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Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2006-0136
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The Journal of Clinical Endocrinology & Metabolism Vol. 91, No. 7 2555-2561
Copyright © 2006 by The Endocrine Society

Change in Cortical Bone Density and Its Distribution Differs between Boys and Girls during Puberty

Saija A. Kontulainen, Heather M. Macdonald and Heather A. McKay

Departments of Orthopaedics (S.A.K., H.A.M.) and Family Practice (H.A.M.), Faculty of Medicine, and School of Human Kinetics (H.M.M.), University of British Columbia, Vancouver, Canada V5Z 1L8

Address all correspondence and requests for reprints to: Heather McKay, Room 588, Department of Orthopaedics, University of British Columbia, 828 West 10th Avenue, Vancouver, British Columbia, Canada V5Z 1L8. E-mail: heather.mckay{at}family.med.ubc.ca.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Concept: Postmenarchal girls and premenopausal women have 3–4% higher cortical bone density (CoD, milligrams per cubic centimeter), compared with postpubertal boys and men, respectively. Females’ denser cortical bone is thought to serve as a calcium reservoir for reproductive needs. However, prospective data are lacking that describe CoD development and bone mineral density distribution during puberty in both sexes.

Objective: Thus, our objectives were to assess maturity and sex differences in the 20-month change of CoD and radial distribution of bone mineral density (RDBMD, milligrams per cubic centimeter) in early-, peri-, and postpubertal girls and boys. Maturity groups were based on change in menarcheal status (girls, n = 68) and pubic hair stage (Tanner) (boys, n = 59). Peripheral quantitative computed tomography was used to measure CoD and RDBMD at the tibial middiaphysis.

Results: The increase in average CoD was 1.9% [22.8 mg/cm3; 95% confidence interval (CI), 10–36], 2.8% (33.8 mg/cm3; 95% CI, 21–47), and 1.5% (55.0 mg/cm3; 95% CI, 17–93) greater in early, peri-, and postpubertal girls, compared with boys, respectively. Analysis of RDBMD revealed that the change in density distribution varied across pubertal groups in girls. Across puberty, all girls showed an increase in the high density midcortical region, whereas only peripubertal girls showed an increase in the lower density subcortical region. A sex-difference in RDBMD change was noted within early and peripubertal groups.

Conclusions: Our findings of sexual dimorphism in CoD development give support to the hypothesis that female bone deposits calcium for reproductive needs by consolidation of cortical bone during puberty.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
IMPROVED KNOWLEDGE OF sexual dimorphism in bone growth and development may help us to better understand sex differences in the aging skeleton and provide valuable insight to primary and secondary fracture prevention. More than 30 years ago, Garn and colleagues (1, 2, 3) compared the second metacarpal bone using radiography across several age groups of both sexes and noted endosteal (i.e. endocortical) apposition of bone in both sexes. Because endosteal apposition began earlier and was of greater magnitude in girls than boys, they proposed that endosteal apposition in girls was a result of the pubertal estrogen surge that supplied calcium for reproduction (1, 2, 3).

More recently it was suggested the mineral storage for reproductive needs can also be obtained by increasing (volumetric) cortical bone density (CoD) (4). Measurement with peripheral quantitative computed tomography (pQCT) showed that adolescent girls after Tanner stage 3 and adult women had 3–4% higher CoD at the proximal radius, compared with their maturity- and age-matched male counterparts (5, 6, 7). Conversely, girls and boys at different stages of maturity had similar CoD at the femoral shaft when measured by QCT (8). The only prospective investigation that assessed changes in CoD over 2 yr in pubertal girls showed a gradual increase in CoD (9). To our knowledge, there are no longitudinal studies that have investigated both sex- and maturity-specific differences in the development of CoD across puberty.

Cortical bone is often assumed to be a uniform tissue; however, this is likely an oversimplification. Bousson et al. (10, 11) showed that for bone specimens of both sexes, bone density was lowest close to the endosteal area in the subcortical region and higher in midcortical and periosteal regions due to greater porosity in the subcortical region. Similar regional differences were obtained in pre- and postmenopausal women when pQCT scans were analyzed based on low-, medium-, and high-density areas (12). Interestingly, high- and medium-density areas were 16–20% lower in postmenopausal, compared with premenopausal, women (12). Only one study has described the change in radial distribution of bone mineral density in vivo within an axial slice of the femur and tibia, and this was with postmenopausal women (13). Density increased from the subcortical region toward the midcortex after hormone replacement therapy and/or high-impact physical exercise (13). According to the proposed theory, the increase in CoD is due to increased cyclical secretion of estrogens after menarche (or hormone replacement therapy) that leads to reduced bone turnover, decreased intracortical remodeling, and less porous cortical tissue (14, 15). In other words, estrogen secretion in puberty may cause packing of excess mineral into female bones for reproductive needs (4, 16, 17, 18).

