Calcif Tissue Int (1992) 51:251-254
Calcified Tissue International 9 1992 Springer-Verlag New York Inc.
Clinical Investigations Sex Differences in the Acquisition of Total Bone Mineral Mass Peak Assessed Through Dual-Energy X-Ray Absorptiometry H. Rico, 1 M. Revilla, 1 E. R. Hernandez, 2 L. F. Villa, 1 and M ~- Alvarez del Buergo 1 1Department of Medicine and Rheumatology Unit, Prfncipe de Asturias Hospital, Alcal~ide Henares University, 28801 Madrid, and 2Department of Morphological Science and Surgery, Alcalfi de Henares University, Madrid, Spain Received January 18, 1991, and in revised form February 19, 1992
Summary. Dual energy X-ray absorptiometry evaluation of total body bone mineral content (TBBM), total bone mineral density (TBMD), and regional bone mineral content (BMC) (head, trunk, arms, and legs) was carried out in order to assess sex differences of bone in 120 women and 121 men aged 15-29 years. Subjects from both sexes were divided into 5-year groups (15 through 19, 20 through 24, and 25 through 29 years old, respectively). Significantly higher values for TBBM, TBMD, and regional BMC were observed in males compared with females in the 20 to 24 and 25 to 29year-old groups (P < 0.001), but not in the group aged 15-19. After adjusting TBBM for lean body mass (LBM), we observed significantly lower values of TBBM/LBM in the males compared with females in all the age groups. A positive and significant correlation was observed between TBBM and age in the males of all the groups (r = 0.624, P < 0.001), but not in the females. These data suggest that total bone mass peak acquisition takes place earlier in women than in men, leading to more reduced bone mass value, which in turn may be an osteoporosis predisposing factor.
Key words: Bone mass peak - Bone densitometry - Sex differences.
It is well known that men suffer from osteoporosis to a lesser degree than women [1, 2]. This fact has been related to the marked bone mass loss observed in women after menopause [3, 4]. The incidence of osteoporotic fractures in women would be significantly diminished if the onset of postmenopausal bone mass loss could be delayed a few years [5]. On the other hand, a person may suffer from osteoporosis by not acquiring an appropriate bone mass peak [6, 7], or by having lower bone mass values as a result of acquiring it too early in life, irrelevant of other factors such as considerable bone mass loss. Total body bone mineral content (TBBM) measurement is an accurate and reliable technique for bone mass assessment [8] and presents a higher discriminating index over other techniques [9] for studying normal and pathologic individuals. This method was recently consolidated following the development of dual energy X-ray absorptiometry (DEXA) [10], a technique considered to be very precise [11].
Offprint requests to: H. Rico
Regional bone mass measurements have revealed sex differences [12, 13] and, as it is well known that puberal changes in both males and females are important in the development of the skeletal system [14], we decided to verify whether there was any chronological sex difference in the total body bone mass peak acquisition and if such a difference could account for the changes in the prevalence of osteoporotic fractures in males and females.
Material and Methods DEXA quantification of TBBM, total bone mineral density (TBMD), and regional bone mineral content (head, trunk, arms, and legs) was performed with a Norland XR-26 densitometer (Norland Co., Fort Atkinson, WI, USA) on 241 individuals aged 15-29 years who were considered normal after clinical and analytical assessment and were not taking any medication that could interfere with calcium metabolism. Average 21-minute assessments were performed on all subjects in the supine position and at periods of time far from meals. Our groups has found a variation coefficient of 1.5% in vivo and 0.6% in vitro for this procedure. Bone measurements were repeated in 12 normal males and 10 normal females at intervals varying from 1 to 36 weeks to assess the reliability of repeated measurement. The XR-26 was calibrated weekly with a calibrator supplied by Norland. Body fat percentage (%BF) was also determined and the lean body mass (LBM) was calculated subtracting TBBM from the value of fat-free mass (FFM). The variation rate for %BF was 2.1% and for FFM it was 1.6%. Subjects were divided into 5-year groups (15-19, 20-24, and 2529) according to sex. A total of 120 females participated in the study of whom 38, 41, and 41 were included into the first, second, and third group, respectively. A total of 121 males participated in the study, of whom 46, 39, and 36 were included into similar age categories as the females. Table 1 shows the different characteristics of the six groups under study. Figure 1 shows the TBBM values for males and females. Body mass index was calculated as weight (kg)/ height (m2). A statistical evaluation of TBBM changes according to sex and age group was performed using Student's t test (mean + SD) and a study of the correlation between TBBM and age according to sex was done using Pearson's test. Both studies were carried out on Sigma Plus software.
