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Effects of physical training on cortical bone at midtibia assessed by peripheral QCT

¹Institute of Health and Sport Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8574; and ²National Institute of Advanced Industrial Science and Technology, Tsukuba, Ibaraki 305-8564, Japan

Submitted 18 November 2002 ; accepted in final form 19 February 2003

	ABSTRACT

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Effects of long-term exercise on volumetric bone mineral density (vBMD), bone mineral content, bone geometric properties, and the strength indexes of bone were examined in a cross-sectional study of athletes and controls. Tibias of 25 jumpers (13 women), 30 swimmers (15 women), and 25 controls (15 women), aged 18–23 yr, were scanned at midsite by using peripheral quantitative computed tomography. The cortical vBMD of female athletes was lower than that of the controls (2.00 ± 0.05, 1.90 ± 0.08, and 1.92 ± 0.12 g/cm³, respectively, for controls, swimmers, and jumpers). On the other hand, periosteal areas of male jumpers and female athletes were greater than that of controls (460 ± 50, 483 ± 46, and 512 ± 55 mm², respectively, for male controls, swimmers, and jumpers, and 283 ± 52, 341 ± 73, and 378 ± 75 mm², respectively, for female controls, swimmers, and jumpers). The endocortical area of female swimmers was greater than that of controls (103 ± 29, 148 ± 52, and 135 ± 54 mm², respectively, for controls, swimmers, and jumpers). The polar moment of inertia and strength strain index of male jumpers and female athletes were significantly greater than those of controls, except for the difference in strength strain index between male jumpers and controls. We conclude that the improvement of mechanical properties of young adult bone in response to long-term exercise is related to geometric adaptation and not to vBMD.

jumper; swimmer; volumetric bone mineral density; bone geometric properties; bone strength indexes; peripheral quantitative computed tomography

The positive effect of physical activity on human bone mass has been well documented in many cross-sectional studies comparing athletes with sedentary controls (3, 8, 11, 14, 16, 17, 21, 23, 29, 42, 43). One of the early studies using DXA of adolescent athletes reported enhanced areal BMD (aBMD) of distal femur (29) and whole body in athletes (11, 43). Furthermore, comparison of aBMD among athletes revealed the importance of impact loading to increase aBMD. Young female athletes who engage in impact loading sports, such as volleyball and gymnastics, have a greater aBMD at a majority of skeletal sites, compared with controls and athletes in an active loading sport, such as swimming, in which loading occurs through muscle strain (6, 11, 26, 43). On the other hand, a previous study assessed the effect of physical activity on the side-to-side differences of tennis players' radii using pQCT and showed that tennis playing led to a slight decrease in cortical vBMD but increase in both periosteal and endocortical bone area at midradius (1). It revealed that an improvement of the mechanical properties of young adult bone in response to long-term unilateral use in exercise is related more to geometric adaptation than to changes in vBMD (1). The preceding observations have been confirmed in a study of professional tennis players by Haapasalo et al. (15).

Because adaptation of bone to physical exercise depends on the nature of the exercise, the following questions remain. 1) Does exercise involving active loading but less impact, such as swimming, also induce changes in bone geometric properties? 2) Does extremely high-impact exercise increase vBMD? The purpose of the present study was to evaluate the effect of long-term exercise on vBMD, geometric properties, and the bone strength indexes of jumpers as a high-impact loading group and swimmers as a nonimpact and active loading group, compared with nonathletic controls, by using pQCT.