Our aim was to prospectively investigate whether the development of cortical bone mineral density differs between sexes across puberty. Specifically, our primary objectives were to assess maturity and sex differences in average CoD (milligrams per cubic centimeter) at baseline and compare CoD change over 20 months in early and peri- and postpubertal girls and boys. Our secondary objective was to describe the radial distribution of bone mineral density (RDBMD; milligrams per cubic centimeter) and compare its change over 20 months in these girls and boys.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects were healthy children and adolescents [68 girls and 59 boys, mean age 11.9 (SD 0.6) yr at baseline] and were participants in the University of British Columbia Healthy Bones Study II (19, 20). The Ethical Review Board at the University of British Columbia approved the protocol, and all parents and participating children signed informed consent.

Maturity

Maturity was assessed by menarcheal status and self-reports of breast (girls) and pubic hair (boys) stage (21). Menarcheal status was assessed by questionnaire at both measurement times. Girls were grouped into one of three maturity groups according to their menarcheal status over the 20-month period. Girls in group 1 (EARLY) were premenarcheal at baseline and remained premenarcheal. Group 2 (PERI) girls were premenarcheal at baseline but reached menarche during the follow-up period. Group 3 (POST) girls were postmenarchal at baseline. For boys, maturity group was based on Tanner pubic hair stage at the end of the study: Tanner stages 1, 2, or 3 were considered early pubertal (EARLY), those at Tanner stage 4 peripubertal (PERI), and those at Tanner stage 5 postpubertal (POST).

Anthropometry and questionnaires

The following procedures were completed at baseline and 20 months. Standing height was measured to the nearest 0.1 cm using a wall-mounted digital stadiometer (model 242; Seca, Hanover, MD), and body weight was measured to the nearest 0.1 kg using an electronic scale (Seca model 840). We measured tibial length as the distance from the distal edge of the medial malleus to the tibial plateau using an anthropometric tape. The mean of two measures for each variable was used for analysis.

Bone measures

We used pQCT (Stratec XCT 2000, Stratec Medizintechnic GmbH, Pforzheim, Germany) measurements to acquire a single 2.5-mm slice (voxel size 0.5 mm) of the left tibia. A 30-mm planar scout view over the joint line was performed to define the anatomical reference line. A reference line was set in the middle of the subchondral bone at the distal tibia. The measurement site was 50% of the tibial length proximal to the reference line. In our laboratory, the short-term precision for CoD for 14 young subjects was 0.4% at the tibial middiaphysis. A phantom was scanned daily to maintain quality assurance.

The pQCT scans were analyzed using Bonalyse software (Bonalyse 2.1, BonAlyse Oy, Jyväskylä, Finland). A threshold algorithm without a contour (D-mode), with a threshold of 171 mg/cm3 was used to separate bone from soft tissue and define periosteal surface (19). A threshold of 540 mg/cm3 was used to define the endosteal surface of the cortex (19). Density thresholds were determined from histogram profiles of the bone images. Our primary outcome variables were baseline and 20-month change in average apparent CoD (milligrams per cubic centimeter), and our secondary outcome variables were baseline and 20-month change in the RDBMD (milligrams per cubic centimeter). Following the anatomical shape of the bone, Bonalyse software defines RDBMD by dividing bone into 20 concentric rings from the center of bone mass to the outer bone edge and calculates the average density for each ring (Fig. 1Go). We refer to rings 1–7 as bone marrow (density less than 171 mg/cm3), rings 8–11 as subcortical bone (densities between 171 and 540 mg/cm3), and rings 12–20 as cortical bone (density greater than 540 mg/cm3). Average bone mineral density for rings 9–19 was used in the analysis (RDBMD9–19). We excluded rings 8 and 20 to avoid the partial volume effect on bone surfaces (4).


Figure 1
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  		FIG. 1. RDBMD. Rings 1–7 refer to bone marrow cavity; rings 8–11, subcortical bone; and rings 12–20, cortical bone.

 
Statistical analysis

Baseline differences between sexes and maturity categories were assessed with ANOVA. The dependent variable was the baseline value of the primary outcome variables (CoD, RDBMD9–19) and (fixed) factors were sex (male, female) and maturity category (EARLY, PERI, POST). A separate ANOVA to assess differences between maturity categories within sex, and between sexes within each maturity category, was performed if a statistically significant main effect and/or interaction between dependent variable and factors was noted.

