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Influence of Puberty on Muscle Area and Cortical Bone Area of the Forearm in Boys and Girls

Research Institute for Children Nutrition (C.M.N., F.M.), 44225 Dortmund; University Children’s Hospital (E.S., E.M.), 50924 Cologne; and Institute of Medical Statistics (G.W.), 50924 Cologne, Germany

Address correspondence and requests for reprints to: PD Dr. E. Schönau, Children’s Hospital University of Cologne, Joseph-Stelzmann-Str. 9, 50924 Cologne, Germany. E-mail: eckhard.schoenau{at}medizin.uni-koeln.de

	Abstract

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The aim of the current study is to analyze the interaction of the muscle and bone system (muscle-bone unit) during puberty in males and females by computed tomography of the nondominant forearm. The data presented here are the first results from 318 healthy children (159 boys and 159 girls), aged 6–22 yr, and 336 adults (parents) participating in the DONALD Study (Dortmund Nutritional and Anthropometric Longitudinally Designed Study). Cortical area (CA) of the radius representing bone strength and muscle area (MA) representing muscle strength were measured with peripheral quantitative computed tomography (XCT 2000; Stratec, Pforzheim, Germany). A single slice measurement at a site corresponding to 65% of the ulnar length proximal to the radial endplate was used. MA and CA of the radius have been determined by a built-in software algorithm using density differences. There was a strong correlation between MA (x) and CA (y) in all children, adolescents, and adults (y = 0.019x + 10.93; r² = 0.77). Before puberty, boys and girls displayed a similar relation between MA and CA. CA in relation to MA was greater in girls than in boys during puberty. Analysis of covariance was performed investigating the dependency of CA on MA, five pubertal stages, sex, and interaction of sex and pubertal stages. MA representing muscle strength was the strongest predictor of CA (P < 0.001) representing bone mass. Pubertal stage (P < 0.001) and interaction of pubertal stage*sex (P = 0.002) also had a significant influence on CA. r² of the model was 0.85. These data suggest that in pubertal girls and women rather than in pubertal boys and men an additional factor shifts the relationship between MA and CA to higher values of cortical area. The present data confirm previous studies of the influence of puberty and estrogens or related factors on the muscle-bone interaction.

	Introduction

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IN 1995, H. M. Frost raised the important question: could estrogen make growing females add more bone than their physical activities need, to store extra calcium for later gestation and lactation (personal communication)? Data from Zanchetta et al. (1) support this hypothesis. This group used dual-energy X-ray absorptiometry to estimate total body bone mineral content and lean body mass in 778 healthy Argentine Caucasian children. These data were reanalyzed by Schiessl et al. (2), who found that bone mass in girls at puberty begins to increase more than in boys with similar lean body masses. Because of methodological and analytical uncertainties in using total bone mineral content and lean body mass as indices of bone and muscle strength, and also because of the potential importance of these findings, additional studies seemed necessary for confirmation. Initial analyses of muscle and bone development during childhood by grip strength and computed tomography (CT) showed a strong correlation between muscle strength and bone geometry [bone strength index, cortical area (CA)], but not between the muscle strength and bone mineral density (spongiosa and cortical bone) (3).

The aim of this study was to analyze the interaction of the muscle and bone system (muscle-bone unit) during puberty in females and males by peripheral quantitative CT at the forearm. The data presented here come from a cross-sectional study of the bone and muscle development in healthy children in dependency on nutrition and physical activities.

	Material and Methods

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Subjects

In 318 healthy children and adolescents (159 boys and 159 girls), aged 6–22 yr, and 336 adults (133 males and 203 females) who took part in the DONALD Study (Dortmund Nutritional and Anthropometric Longitudinally Designed Study) (4), the CA of the radius as in index of bone strength and muscle area (MA) representing muscle strength, were measured with peripheral quantitative CT, using the XCT 2000 machine (Stratec, Pforzheim, Germany). The pubertal stages were determined by the standards of Tanner (5). The subjects undressed to vest and pants and had their height measured to the nearest 1 mm in a standing position, using a digital telescopic wall-mounted stadiometer (Harpenden, Coymych, UK). For weight measurements to the nearest 0.1 kg, an electronic scale (Seca 753 E) was used. Height and weight were within normal ranges for German children and adolescents. Informed consent was obtained from the parents, who stayed with the children while the study was performed. This study was approved by the ethical committee of the medical faculty of the University of Cologne and by the "Bundesamt für Strahlenschutz" (Salzgitter, Germany).

Bone and muscle analysis

Single slice measurements were made at a site corresponding to 65% of the ulnar length proximal to the radial endplate. That site was chosen because in this region the forearm muscles had the highest circumference and cross-section area. The CA and MA were separated by a built-in software algorithm (6).

Statistical methods

Comparisons between the data of the ratio of CA and MA from different groups were carried out using nonparametric tests that compared boys and girls of the five pubertal groups (U test). Analysis of covariance was performed to show the effects of sex and pubertal stages on the dependency of CA to MA (SAS 6.12, PROC GLM)

	Results

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There was a strong correlation between MA (x) and CA (y) of the radius in all children, adolescents, and adults (y = 0.018x + 13.8, r² = 0.77). Fig. 1 shows the different correlations between MA and CA in males and females. Before puberty, boys and girls showed the same relation of MA and CA (Fig. 1). But after puberty, in girls the CA was greater in relation to MA than in boys (Fig. 1).

View larger version (22K): [in this window] [in a new window]   Figure 1. Cortical bone area in relation to MA in prepubertal and pubertal boys and girls.

View larger version (24K): [in this window] [in a new window]   Figure 2. Ratio of CA and MA dependent on the pubertal Tanner stages 1–5 in boys and girls.