Results In addition to characteristics, Table 1 shows the TBBM, TBMD, TBBM adjustment for LBM (TBBM/LBM), and regional bone mineral content (head, trunk, arms, and legs)
252
H. Rico et al.: Sex Differences and Peak of Total Body Bone Mineral
Table 1, Characteristics and total body bone mineral, total bone mineral density, and regional bone mineral content (head, trunk, arms, and legs) values in g of the six study groups according to age and sex Females
Males
Females
15-19 years N Weight k Height cm BMIk/m 2 Head g g/cm 2 Trunk g g/cm 2 Arms g g/cm 2 Legs g g/cm 2 TBBM g TBMD g/cm 2 %BF LBMk TBBM/LBM
38 52.6 166 20.3 485 1.9 875 0.85 324 0.87 832 1.16 2542 1.09 26.3 34.9 78.6
Males
Females
20-24 years 46 61.0 171 21.1 492 2.0 933 0.87 397 0.87 875 1.17 2724 1.12 16.4 49.2 55.7
6.8 +-- 7 --- 1.6 +- 73 • 0.2 • 252 --- 0.08 +-- 71 -+ 0.05 +-- 173 --- 0.09 +-- 606 --- 0.08 • 7.5 • 4.1 -+ 8.2
-2_ • • • ----• +• • -+ • • +-
7.6 ~,b 7 2.0 100 0.4 251 b 0.09 b 95b 0.09 b 176b 0.08 b 572b 0.10 b 9.2 7.6 a 5.1 a'b
Males
25-29 years
41 55.1 --- 4.7 167 --- 4 21.4 +-- 2.0 523 --- 75 2.0 +- 0.3 954 • 91 0.86 • 0.08 333 --- 38 0.87-+ 0.06 856 - 87 1.16 0.08 2682 +-- 286 1.10 --- 0.06 28.2 -+ 8.1 37.1 --- 4.3 77.9 • 7.3
39 75.7 174 25.9 517 2.1 1226 0.91 495 0.90 1164 1.21 3320 1.21 16.4 50.3 66.0
+-- 9.7 a -+ 8 -+ 3.8 -+ 106 • 0.4 • 243 a -2_ 0.07 -+ 107a • 0.04 ~ • 261 a --- 0.07t - 401 a • 0.10 a +- 7.6 -!-- 5.2 ~ • 5.9"
41 55.2 165 20.2 512 2.0 963 0.88 326 0.87 814 1.16 2656 1.13 27.7 38.7 73.5
• 5.1 +- 6 3.1 • 69 --- 0.2 --- 125 --- 0.09 • 39 • 0.06 -2_ 85 • 0.07 +- 300 --- 0.09 -+ 7.1 • 4.0 +- 6.8
36 76.1 177 26.2 575 2.2 1246 0.92 499 0.91 1185 1.22 3521 1.22 18.7 58.1 64.4
--- 7.8" ~- 5 -+ 2.7 • 83 • 0.3 a -2_ 266~ • 0.08 c -2_ 574 0.05 d + 145a -+ 0.06 a - 468 ~ --- 0.08 a +- 8.3 • 7.9 a'b • 5.7 a
P < 0.001 vs females of the same age b p < 0.001 vs the other males c p < 0.01 vs females of the same age d p < 0.005 vs females of the same age N = number of cases, BMI = body mass index, %BF = percent body fat, LBM = lean body mass. TBBM/LBM = total body bone mineral adjustment to LBM. P according to Student's t test (mean - SD)
4000 " 3500]
age g r o u p (P < 0.001). N o d i f f e r e n c e s in h e a d B M C w e r e o b s e r v e d regarding age or sex. T h e L B M v a l u e s in m a l e s w e r e significantly h i g h e r (P < 0.001) only in the 25-29 age g r o u p c o m p a r e d w i t h t h e o t h e r t w o g r o u p s , a n d in all t h r e e g r o u p s w h e n c o m p a r e d w i t h f e m a l e s of t h e s a m e age g r o u p s . A f t e r a d j u s t i n g T B B M for L B M we o b s e r v e d significantly l o w e r v a l u e s of T B B M / L B M in the m a l e s c o m p a r e d w i t h f e m a l e s ( P < 0.001) in all t h e age groups, a n d in the m a l e s of t h e y o u n g e s t g r o u p c o m p a r e d w i t h t h e m a l e s of t h e o t h e r g r o u p s (P < 0.001).
p
Calcified Tissue International 9 1992 Springer-Verlag New York Inc.