Change in CoD and RDBMD9–19 within each maturity group was assessed with a paired-samples t test. Between-maturity and between-sex differences in change in CoD and RDBMD9–19 were evaluated with analysis of covariance. Dependent variables were follow-up values of CoD and RDBMD9–19 and (fixed) factors were sex (male, female) or maturity category (EARLY, PERI, POST). Baseline values were used as covariates. Multiple comparisons were adjusted by Bonferroni’s method. Data were analyzed with SPSS (version 13.0; SPSS Inc., Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Baseline data

Anthropometry for all subjects is provided in Table 1Go.


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  		TABLE 1. Baseline and follow-up characteristics of subjects

 
We found no main effects of sex or maturity for baseline CoD, but there was a significant interaction (P < 0.001) between maturity and sex. For baseline RDBMD9–19, there was a significant main effect of sex (P < 0.001) and an interaction between maturity and sex (P < 0.037).

Comparison of CoD and RDBMD9–19 across maturity groups within sex

At baseline, POST girls had 3.4% [36 mg/cm3; 95% confidence interval (CI) 13–59] greater CoD than EARLY girls and 4.1% (45 mg/cm3; 95% CI, 24–66) greater CoD than PERI girls. Among boys, baseline CoD differed between POST and EARLY groups; POST boys had 4.3% (35 mg/cm3; 95% CI, 6–36) lower CoD than EARLY boys (Table 2Go).


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  		TABLE 2. Baseline, follow-up (mean, SD) and change in CoD ({Delta}, 95% CI) and the sex difference in CoD change ({Delta} difference, 95% CI)

 
The RDBMD curve showed a wide spectrum of bone mineral densities within the cortex in both sexes across maturity categories (Figs. 2Go and 3Go). The only difference between maturity groups in baseline RDBMD9–19 was obtained in girls; PERI girls had 2.2% (25.2 mg/cm3; 95% CI, 2–49) greater density in ring 15 than EARLY girls.


Figure 2
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  		FIG. 2. RDBMD change within maturity groups in girls: early (A), peri- (B), and postpubertal groups (C).

 

Figure 3
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  		FIG. 3. RDBMD change within maturity groups in boys: early (A), peri- (B), and postpubertal groups (C).

 
Sexual dimorphism in CoD and RDBMD9–19 across maturity groups

Baseline CoD differed between sexes in the PERI and POST groups. PERI girls had 3% (25 mg/cm3; 95% CI, 5–45) greater CoD than PERI boys. POST girls had 10% (91 mg/cm3; 95% CI, 68–115) greater CoD than POST boys (Table 2Go). A sex difference in baseline RDBMD9–19 was also noted in PERI and POST groups (Table 3Go). Compared with boys, PERI girls had greater density in rings 15–17 and POST girls had greater density in rings 13–19 (Table 3Go).


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  		TABLE 3. Change in RDBMD9–19 ({Delta} , 95% CI) and the sex difference in RDBMD9–19 change ({Delta} difference, 95% CI)

 
Twenty-month changes

Changes within maturity groups. In girls, CoD increased statistically significantly across maturity groups. Average CoD increased by 1.9% in EARLY girls, 4.2% in PERI girls, and 2.7% in POST girls (Table 2Go). Among boys, CoD increased in the PERI group only (1.3%) (Table 2Go).

Analysis of RDBMD9–19 change showed an increased density across the cortex from the subcortical region close to the periosteal surface. In EARLY and PERI girls, density increased in rings 13–19 and 9–16, respectively (Table 3Go and Fig. 2Go, A and B). In POST girls density increased in rings 15–17 (Fig. 2CGo). In EARLY boys density increased near the periosteal boundary (ring 18) only (Table 3Go and Fig. 3AGo), whereas in PERI boys density increased across the cortex in rings 8, 9, 11, 12, 14, and 15 (Table 3Go and Fig. 3BGo). In POST boys, RDBMD9–19 did not change statistically significantly (Table 3Go and Fig. 3CGo).

Comparison across maturity groups within sex. We found significant main effects of both maturity (P < 0.05) and sex (P < 0.01) for CoD and RDBMD9–19 changes when adjusted for baseline values. In girls, CoD increased 2.0% (19 mg/cm3; 95% CI, 10–30) more in the PERI group, and 0.8% (17 mg/cm3; 95% CI, 5–29) more in the POST group than the EARLY group (Table 2Go and Fig. 3Go). In boys, CoD change was similar across maturity groups (Table 2Go and Fig. 3Go).

