BA size of the lumbar spine would have significant influence upon aBMD and the diagnosis of osteoporosis, i.e. the larger the BA, the greater the aBMD and the lower the osteoporosis detection rate while conversely, the smaller the BA, the smaller the aBMD and the higher the osteoporosis detection rate. Though vBMD does not change with BA sizes of the lumbar spine, it is a sensitive marker for diagnosing osteoporosis.

	Introduction

Top Abstract Introduction Methods and subjects Results Discussion References

 
Many studies have determined that among peer age groups of different sexes and races, the areal bone density (aBMD) is exceeded by men compared with women, by blacks compared with whites and by whites compared with Asians [1–10]. However, such sexual [1–3] and racial differences [7–10] diminish or disappear with volumetric bone density (vBMD; real density). It is generally accepted that the main case for the sexual and racial specific differences in aBMD is based on the larger sizes of the male vs. female skeletons [1–3] and the larger sized skeletons in the white vs. Asian race [7, 8]. To evaluate the association of the bone area size of the lumbar spine and bone density as well as the influence of the bone area size upon the diagnosis of osteoporosis in healthy pre-menopausal women of the same race in the same region, we used the dual-energy X-ray absorptiometry (DXA) bone densitometer to scan the posteroanterior (PA)/lateral spine and measured the projected bone area (reflecting the bone size), bone mineral content (BMC), aBMD and vBMD at the PA and lateral spine of subjects. The subjects were subsequently grouped according to the various values of projected bone area (BA); differences in the measurements among these groups and their effects on the diagnosis of osteoporosis were then analysed.

	Methods and subjects

Top Abstract Introduction Methods and subjects Results Discussion References

 
Subjects
1436 healthy pre-menopausal women aged 20–56 years were randomly selected from Changsha and its surrounding area. All subjects were screened by a detailed questionnaire, history and physical examination. Subjects were excluded from the study if they had conditions affecting bone metabolism, such as diseases of the kidney, liver, parathyroid, thyroid, diabetes mellitus, oligomenorrhoea or amenorrhoea before 40 years of age, hyperprolactinaemia, oophorectomy, rheumatoid arthritis, ankylosing spondylitis, malabsorption syndromes, malignant tumours, haematologic diseases and previous pathological fractures. Subjects were also excluded if they had been receiving glucocorticoids, oestrogens, thyroid hormone, fluoride, biphosphonate, calcitonin, thiazide diuretics, barbiturates, antiseizure medications, vitamin D or calcium-containing drugs. All subjects had their body height and weight measured using a stadiometer and standardized balance-beam scale, respectively. Distribution by age of subject weight, height and body mass index (BMI) is shown in Table 1. All participating volunteers gave informed consent.

The in vivo precision deviations on DXA on two repeated BA, BMC, aBMD and vBMD measurements of different BMD values for 33 subjects with the root-mean-square coefficient of variation (RMSCV) [11] were: for the PA spine, 0.89% for the BA, 0.94% for the BMC and 0.86% for the aBMD; and for the lateral spine, 1.53% for the BA, 2.34% for the BMC, 2.06% for the aBMD and 1.99% for the vBMD, respectively. A control PA spine phantom scan was performed each day with a long-term (exceeding 5 years) coefficient of variation (CV) of not greater than 0.40% for the BMD, and intraobserver reproducibility at the phantom PA site (n=25) of 0.59% for the BA, 0.74% for the BMC and 0.44% for the aBMD, respectively, and for the lateral site (n=10) of 0.56% for the BA, 0.28% for the BMC, 0.41% for the aBMD and 0.82% for the vBMD, respectively.

Statistical analysis
The data obtained in this study were analyzed using SPSS 10.0 for Windows statistical software (SPSS Inc., Chicago, IL, USA). The means and standard deviations (SD) for all parameters including BA, BMC, aBMD, and vBMD for all subjects were calculated and expressed as mean±SD. The relationships between BA and BMC, aBMD and vBMD were assessed with linear regression and Pearson correlation analysis. Multiple linear regression was used to determine the major factors influencing BA, BMC and aBMD. All subjects were divided into three groups according to BA at the PA/lateral spine. With the BA of ±1 SD beyond the mean as the cut-off value; the means and SD for all parameters for each group were calculated and the mean values of different parameters from different groups were compared with each other for significant differences and assessed using One-Way ANOVA whenever significant.