	MATERIALS AND METHODS

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Subjects. A study population comprising 37 male adults (10 controls, 15 swimmers, and 12 jumpers) and 43 female adults (15 controls, 15 swimmers, and 13 jumpers), aged 18–23 yr, was recruited from the University of Tsukuba, Japan. The jumpers, including long-jump, high-jump, triple-jump, and pole-jump athletes, and the swimmers, including backstroke, breast-stroke, butterfly stroke, and freestyle swimming athletes, were active top level. The controls consisted of gender- and age-matched sedentary nonathletes. Training history, age at training onset, and condition of menorrhea (female participants were asked to recall the menarche age and the menstrual cycles over the past year) were investigated by direct interview. The exercise, smoking, and alcohol use habits and medical history were obtained through questionnaires. The subjects were clinically healthy, and none had any disease, took medication affecting bone metabolism, or had had tibial fractures, except for one jumper, who had had a left tibial fracture. Group characteristics are given in Table 1. Written, informed consent was obtained before the study, and the project was approved by the University of Tsukuba Human Subjects Institutional Review Board.

Bone measurement. The midtibia of the nondominant limb was measured by using pQCT (Densiscan1000, Scanco Medical, Zurich, Switzerland), with an effective X-ray energy of 40 keV. The nondominant leg was positioned in a radiolucent cast anatomically suitable for the subject during computed tomography scanning. After an anterior-posterior projectional scout view was displayed, a reference line was set at the right angle to the long axis of the lower limb and placed on the middle point of the end-plate of the distal tibia. A slice 66 mm proximal from the reference line was analyzed, according to the manufacturer's suggestion for cortical bone assessment. The thickness of one slice was 1 mm, and a voxel size was 0.355 x 0.355 mm. A standard phantom measurement was performed daily, which resulted in a long-term reproducibility of 0.3%, as vBMD was measured in adults of various age groups of both genders (35, 36).

Data analysis. The pQCT bone image was transmitted to a Macintosh computer in custom mode (resolution: 256 x 256 pixels) and imported into NIH Image [version 1.61, Wayne Rasband, National Institutes of Health (NIH)] to analyze vBMD, bone mineral content (BMC), and geometric properties. The cortical bone was defined as that with a volumetric density of >0.7 g/cm³ (44). Endocortical and periosteal areas were defined as cross-sectional areas surrounded by the inner and outer surface of the cortical bone, respectively. Cortical area was defined by the difference between periosteal and endocortical areas. Cortical thickness was defined as the mean distance between the inner and outer edge of the cortical shell. BMC was defined as the mineral content of the bone within a 1-mm slice (g/mm). Coefficients of variation for triplicate measurements of three human subjects after repositioning were 0.10–0.72% for vBMD, 0.44–0.74% for bone area, and 0.79% for cortical thickness. The polar moment of inertia and strength strain index (SSI) were calculated as the measure of the strength indexes of bone (39). Figure 1 shows an inverse image of the tibia on NIH image software.

View larger version (71K): [in this window] [in a new window]   Fig. 1. Calculation of polar moment of inertia and strength strain index (SSI). A Densiscan image of the tibia was imported into NIH Image to analyze the volumetric bone mineral density (vBMD), bone mineral content (BMC), geometric properties, and strength indexes of the bone. This example is an inverse image of a tibia on NIH Image software. Cortical bone was defined as that with a volumetric density of >0.7 g/cm3, and the strength indexes were calculated as follows (39): polar moment of inertia (mm4) = (d2 x A) and SSI (mm3) = (d2 x A x vBMDvox/vBMDmax)/dmax, where d is the distance (mm) of the voxel from the center of gravity (C), A is the cross-sectional area of a voxel (in this study it is 0.076 mm2), vBMDvox is the vBMD in the voxel (mg/mm3), vBMDmax is the maximum vBMD (mg/mm3), and dmax is the maximum distance of any of the voxels of the cortical cross section from the center of gravity (mm).

Statistical analysis. Values are presented as means ± SD. Group differences in descriptive data were evaluated by using ANOVA for men and women separately. Fisher's post hoc test analysis was performed for the significant values in ANOVA, and a correlation was also run between vBMD and bone geometric properties.

In addition to mechanical loading, measures of bone geometric and biomechanical indexes may also be influenced by interindividual variation in body size (both height and weight). To adjust potentially confounding differences related to height or weight in this present study, analysis of covariance (ANCOVA) was performed, and the adjusted values were presented, if necessary. Statistical significance was taken at the P < 0.05 level.