The only statistically significant difference in RDBMD9–19 change was found between EARLY and PERI girls. PERI girls had a 2.3% (28.3 mg/cm3; 95% CI, 6–51) greater increase in ring 15 density than EARLY girls.

Sexual dimorphism across maturity groups. CoD increased significantly more in girls than boys across all maturity groups (Table 2Go). The increase in CoD was 1.9% (23 mg/cm3; 95% CI, 10–36), 2.8% (34 mg/cm3; 95% CI, 21–47), and 1.5% (55 mg/cm3; 95% CI, 17–98) greater for EARLY, PERI, and POST girls, respectively, compared with boys in the same maturity groups.

The sex difference in RDBMD9–19 change was obtained for EARLY and PERI groups. In the EARLY group, girls had a greater increase in density in rings 13–17 (Table 3Go). In the PERI group, girls had a greater increase in density in rings 10–15, whereas PERI boys had a greater increase in ring 18 density (Table 3Go).


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
We prospectively assessed CoD development and radial distribution of bone mineral density across the axial plane of the tibial diaphysis in early and peri- and postpubertal girls and boys. Over 20 months, girls had a 2–3% greater increase in CoD than boys in each maturity group. Peripubertal girls, who reached menarche during the follow-up, showed the greatest increase in average CoD and consolidation in the subcortical region.

This is the first investigation of CoD changes across early and peri- and postpuberty in both sexes. It has been proposed from cross-sectional pQCT studies that at puberty, girls acquire mineral storage in cortical bone by endosteal apposition (2), and increased bone mineral density (4). Our data provide evidence for the latter: girls demonstrated not only higher baseline values but also a greater increase in CoD at the tibial middiaphysis, compared with boys, at similar maturational stages. These results extend recent cross-sectional comparisons of sex differences in CoD at the femoral and radial shafts (4, 5, 22). Contrary to those studies that indicated endosteal apposition (endocortical contraction) in girls (1, 2, 3, 9, 23, 24), we found in our previous investigation of this same cohort that the area of marrow cavity increased at the tibial middiaphysis in early and peripubertal girls and remained stable in postpubertal girls (19).

In the present study, we assessed the distribution of bone mineral density throughout the cortex by radial distribution of bone mineral density curves. The general shape of the radial distribution curve within the cortical wall was similar between sexes. Bone density increased from the subcortical region toward the midcortex and dropped slightly before the periosteal surface. Previous work showed that CoD is related to cortical porosity at the femoral diaphysis in vitro (10). Porosity in inner parts of the cortex becomes more pronounced with age, especially in women, resulting in significant cortical thinning (11, 12, 25). In growing bone, low density bone in the subcortical region may be due to the presence of resorption spaces resulting from enlargement of the marrow cavity and cortical drift (26). In contrast, high CoD in the midcortex may be related to lower porosity (25) that may reflect differences in Haversian bone structure, compared with other regions of the cortex (27). The lower CoD values in the farthest ring at the periosteal surface may reflect the presence of primary osteons and newly formed, less mineralized circumferential lamellae. In addition, lower densities near bone surfaces are a result of the partial volume effect due to low spatial resolution of the pQCT technique. We tried to avoid the influence of partial volume effect in the analysis of RDBMD by excluding rings at the periosteal (ring 20) and endosteal (ring 8) bone surfaces.

Our findings indicate that consolidation of bone throughout the cortical wall occurs in pubertal girls. Girls who reached menarche during the follow-up showed consolidation, especially in the subcortical region. We defined the subcortical region based on RDBMD ring density values above 171 mg/cm3 and less than 540 mg/cm3. Defined boundaries that narrow this transitional zone between cortical and cancellous bone tissue are not generally accepted in bone histomorphometry (28). Furthermore, there are no standardized methods to select threshold or gray-scale values that define periosteal and endosteal surfaces or subcortical boundaries in bone imaging. Currently the pQCT manufacturer recommends using a threshold of 710 mg/cm3 to define the endosteal border of cortical bone (http://www.stratec-med.com/literatur/manuals/man55eres.pdf). This protocol may exclude a significant amount of lower density bone from the analysis, particularly in growing bone with a high (re-)modeling rate. There is an immediate need for validation studies of pQCT analysis protocols used to assess bone geometry and density of the growing, mature, and aging skeleton.