Reference to the World Health Organization (WHO) definition [12] and the reference standard established by our group [13], subjects with aBMD or vBMD of 2.5 SD lower than the peak mean of the same gender (T-2.5) were determined osteoporotic. Differences in detection rates of osteoporosis between different groups and parameters were evaluated with Chi-square test.

	Results

Top Abstract Introduction Methods and subjects Results Discussion References

 
Relationships between bone mass and BA
There was a significant positive correlation found between BMC and aBMD at the PA/lateral spine and BA (Figures 1 and 2), but the correlation between vBMD and BA was not statistically significant. Using linear regression equations, results indicated that, with the increase of 1 cm² in BA at the PA spine, BMC and aBMD increased by 1.4605 g and 0.0112 g cm^-2, respectively; with the variation of 1 SD in BA at the PA spine, BMC and aBMD correspondingly changed by 12.6% and 4.3% on the basis of their respective means. With the increase of 1 cm² in BA at the lateral spine, BMC and aBMD increased by 1.1177 g and 0.0124 g cm^-2, respectively; with the variation of 1 SD in BA at the lateral spine, BMC, aBMD and vBMD correspondingly changed by 13.8%, 4.4% and 1.73% on the basis of their respective means. However, vBMD hardly responded to changes in BA at the PA spine.

View larger version (27K): [in this window] [in a new window]   Figure 1. Correlation scatter diagrams of the projective bone area (BA) with (a) bone mineral content (BMC), (b) areal bone mineral density (aBMD) and (c) volumetric bone mineral density (vBMD) at posteroanterior spine (L2–4) in 1436 pre-menopausal women.

View larger version (27K): [in this window] [in a new window]   Figure 2. Correlation scatter diagrams of the projective bone area (BA) with (a) bone mineral content (BMC), (b) areal bone mineral density (aBMD) and (c) volumetric bone mineral density (vBMD) at lateral spine (L2–4) in 1436 pre-menopausal women.

View larger version (18K): [in this window] [in a new window]   Figure 3. The prevalence rates of osteoporosis diagnosed (subjects 40 years of age, n=821) with bone mineral density at different groups according to World Health Organization (WHO) criteria. PA-aBMD, areal bone mineral density at posteroanterior spine; Lat-aBMD, areal bone mineral density at lateral spine; vBMD, volumetric bone mineral density; SBAG, small bone area group; MBAG, medial bone area group; GBAG, great bone area group.

View larger version (19K): [in this window] [in a new window]   Figure 4. Comparison of the prevalence rates of osteoporosis diagnosed (subjects 40 years of age n=821) with parameters in groups reference to World Health Organization (WHO) criteria. SBAG, small bone area group; MBAG, medial bone area group; GBAG, great bone area group; PA-aBMD, areal bone mineral density at posteroanterior spine; Lat-aBMD, areal bone mineral density at lateral spine; vBMD, volumetric bone mineral density.