	RESULTS

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Physical characteristics of the subjects. The physical characteristics of the groups are given in Table 1. There was no significant difference in height among the male groups, whereas swimmers were significantly heavier than the other groups. The female athletes were significantly taller and heavier than the controls, although there were no significant differences between swimmers and jumpers. The starting age of training was earlier and the training duration was longer for the swimmers than the jumpers for both men and women. The age of menarche and the number of menstrual cycles during the past 12 mo were similar among the three female groups.

Bone measurement. There were no differences in vBMD of whole and cortical bone among the three male groups. In the women, the whole vBMD of the swimmers was 13.2 and 13.8% lower than that of controls and jumpers, and the cortical vBMD of swimmers and jumpers was 5.0 and 4.0% lower, respectively, than that of the controls. The cortical BMC of the male jumpers was 8.0 and 10.2% greater than that of the controls and swimmers, and that of female jumpers was 30.6 and 27.0% greater, respectively, than that of controls and swimmers. The periosteal areas of male jumpers, female swimmers, and female jumpers were 11.4, 20.3, and 33.5%, respectively, greater than that of controls. The endocortical area of female swimmers was 43.5% greater than that of controls. The cortical area of jumpers was greater than that of controls (10.2% in men and 34.8% in women) and swimmers (11.1% in men and 26.0% in women). The cortical thickness of jumpers was thicker than that of swimmers (9.6% in men and 25.0% in women), and the female jumpers' cortical thickness was also 18.2% thicker than that of the controls. The polar moment of inertia of male jumpers was 22.4% greater than that of controls, and that of female swimmers and female jumpers was 47.7 and 95.4% greater, respectively, than that of controls. Compared with swimmers, the polar moment of inertia of jumpers was 15.1% greater in men and 32.3% greater in women. SSI of female swimmers and jumpers were 51.5 and 82.1%, respectively, greater than that of controls. By ANCOVA, it was suggested that the body size (height and weight) influenced the cortical area in men and cortical thickness in both men and women significantly. However, statistical differences among group means remained unchanged after size-adjusted analysis (Table 2).

Correlation. Periosteal and endocortical areas were negatively correlated with cortical vBMD in both genders (Fig. 2).

View larger version (27K): [in this window] [in a new window]   Fig. 2. Correlation of periosteal and endocortical areas with cortical vBMD in male and female subjects. Periosteal (, men; , women) and endocortical (, men; , women) areas were negatively correlated with cortical vBMD. The regression formulas are y = 1,200.4 - 397.35x (r2 = 0.366, P = 0.0001) for male periosteal area; y = 1,471.4 - 586.73x (r2 = 0.526, P = 0.0001) for female periosteal area; y = 732.72 - 294.80x (r2 = 0.272, P = 0.001) for male endocortical area; and y = 939.72 - 417.80x (r2 = 0.647, P = 0.0001) for female endocortical area.

	DISCUSSION

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pQCT allows estimation of true BMD, i.e., vBMD in grams per cubic centimeter, and the geometric properties of the bone (12, 37, 38). Studies concerning the effect of physical training on bone using pQCT are scarce, with a few studies analyzing the side-to-side difference in tennis players' arms (1, 15, 28), a limited number on jumpers' legs (19), and a study on volleyball players' lower legs (34).