Clinical Investigations Sex Differences in the Acquisition of Total Bone Mineral Mass Peak Assessed Through Dual-Energy X-Ray Absorptiometry H. Rico, 1 M. Revilla, 1 E. R. Hernandez, 2 L. F. Villa, 1 and M ~- Alvarez del Buergo 1 1Department of Medicine and Rheumatology Unit, Prfncipe de Asturias Hospital, Alcal~ide Henares University, 28801 Madrid, and 2Department of Morphological Science and Surgery, Alcalfi de Henares University, Madrid, Spain Received January 18, 1991, and in revised form February 19, 1992
Summary. Dual energy X-ray absorptiometry evaluation of total body bone mineral content (TBBM), total bone mineral density (TBMD), and regional bone mineral content (BMC) (head, trunk, arms, and legs) was carried out in order to assess sex differences of bone in 120 women and 121 men aged 15-29 years. Subjects from both sexes were divided into 5-year groups (15 through 19, 20 through 24, and 25 through 29 years old, respectively). Significantly higher values for TBBM, TBMD, and regional BMC were observed in males compared with females in the 20 to 24 and 25 to 29year-old groups (P < 0.001), but not in the group aged 15-19. After adjusting TBBM for lean body mass (LBM), we observed significantly lower values of TBBM/LBM in the males compared with females in all the age groups. A positive and significant correlation was observed between TBBM and age in the males of all the groups (r = 0.624, P < 0.001), but not in the females. These data suggest that total bone mass peak acquisition takes place earlier in women than in men, leading to more reduced bone mass value, which in turn may be an osteoporosis predisposing factor.
Key words: Bone mass peak - Bone densitometry - Sex differences.
It is well known that men suffer from osteoporosis to a lesser degree than women [1, 2]. This fact has been related to the marked bone mass loss observed in women after menopause [3, 4]. The incidence of osteoporotic fractures in women would be significantly diminished if the onset of postmenopausal bone mass loss could be delayed a few years [5]. On the other hand, a person may suffer from osteoporosis by not acquiring an appropriate bone mass peak [6, 7], or by having lower bone mass values as a result of acquiring it too early in life, irrelevant of other factors such as considerable bone mass loss. Total body bone mineral content (TBBM) measurement is an accurate and reliable technique for bone mass assessment [8] and presents a higher discriminating index over other techniques [9] for studying normal and pathologic individuals. This method was recently consolidated following the development of dual energy X-ray absorptiometry (DEXA) [10], a technique considered to be very precise [11].
Offprint requests to: H. Rico
Regional bone mass measurements have revealed sex differences [12, 13] and, as it is well known that puberal changes in both males and females are important in the development of the skeletal system [14], we decided to verify whether there was any chronological sex difference in the total body bone mass peak acquisition and if such a difference could account for the changes in the prevalence of osteoporotic fractures in males and females.
Material and Methods DEXA quantification of TBBM, total bone mineral density (TBMD), and regional bone mineral content (head, trunk, arms, and legs) was performed with a Norland XR-26 densitometer (Norland Co., Fort Atkinson, WI, USA) on 241 individuals aged 15-29 years who were considered normal after clinical and analytical assessment and were not taking any medication that could interfere with calcium metabolism. Average 21-minute assessments were performed on all subjects in the supine position and at periods of time far from meals. Our groups has found a variation coefficient of 1.5% in vivo and 0.6% in vitro for this procedure. Bone measurements were repeated in 12 normal males and 10 normal females at intervals varying from 1 to 36 weeks to assess the reliability of repeated measurement. The XR-26 was calibrated weekly with a calibrator supplied by Norland. Body fat percentage (%BF) was also determined and the lean body mass (LBM) was calculated subtracting TBBM from the value of fat-free mass (FFM). The variation rate for %BF was 2.1% and for FFM it was 1.6%. Subjects were divided into 5-year groups (15-19, 20-24, and 2529) according to sex. A total of 120 females participated in the study of whom 38, 41, and 41 were included into the first, second, and third group, respectively. A total of 121 males participated in the study, of whom 46, 39, and 36 were included into similar age categories as the females. Table 1 shows the different characteristics of the six groups under study. Figure 1 shows the TBBM values for males and females. Body mass index was calculated as weight (kg)/ height (m2). A statistical evaluation of TBBM changes according to sex and age group was performed using Student's t test (mean + SD) and a study of the correlation between TBBM and age according to sex was done using Pearson's test. Both studies were carried out on Sigma Plus software.