View larger version (21K): [in this window] [in a new window]   Figure 3. Regression lines and 95% confidence intervals of the correlation MA vs. periosteal and endosteal circumference.

	Discussion

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During puberty in females, CA increases more rapidly than before puberty, resulting in higher ratios of CA to MA in postpubertal girls than in boys. The presented data showed that the higher values of CA related to MA in females are due to endosteal apposition and not to periosteal expansion. This relationship could also be shown in adults. Further evaluations have to show whether the number of gestations have an influence on the relationship between CA and MA.

These data support ideas about bone development during childhood and adolescence proposed by Frost and the Utah paradigm of skeletal physiology (2, 8, 9, 10). "The largest voluntary loads on bones come from muscles. To adapt bone strength and mass to them, special strain threshold ranges determine where modeling adds and strengthens bone and when remodeling conserves or removes it, just as different thermostat settings control the heating and cooling systems in a house. If estrogens affect the sensitivity of the mechanostat by lowering the remodeling threshold, at puberty in girls, bone mass should begin to increase more rapidly than in boys with similar muscle strengths, due to decreased remodeling-dependent bone losses. The results presented here complement studies by Zanchetta et al. (1), Schiessl et al. (2) and Feretti et al. (11) and support the cited concept. Furthermore, these data are in accordance with studies of radiogrammetry, which showed that premenopausal women have an higher percentage of cortical bone as compared with men (12, 13, 14).

Accordingly, one can argue that the differences in bone adaptations during puberty in males and females are due, at least in part, to estrogens or related factors in females. The importance of this data for understanding the physiology and pathophysiology of bone development has been described in detail by Frost (8). At present, the relevant signal for the change in bone adaptation in girls during puberty is unknown. Is it the mean estrogen level, which is not extremely higher during all times in girls than in boys, or is it the estrogen peak in the mid of menstrual cycle? If the latter is the more important feature, we could speculate that the conventional treatment of ovarian dysfunction, and also early oral contraceptive use without including a mid menstrual estrogen peak, might not optimize the development of peak bone mass in girls.

Furthermore, these data showed that testosterone has no direct influence on the skeletal system during puberty, but might be more important for the higher rate of total muscle mass in boys compared with girls.

In conclusion, the muscle system is an important predictor for bone development in children and adolescents. In pubertal girls, CA, as index of bone strength and bone mass, was greater than in boys with similar muscle strengths. The present data confirm previous studies of the influence of puberty and estrogens or related factors on the muscle-bone interaction.

	Acknowledgments

 
We are gratefully indebted to Dr. H. M. Frost and H. Schiessl for their helpful discussion and review of the manuscript.

Received June 16, 1999.

Revised November 4, 1999.

Accepted November 22, 1999.

	References

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1. Zanchetta JR, Plotkin H, Alvarez-Figueira ML. 1995 Bone mass in children: normative values for the 2–20-year-old population. Bone. 16:3935–3995.
2. Schiessl H, Frost HM, Jee WSS. 1998 Estrogen and bone-muscle strength and mass relationships. Bone. 22:1–6.[Medline]
3. Schoenau E. 1998 The development of the skeletal system in children and the influence of muscular strength. Horm Res. 49:27–31.[CrossRef][Medline]
4. Kersting M, Sichert Hellert W, Lausen B, Alexy U, Manz F, Schöch G. 1998 Energy intake of 1 to 18 year old German children and adolescents. Z Ernä-hrungswiss. 37:47–55.[CrossRef][Medline]
5. Schiessl H, Willnecker J. 1999 Muscle cross sectional area and bone cross sectional area in the human lower leg measured with peripheral computed tomography. In: Lyritis G-P, ed. Musclo skeletal interactions, vol 2. Athens: Hylonome Editions; 47–52.
6. Tanner JM. 1962 Growth at adolescence, 2nd ed. Oxford and Edinburgh: Blackwell.
7. Schoenau E, Westermann F, Mokov E, et al. 1998 The functional muscle-bone-unit in health and disease. In: Schoenau E, Matkovic L, eds. Paediatric osteology. Prevention of osteoporosis–a paediatric task? Singapore: Elsevier Science; 191–202.
8. Frost HM. 1995 Introduction to a new skeletal physiology, vols I and II. Pueblo, CO: Pajaro Group.
9. Frost HM. 1996 Bone development during childhood: insights from a new paradigm. In: Schoenau E, ed. Paediatric osteology: new trends and developments in diagnostic and therapy. Amsterdam: Elsevier Science; 3–39.
10. Jee WSS, Frost HM. 1992 Skeletal adaptions during growth. Triangle. 31:77–88.[Medline]
11. Feretti JL, Capozza RF, Cointry GR, et al. 1998 Gender-related differences in the relationship between densitometric values of whole-body bone mineral content and lean body mass in humans between 2 and 87 years of age. Bone. 22:683–690.[Medline]
12. Matkovic V, Ciganovic M, Tominac C, Kostial K. 1980 Osteoporosis and epidemiology of fractures in Croatia. Henry Ford Hosp Med J. 28:116–126.[Medline]
13. Matkovic V, Badenhop NE, Landoll JD, Ilich JZ, Rosen CJ, Buell JL. 1998 Skeletal growth in a nutrition perspective: genetic and endocrine interaction. In: Schoenau E, Matkovic V, eds. Paediatric osteology: prevention of osteoporosis–a paediatric task? Amsterdam: Elsevier Science; 53–71.
14. Garn SM. 1972 The course of bone gain and the phases of bone loss. Orthop Clin North Am. 3:503–520.[Medline]

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