The present study evaluated vBMD, BMC, geometric properties, and the strength indexes of the tibia of male and female jumpers as a typical example of bone exposed to an extremely high-impact mechanical load. The periosteal area, cortical area, and polar moment of inertia were greater in male and female jumpers than in controls. The results showed the significant wider periosteal area (drift toward periosteal direction) and not a greater vBMD in jumpers' tibiae, confirming the conclusions of previous studies in young subjects (1, 15, 19) that improvement of the mechanical properties of bone in response to long-term physical exercise is related to geometric adaptation and not to vBMD. The results suggest that there is no margin for physical exercise to increase bone mineral, because the cortical bone of young sedentary subjects is already saturated with mineral, and, therefore, bone has expanded in a periosteal direction, resulting in periosteal drift. Contrary to the well-accepted notion from studies using DXA that exercise increases aBMD, the cortical vBMD of jumpers in the present study was lower than that of controls, and the difference was statistically significant in female jumpers. The present results and previous observations in tennis players that the cortical vBMD of the dominant arm was lower than that of the nondominant arm (1, 15) suggest that the cortical bone increased in size at the expense of bone density in young subjects. Previous reports using DXA suggest that athletes in impact-load sports (volleyball, basketball, handball, high jump, gymnastics, etc.) had greater aBMD (6, 11, 26, 43). However, the aBMD assessed by DXA represents area density expressed as grams per square centimeter, and it reflects vBMD and bone geometry (5, 12, 17, 25).

The present study also evaluated the tibia of male and female swimmers as a typical example of low-impact and active load. In male subjects, there was no significant difference in any parameter between swimmers and controls, whereas female swimmers had significantly greater periosteal area, endocortical area, polar moment of inertia and SSI, and lower whole vBMD and cortical vBMD compared with controls. When swimmers were compared with jumpers, endocortical area was greater, whereas periosteal area was smaller, in both men and women, although the differences were not statistically significant. These observations are consistent with a notion that impact loading (such as jumping) expands periosteal area, whereas active loading (such as swimming) expands endocortical area (10). Jumping and running forces produce ground reaction forces three to five times a person's body weight, and the force produced at the tissue level can be as high as 10 times the body weight (4, 31).

The greater polar moment of inertia and SSI with cortical drift observed only in female swimmers was unexpected and worth discussing. Parfitt (30) divided the life span into five phases, on the basis of chronological changes of cortical bone geometry (30). The endocortical area expands during puberty, from age 6 to 12 yr, and decreases from adolescence to middle age. Seeman (40) suggested that delayed puberty resulted in larger periosteal and endocortical area in girls but not in boys. As an average in the present study, female swimmers began their training (7.6 ± 1.9 yr) in the earlier part of puberty, but female jumpers began training (12.7 ± 1.5 yr) after puberty, and the athletes had slightly later menarche compared with the controls, although the difference was not statistically significant. Consequently, the different starting age of training between swimmers and jumpers probably caused the cortical drift seen only in female swimmers. The question of whether physical exercise before puberty accelerates the expansion of the endocortical area remains to be settled.

Although the present study is a cross-sectional study, the differences in bone geometry among groups were also observed in the previous studies (1, 15), which assessed side-to-side differences of tennis players' radius. To adjust potentially confounding differences related to height or weight in the present study, ANCOVA was performed, and the adjusted values were presented, if necessary. However, the statistical differences among group means remained unchanged, even after being size adjusted. The differences in bone geometry and strength indexes in the present study were, therefore, more likely associated with the different types of physical exercise than with the selection bias on the basis of bone size.

Cross-sectional area (cortical area) and polar moment of inertia of cortical bone in jumpers were greater than those in swimmers and controls, suggesting stronger bone against compressive and bending strains. On the other hand, the index for torsional strain assessed by SSI was significantly greater in female athletes (swimmers and jumpers) but not in male athletes. SSI is a function of vBMD and geometry of a bone, and greater vBMD and cortical drift toward periosteal direction result in greater SSI. Interestingly, in the present study, periosteal and endocortical areas were negatively correlated with cortical vBMD in both male and female subjects. Consistently, previous studies observed a negative correlation between relative side-to-side difference in perosteal area and cortical vBMD of midradius in tennis players (1). Exercise seems to increase the cross-sectional area of bone at the expense of BMD. A preferential increase in cross-sectional area to cortical density has also been reported during the adolescent growth spurt (22). Thus, given a limited calcium intake (22), an increase in cortical drift due to exercise and growth is partly offset by an increase in cortical porosity. Furthermore, it remains to be clarified how bone metabolism between the inner and outer edge of the cortical shell is integrated to effect the changes in cortical vBMD.