	Discussion

Top Abstract Introduction Methods and subjects Results Discussion References

Our data demonstrated that BMC and aBMD at the lumbar spine in pre-menopausal women had a significant positive correlation with BA (Figures 1 and 2). However, there was a greater correlation between BMC and BA than that between aBMD and BA, suggesting a closer relationship between skeletal size of the lumbar spine and BMC than with aBMD. Division of BMC by BA partly eliminates the effect of skeletal sizes on aBMD. Little correlation existed between vBMD and BA at the lumbar spine. Calculated using respective regression equations with variation of 1 SD in BA, BMC and aBMD at the PA spine correspondingly changed by 12.6% and 4.3% on the basis of means, respectively, BMC and aBMD at the lateral spine changed by 13.8% and 4.4%, respectively, while vBMD changed by 1.73% (variation in BA at the lateral spine). If the normal distribution range of mean±2 SD for BA at the lumbar spine in healthy pre-menopausal women was taken into consideration, the fluctuating ranges for BMC and aBMD at the PA spine resulting from variation in skeletal sizes would be 50.4% (12.6% x 4 SD) and 17.2% (4.3% x 4 SD), respectively, BMC and aBMD at the lateral spine would be 55.2% (13.8% x 4 SD) and 17.6% (4.4% x 4 SD), respectively, while vBMD would be 6.93% (variation in BA at the lateral spine). Variation in BA at the PA spine did not affect vBMD. The research of Nielsen et al [17] discovered that when BMC and BMD were measured with the planar bone densitometry, there was a significant positive correlation between BMC and BMD of a subject and her body surface area (BS), and variation of BS significantly affected measurements of BMC and BMD and calculation of Z value. Therefore, it is considered that the impact of the size of subjects cannot be ignored when the planar bone densitometry is used to measure BMD in the diagnosis of osteoporosis. It is also suggested that all BMD measurements should be standardized based on the body surface area of a patient.

We found that, when evaluating intercomparison relationships between groups with different BA sizes (Table 2), means of subjects' height, weight, BA, BMC and aBMD revealed significant differences (all p=0.000), and these differences were in increasing order, i.e. MBAG was greater than SBAG and GBAG greater than MBAG. Just as Seeman [18] proposed, a larger bone has a greater aBMD, but its actual density is not actually greater; this is fully supported by the results of our present study. The differences in the means of age, BMI and vBMD of subjects between groups were not significant. Therefore, when age and BMI are matched, the differences in BA, BMC and aBMD between groups may derive from the differences in subjects' height and weight, i.e. subjects with greater height and weight have greater BA, BMC and aBMD, while subjects with smaller height and weight have smaller BA, BMC and aBMD. In summary, the effect of skeletal size on aBMD not only exists between different sexes or races, but also exists in a population of the same sex and race. The results of multiple linear regression indicated that the major factor influencing BA was height. Previous studies indicated that aBMD at the lumbar spine of the Chinese is lower than that of Europeans [10, 19–21]; after adjustment for height, the differences in aBMD between the group disappeared [20, 21]. Delezé et al [22] reported that the aBMD of the population in southern Mexico was lower than northerners due to the shorter stature of the southerners.