Change in CoD and its distribution were related to maturation and sex. Postpubertal girls had greater CoD at baseline than both early and peripubertal girls and postpubertal boys. In addition, CoD increased further in postpubertal girls, especially in the high-density midcortical region. Although pQCT has insufficient spatial resolution to image porosity or material density across the cortex, regional differences in density distribution across the cortical wall were related to tissue porosity (10). Young men (20–44 yr) have higher porosity in the subcortical and midcortical regions of the femur in vitro (25). Apart from density and size of osteons, cortical porosity depends on the size of the remodeling spaces and rate of intracortical remodeling (29). The proportion of bone cortex occupied by secondary osteons was related to the loading environment in the sheep femur (30). We have previously shown that increases in height, weight, lean mass, tibial length, and muscle cross-sectional area were significantly greater for boys than girls over 20 months (20). In addition, level of physical activity (as measured by questionnaire) was greater in boys (20). Thus, the mechanical demands on the tibial shaft were likely greater in boys, compared with girls. This may have caused more microdamage in boys’ cortical bone, which may have resulted in increased intracortical remodeling (30).

In addition to mechanical loading, bone turnover during puberty is regulated by several local and systemic factors (15, 31). Due to the central role of estrogen in bone turnover (15, 31, 32) and proposed theory of postmenarchal consolidation of bone (4), we were interested in CoD and RDBMD changes in peripubertal girls who reached menarche during the follow-up. Peripubertal girls had the greatest increases in average CoD and RDBMD. Interestingly, early pubertal girls had a greater increase in CoD, compared with boys. Although estrogen levels are low in prepubertal girls and boys, girls have an 8-fold higher estrogen level than boys already at prepuberty (33). Estrogen is thought to have a biphasic role in bone growth in both sexes; lower levels stimulate growth, possibly by stimulating GH and IGF-I, and higher levels reduce growth and lead to the closure of the epiphyseal growth plates (15, 31, 32). The rise in estrogen levels and cyclical secretion of estrogen at menarche in girls is associated with a large reduction in bone turnover markers, reflecting reduction in periosteal apposition, endosteal resorption, and bone remodeling (15). As a result of reduced intracortical remodeling activity, cortical porosity decreases and tissue density increases (27, 34). Further research is needed to clarify the possible relationship between bone mineral distribution and Haversian bone remodeling.

Although the longitudinal component of our study design allows for the description of bone density development within maturational groups in both sexes, we acknowledge the limitations of cross-sectional comparisons between maturity categories and sexes. Girls and boys were divided into representative maturational stages, but these categories are unable to capture the continuing process of growth or differences in the timing and tempo of maturation (35). In addition, Tanner staging is not ideal for between-sex comparisons (35, 36). We categorized girls based on their menarcheal status and boys according to their pubic hair development. Age at menarche is strongly associated with age a peak height velocity (36) and coincides with peak bone accrual (37). Longitudinal dual-energy x-ray absorptiometry studies have shown that at Tanner stage 4, 95% of boys have attained peak height velocity (36), but an additional 8 months are needed to attain peak bone mineral accrual (6, 7, 37, 38, 39). Therefore, it is possible that peripubertal boys in our sample might consolidate cortical bone later in puberty and eventually reach girls’ CoD values. Postpubertal boys had lower and similar CoD at baseline, compared with early and peripubertal boys, respectively, and the increase in CoD was similar across maturity groups. Comparisons within sex across our maturity groups must be interpreted cautiously, particularly within the POST group due to the small number of boys (n = 9). However, the finding that premenopausal women have 3–4% higher CoD at the radius, compared with same-age male counterparts (36), supports our findings. Finally, because we did not measure cyclical secretion of estrogen or other hormones directly, we can only speculate about the biological processes that may underpin our findings. Future studies that establish maturity time points from individual growth trajectories will provide a better basis of comparison across sexes. In addition, studies that assess bone markers and endo- and paracrine regulation of bone growth are needed to confirm our observations.

In summary, our observations with prospective pQCT measurements provide important evidence that pubertal girls do not necessarily experience greater endosteal apposition (19) but seem to consolidate cortical bone at the subcortical and midcortical regions more than pubertal boys. These findings of sexual dimorphism in cortical bone density development are consistent with the hypothesis that female bone deposits calcium for reproductive needs during puberty.


   Footnotes
 
This work was supported by grants from the Ministry of Education, Finland; Academy of Finland; Michael Smith Foundation for Health Related Research (postdoctoral studies, to S.A.K.). Canadian Institutes for Health Research is acknowledged for the financial support to conduct this study.

Conflict of interest: S.A.K., H.M.M., and H.A.M. have nothing to declare.

First Published Online April 24, 2006

Abbreviations: CI, Confidence interval; CoD, cortical bone density; pQCT, peripheral quantitative computed tomography; RDBMD, radial distribution of bone mineral density.

Received January 23, 2006.

Accepted April 13, 2006.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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