In conclusion, 1) an improvement of the mechanical properties of a young athlete's bone in response to long-term physical exercise is related to geometric adaptation and not to vBMD; 2) increases in periosteal and endocortical area are inversely related to reduced cortical vBMD in athletes; and 3) in female swimmers, physical training started in the earlier part of puberty may contribute to enlarged endocortical area. Thus exercise affects bone geometry through loading mechanical impact on the bone, but it may also affect the endocrine system by delaying puberty.

	FOOTNOTES

 

Address for reprint requests and other correspondence: K. Tokuyama, Institute of Health and Sport Sciences, Univ. of Tsukuba, Tennodai 1-1-1, Tsukuba, Ibaraki, 305-8574 Japan (E-mail: tokuyama{at}taiiku.tsukuba.ac.jp).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

	REFERENCES

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

1. Ashizawa N, Nonaka K, Michikami S, Mizuki T, Amagai H, Tokuyama K, and Suzuki M. Tomographical description of tennis-loaded radius: reciprocal relation between bone size and volumetric BMD. J Appl Physiol 86: 1347-1351, 1999.[Abstract/Free Full Text]
2. Augat P, Fuerst T, and Genant HK. Quantitative bone mineral assessment at the forearm: a review. Osteoporos Int 8: 299-310, 1998.[ISI][Medline]
3. Bradney M, Pearce G, Naughton G, Sullivan C, Bass S, Beck T, Carlson J, and Seeman E. Moderate exercise during growth in prepubertal boys: changes in bone mass, size, volumetric density, and bone strength: a controlled prospective study. J Bone Miner Res 13: 1814-1821, 1998.[ISI][Medline]
4. Burdett RG. Forces predicted at the ankle during running (Abstract). Med Sci Sports Exerc 14: 308, 1982.[ISI][Medline]
5. Carter DR, Bouxsein ML, and Marcus R. New approaches for interpreting projected bone densitometry data. J Bone Miner Res 7: 137-145, 1992.[ISI][Medline]
6. Creighton DL, Morgan AL, Boardley D, and Brolinson PG. Weight-bearing exercise and markers of bone turnover in female athletes. J Appl Physiol 90: 565-570, 2001.[Abstract/Free Full Text]
7. Cummings SR, Black DM, Nevitt MC, Browner W, Cauley J, Ensrud K, Genant HK, Palermo L, Scott J, and Vogt TM. Bone density at various sites for prediction of hip fractures. The Study of Osteoporotic Fractures Research Group. Lancet 341: 72-75, 1993.[ISI][Medline]
8. Dalen N and Olsson KE. Bone mineral content and physical activity. Acta Orthop Scand 45: 170-174, 1974.[ISI][Medline]
9. Dambacher MA, Neff M, Kissling R, and Qin L. Highly precise peripheral quantitative computed tomography for the evaluation of bone density, loss of bone density and structures. Consequences for prophylaxis and treatment. Drugs Aging 12, Suppl 1: 15-24, 1998.
10. Duncan CS, Blimkie CJR, Kemp A, Higgs W, Cowell CT, Woodhead H, Briody JN, and Howman-Giles R. Mid-femur geometry and biomechanical properties in 15- to 18-yr-old female athletes. Med Sci Sports Exerc 34: 673-681, 2002.[ISI][Medline]
11. Fehling PC, Alekel L, Clasey J, Rector A, and Stillman RJ. A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone 17: 205-210, 1995.[Medline]
12. Formica CA, Nieves JW, Cosman F, Garrett P, and Lindsay R. Comparative assessment of bone mineral measurements using dual X-ray absorptiometry and peripheral quantitative computed tomography. Osteoporos Int 8: 460-467, 1998.[ISI][Medline]