Our results also demonstrate a highly significant difference in detection rates of osteoporosis between groups of different BA sizes, between the PA and lateral lumbar spine, and between aBMD and vBMD (Figures 3 and 4). When diagnosed with aBMD, the prevalence rate of osteoporosis in subjects with smaller BA (or smaller skeletal size) was notably higher than that of subjects with larger BA. We understand that the WHO criteria (T-scores-2.5) are only suitable for diagnosis of post-menopausal women with osteoporosis. This research does not primarily focus on accurately assessing the prevalence of osteoporosis, but aims to observe the phenomenon that the number of subjects with T-scores-2.5 changes with BA, in order to suggest the impact of bone projection area of subjects on diagnosis of osteoporosis. We adopted T-score=-2.5 as the critical cut-off value to observe the change of the number of subjects with BA, and Nielsen et al [17] used Z-score as critical cut-off value to observe the change of the number of subjects with BS. The two methods were used to calculate the impact of BA or BS on diagnosis of osteoporosis. The design objective of both is of some significance. However, we adopted T-score=-2.5 as the critical cut-off value (which is equal to the critical cut-off value adopted in the WHO criteria for diagnosis of osteoporosis), which facilitated understanding for readers. We refer to diagnostic methods recommended by WHO, regardless of skeletal size, the same reference standard is used as the diagnostic cut-off value for subjects of the same gender. Therefore, detection rates of osteoporosis in subjects with smaller skeletal sizes are higher because they have lower aBMD (Table 2) while detection rates of osteoporosis in subjects with larger skeletal sizes are lower because of their higher aBMD. When diagnosed with vBMD, no significant difference was detected in the prevalence rates of osteoporosis between groups of different skeletal sizes (Figure 3) since vBMD is not influenced by skeletal size. In the total group (subjects aged from 40 to 56 years old, n=821), detection rates of osteoporosis using aBMD at the PA spine were the lowest (1.6%), using aBMD at the lateral spine intermediate (7.1%), and using vBMD the highest (7.4%), but no significant differences were found in the detection rates of osteoporosis by aBMD at the lateral spine and vBMD. The detection rate of osteoporosis using aBMD at the lateral spine was notably higher than at the PA spine, similar to previous research results [3, 23, 24]. The lower detection rate of osteoporosis at the PA spine results partially from the interference of aortal calcification and/or vertebral hyperplasia related to age [25–27] with the measurement of aBMD at the PA spine while the higher detection rate of osteoporosis at the lateral spine is due to improve the ability of the lateral scan to detect loss of vertebral bone [28, 29]. When the WHO criteria (T-score–2.5) were adopted to diagnose the prevalence of osteoporosis, Faulkner et al [30] discovered that the prevalence of osteoporosis at the heel with ultrasound measurement was 3%; at the spine with quantitative CT (QCT) measurement, 50%; at the PA spine with DXA bone densitometry measurement, 14%; at the lateral spine, 38%; at the forearm, 12%; and at the hip, 6%. Therefore, it is considered that only T-score criteria cannot be universally applicable to all BMD measurements. Considering the accuracy in diagnosis of osteoporosis, we also think that different T-score criteria should be adopted when instruments based on different measurement principles are used or different skeletal regions are measured with the same instrument. However, it is insufficient that we only take such a factor as T-score criteria into consideration, because T-score=(BMD of a subject-mean of peak BMD)/SD of peak BMD, which indicates that T-score is closely associated with BMD of a subject, mean of peak BMD and SD of peak BMD. When BMD of a subject remains constant, variation of T-score depends on mean of peak BMD and SD. If mean of peak BMD is representative or reliable, variation of SD will significantly affect the calculation of T-score [30]. SD reflects BMD distribution status between each individual of peak group at peak age. Calculated from the results reported by Arlot et al [24], coefficients of biological variation of peak BMD at different skeletal regions (SD of peak BMD/mean of peak BMD x 100%) are 6.8% (radius mid-joint) to 17.6% (Ward's triangle). If T-score=–2.5 is adopted as the cut-off value for all criteria, a subject can be diagnosed with osteoporosis when BMD of a subject at radius mid-joint-mean of peak BMD is 17% (6.8% x 2.5). However, a subject can be diagnosed with osteoporosis when BMD of a subject at Ward's triangle-mean of peak BMD is 44% (17.6% x 2.5). Considering this difference between coefficients of biological variation of peak BMD at different skeletal regions, the criteria formulated by the Japanese Society for Bone and Mineral Research used <30% of mean of peak BMD as the critical cut-off value for diagnosis of osteoporosis at different skeletal regions [31]. In this study, we adopted peak BMD [13] recently reported as reference criteria for calculation of T-score. Coefficients of biological variation of aBMD at the PA spine, aBMD at the lateral spine and vBMD were 11.1%, 10.1% and 9.09%, respectively, which were very close to the coefficients of Arlot et al [24]. When we adopted T-score=-2.5 as critical cut-off value, the reduced percentage rates of aBMD at the spine, aBMD at the lateral spine and vBMD were 27.8% (11.1% x 2.5), 25.3% (10.1% x 2.5) and 22.7% (9.09% x 2.5), respectively. Some researchers have also discovered that, for subjects of short stature, the prevalence rate of osteoporosis decreases after adjusting for the effect of skeletal size [8, 32]. Other researchers have found that vertebral volume of the lumbar spine often decreases after vertebral fractures [33–35], and like QCT, vBMD from paired PA and lateral scans are more strongly associated with vertebral fracture than standard aBMD at the PA spine [36].

Our conclusions indicate that the effect of skeletal size of the lumbar spine on aBMD also exists between populations of the same gender in the same area and its influence upon measurement of aBMD and the diagnosis of osteoporosis in healthy pre-menopausal women must be taken into consideration. With regard to the general population or people with larger skeletal sizes, vBMD at the lumbar spine provides a sensitive marker in the diagnosis of osteoporosis.

Received for publication August 19, 2002. Revision received December 20, 2002. Accepted for publication April 24, 2003.

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