Results In addition to characteristics, Table 1 shows the TBBM, TBMD, TBBM adjustment for LBM (TBBM/LBM), and regional bone mineral content (head, trunk, arms, and legs)
252
H. Rico et al.: Sex Differences and Peak of Total Body Bone Mineral
Table 1, Characteristics and total body bone mineral, total bone mineral density, and regional bone mineral content (head, trunk, arms, and legs) values in g of the six study groups according to age and sex Females
Males
Females
15-19 years N Weight k Height cm BMIk/m 2 Head g g/cm 2 Trunk g g/cm 2 Arms g g/cm 2 Legs g g/cm 2 TBBM g TBMD g/cm 2 %BF LBMk TBBM/LBM
38 52.6 166 20.3 485 1.9 875 0.85 324 0.87 832 1.16 2542 1.09 26.3 34.9 78.6
Males
Females
20-24 years 46 61.0 171 21.1 492 2.0 933 0.87 397 0.87 875 1.17 2724 1.12 16.4 49.2 55.7
6.8 +-- 7 --- 1.6 +- 73 • 0.2 • 252 --- 0.08 +-- 71 -+ 0.05 +-- 173 --- 0.09 +-- 606 --- 0.08 • 7.5 • 4.1 -+ 8.2
-2_ • • • ----• +• • -+ • • +-
7.6 ~,b 7 2.0 100 0.4 251 b 0.09 b 95b 0.09 b 176b 0.08 b 572b 0.10 b 9.2 7.6 a 5.1 a'b
Males
25-29 years
41 55.1 --- 4.7 167 --- 4 21.4 +-- 2.0 523 --- 75 2.0 +- 0.3 954 • 91 0.86 • 0.08 333 --- 38 0.87-+ 0.06 856 - 87 1.16 0.08 2682 +-- 286 1.10 --- 0.06 28.2 -+ 8.1 37.1 --- 4.3 77.9 • 7.3
39 75.7 174 25.9 517 2.1 1226 0.91 495 0.90 1164 1.21 3320 1.21 16.4 50.3 66.0
+-- 9.7 a -+ 8 -+ 3.8 -+ 106 • 0.4 • 243 a -2_ 0.07 -+ 107a • 0.04 ~ • 261 a --- 0.07t - 401 a • 0.10 a +- 7.6 -!-- 5.2 ~ • 5.9"
41 55.2 165 20.2 512 2.0 963 0.88 326 0.87 814 1.16 2656 1.13 27.7 38.7 73.5
• 5.1 +- 6 3.1 • 69 --- 0.2 --- 125 --- 0.09 • 39 • 0.06 -2_ 85 • 0.07 +- 300 --- 0.09 -+ 7.1 • 4.0 +- 6.8
36 76.1 177 26.2 575 2.2 1246 0.92 499 0.91 1185 1.22 3521 1.22 18.7 58.1 64.4
--- 7.8" ~- 5 -+ 2.7 • 83 • 0.3 a -2_ 266~ • 0.08 c -2_ 574 0.05 d + 145a -+ 0.06 a - 468 ~ --- 0.08 a +- 8.3 • 7.9 a'b • 5.7 a
P < 0.001 vs females of the same age b p < 0.001 vs the other males c p < 0.01 vs females of the same age d p < 0.005 vs females of the same age N = number of cases, BMI = body mass index, %BF = percent body fat, LBM = lean body mass. TBBM/LBM = total body bone mineral adjustment to LBM. P according to Student's t test (mean - SD)
4000 " 3500]
age g r o u p (P < 0.001). N o d i f f e r e n c e s in h e a d B M C w e r e o b s e r v e d regarding age or sex. T h e L B M v a l u e s in m a l e s w e r e significantly h i g h e r (P < 0.001) only in the 25-29 age g r o u p c o m p a r e d w i t h t h e o t h e r t w o g r o u p s , a n d in all t h r e e g r o u p s w h e n c o m p a r e d w i t h f e m a l e s of t h e s a m e age g r o u p s . A f t e r a d j u s t i n g T B B M for L B M we o b s e r v e d significantly l o w e r v a l u e s of T B B M / L B M in the m a l e s c o m p a r e d w i t h f e m a l e s ( P < 0.001) in all t h e age groups, a n d in the m a l e s of t h e y o u n g e s t g r o u p c o m p a r e d w i t h t h e m a l e s of t h e o t h e r g r o u p s (P < 0.001).
p