13. Guglielmi G, De Serio A, Fusilli S, Scillitani A, Torlontano M, and Cammisa M. Age-related changes assessed by peripheral QCT in healthy Italian women. Eur Radiol 10: 609-614, 2000.[ISI][Medline]
14. Haapasalo H, Kannus P, Sievänen H, Pasanen M, Uusi-Rasi K, Heinonen A, Oja P, and Vuori I. Effect of long-term unilateral activity on bone mineral density of female junior tennis players. J Bone Miner Res 13: 310-319, 1998.[ISI][Medline]
15. Haapasalo H, Kontulainen S, Sievänen H, Kannus P, Jarvinen M, and Vuori I. Exercise-induced bone gain is due to enlargement in bone size without a change in volumetric bone density: a peripheral quantitative computed tomography study of the upper arms of male tennis player. Bone 27: 351-357, 2000.[Medline]
16. Haapasalo H, Sievänen H, Kannus P, Heinonen A, Oja P, and Vuori I. Long-term unilateral loading and bone mineral density and content in female squash players. Calcif Tissue Int 54: 249-255, 1994.[ISI][Medline]
17. Haapasalo H, Sievänen H, Kannus P, Heinonen A, Oja P, and Vuori I. Dimensions and estimated mechanical characteristics of the humerus after long-term tennis loading. J Bone Miner Res 11: 864-872, 1996.[ISI][Medline]
18. Hasegawa Y, Schneider P, Reiners C, Kushida K, Yamazaki K, Hasegawa K, and Nagano A. Estimation of the architectural properties of cortical bone using peripheral quantitative computed tomography. Osteoporos Int 11: 36-42, 2000.[ISI][Medline]
19. Heinonen A, Sievänen H, Kyröläinen H, Perttunen J, and Kannus P. Mineral mass, size, and estimated mechanical strength of triple jumpers' lower limb. Bone 29: 279-285, 2001.[Medline]
20. Ito M, Tsurusaki K, and Hayashi K. Peripheral QCT for the diagnosis of osteoporosis. Osteoporos Int 7: S120-S127, 1997.
21. Karlsson MK, Johnell O, and Obrant KJ. Bone mineral density in weight lifters. Calcif Tissue Int 52: 212-215, 1993.[ISI][Medline]
22. Kleerekoper M, Tolia K, and Parfitt AM. Nutritional, endocrine, and demographic aspects of osteoporosis. Orthop Clin North Am 12: 547-558, 1981.[ISI][Medline]
23. Lee EJ, Long KA, Risser WL, Poindexter HB, Gibbons WE, and Goldzieher J. Variations in bone status of contralateral and regional sites in young athletic women. Med Sci Sports Exerc 27: 1354-1361, 1995.[ISI][Medline]
24. Lehmann R, Wapniarz M, Kvasnicka HM, Baedeker S, Klein K, and Allolio B. Reproducibility of measurements of bone mineral density of the distal radius with a special-purpose computed tomography scanner. Radiology 32: 177-181, 1992.
25. Lu PW, Cowell CT, Lloyd-Jones SA, Briody JN, and Howman-Giles R. Volumetric bone mineral density in normal subjects, aged 5–27 years. J Clin Endocrinol Metab 81: 1586-1590, 1996.[Abstract]
26. Matsumoto T, Nakagawa Nishida S, and Hirota R. Bone density and bone metabolic markers in active collegiate athletes: findings in long-distance runners, judoists, and swimmers. Int J Sports Med 18: 408-412, 1997.[ISI][Medline]
27. Metton LJ, Atkinson EJ, O'Fallon WM, Wahner HW, and Riggs BL. Long-term fracture prediction by bone mineral assessed at different skeletal sites. J Bone Miner Res 8: 1227-1233, 1993.[ISI][Medline]
28. Nara-Ashizawa N, Liu LJ, Higuchi T, Tokuyama K, Hayashi K, Shirasaki Y, Amagai H, and Saitoh S. Paradoxical adaptation of mature radius to unilateral use in tennis playing. Bone 30: 619-623, 2002.[Medline]
29. Nilsson BE and Westlin NE. Bone density in athletes. Clin Orthop 77: 179-182, 1971.[Medline]
30. Parfitt AM. The two faces of growth: benefits and risks to bone integrity. Osteoporos Int 4: 382-398, 1994.[ISI][Medline]
31. Payne AH. A comparison of the ground forces in race walking with those in normal walking and running. In: Biomechanics VI: Proceedings of the Sixth International Congress of Biomechanics, Copenhagen, Denmark, edited by Asmussen E and Jorgensen K. Baltimore, MD: University Park Press, 1978, p. 293.
32. Qin L, Au S, Chan KM, Lau MC, Woo J, Dambacher MA, and Leung PC. Peripheral volumetric bone mineral density in pre- and postmenopausal Chinese women in Hong Kong. Calcif Tissue Int 67: 29-36, 2000.[ISI][Medline]
33. Radspieler H, Dambacher MA, Kissling R, and Neff M. Is the amount of trabecular bone-loss dependent on bone mineral density? A study performed by three centres of osteoporosis using high resolution peripheral quantitative computed tomography. Eur J Med Res 5: 32-39, 2000.[Medline]
34. Rittweger J, Beller G, Ehrig J, Jung C, Koch U, Ramolla J, Schmidt F, Newitt D, Majumdar S, Schiessl H, and Felsenberg D. Bone-muscle strength indices for the human lower leg. Bone 27: 319-326, 2000.[Medline]
35. Rüegsegger P. The use of peripheral QCT in the evaluation of bone remodeling. Endocrinologist 4: 167-176, 1994.
36. Rüegsegger P. Bone density measurement. In: Osteoporosis: A Guide to Diagnosis and Treatment, edited by Bröll H and Dambacher MA. Basel: Karger, 1996, vol. 18, p. 103-116.
37. Rüegsegger P, Elsasser U, Anliker M, Gnehm H, Kind HP, and Prader A. Quantification of bone mineral mineralization using computed tomography. Radiology 121: 93-97, 1976.[Abstract]
38. Schneider P and Börner W. Peripheral quantitative computed tomography for bone mineral measurement using a new special QCT-scanner. Methodology, normal values, comparison will manifest osteoporosis. Rofo Fortschr Geb Rontgenstr Neuen Bildgeb Verfahr 154: 292-299, 1991.[Medline]
39. Schoenau E, Neu CM, Rauch F, and Manz F. The development of bone strength at the proximal radius during childhood and adolescence. J Clin Endocrinol Metab 86: 613-618, 2001.[Abstract/Free Full Text]
40. Seeman E. Sexual dimorphism in skeletal size, density, and strength. J Clin Endocrinol Metab 86: 4576-4584, 2001.[Free Full Text]
41. Sievänen H, Koskue V, Rauhio A, Kannus P, Heinonen A, and Vuori I. Peripheral quantitative computed tomography in human long bones: evaluation of in vitro and in vivo precision. J Bone Miner Res 13: 871-882, 1998.[ISI][Medline]
42. Slemenda CW, Reister TK, Hui SL, Miller JZ, Christian JC, and Johnston CC. Influences on skeletal mineralization in children and adolescents: evidence for varying effects of sexual maturation and physical activity. J Pediatr 125: 201-207, 1994.[ISI][Medline]
43. Taaffe DR, Snow CM, Connolly DA, Robinson TL, Brown MD, and Marcus R. Differential effects of swimming versus weight-bearing activity on bone mineral status of eumenorrheic athletes. J Bone Miner Res 10: 586-593, 1995.[ISI][Medline]
44. Takagi Y, Fujii Y, Miyauchi A, Goto B, Takahashi K, and Fujita T. Transmenopausal change of trabecular bone density and structural pattern assessed by peripheral quantitative computed tomography in Japanese women. J Bone Miner Res 10: 1830-1834, 1995.[ISI][Medline]

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