- Email: [email protected]
Cortical and Trabecular Bone at the Forearm Show Different Adaptation Patterns in Response to Tennis Playing
Journal of Clinical Densitometry, vol. 7, no. 4, 399–405, 2004 © Copyright 2004 by Humana Press Inc. All rights of any nature whatsoever reserved. 1094-6950/04/7:399–405/$25.00
Original Article
Cortical and Trabecular Bone at the Forearm Show Different Adaptation Patterns in Response to Tennis Playing Gaële Ducher, Stéphanie Prouteau, Daniel Courteix, and Claude-Laurent Benhamou Laboratoire Architecture du lisse Osseux et Exercise Physique, UFR STAPS, Université d’Orléans et Inserm ERIT-M0101, CHR Orléans, Orléans, France
Abstract Bone responds to impact-loading activity by increasing its size and/or density. The aim of this study was to compare the magnitude and modality of the bone response between cortical and trabecular bone in the forearms of tennis players. Bone area, bone mineral content (BMC), and bone mineral density (BMD) of the ulna and radius were measured by dual-energy X-ray absorptiometry (DXA) in 57 players (24.5 ± 5.7 yr old), at three sites: the ultradistal region (50% trabecular bone), the mid-distal regions, and third-distal (mainly cortical bone). At the ultradistal radius, the side-to-side difference in BMD was larger than in bone area (8.4 ± 5.2% and 4.9 ± 4.0%, respectively, p < 0.01). In the cortical sites, the asymmetry was lower (p < 0.01) in BMD than in bone area (mid-distal radius: 4.0 ± 4.3% vs 11.7 ± 6.8%; third-distal radius: 5.0 ± 4.8% vs 8.4 ± 6.2%). The asymmetry in bone area explained 33% of the variance of the asymmetry in BMC at the ultradistal radius, 66% at the mid-distal radius, and 53% at the third-distal radius. The ulna displayed similar results. Cortical and trabecular bone seem to respond differently to mechanical loading. The first one mainly increases its size, whereas the second one preferentially increases its density. Key Words: Bone geometry; trabecular and cortical adaptations; tennis players; bone mineral density.
Introduction
than compact bone, therapeutic effects can be detected earlier in these regions (14). This does not imply, however, that trabecular bone is more sensitive than cortical bone to long-term mechanical loading. Heinonen et al. (15) found that the cortical cross-sectional area at the distal and diaphyseal radii were larger in weight lifters than in nonactive students. Additionally, studies in racket sports revealed that the cortical sites of the diaphyseal humerus display a marked side-to-side difference (also referred to as “asymmetry”) in BMC and cortical wall thickness (16,17). The study of former tennis players led by Etherington et al. (18) reports a significant side-to-side difference in radial BMD at cortical sites (mid and third radius) but not at trabecular sites (ultradistal radius), showing the ability of cortical bone to respond to long-term tennis playing. Although the site-specific effects of mechanical stress have been described on the dominant limb of tennis players (19,20), the authors did not focus on specific trabecular and cortical
Physical activities involving impact and loading forces are known to exert positive effects on bone (1–6). It has been convincingly shown that the bone response to mechanical loading is site-specific, depending on the rate, magnitude, and orientation of the mechanical strains (7,8). Conversely, the skeletal sites that are not loaded during the physical practice tend to show a “deficit” in bone mass (9,10), notably the skull (11). Cross-sectional studies evidenced a higher bone mineral content (BMC) and bone mineral density (BMD) in adult athletes than in sedentary subjects, especially at trabecular bone sites (12,13). Cancellous bone being metabolically more active Received 04/30/04; Revised 07/02/04; Accepted 07/02/04. * Address correspondence to Gaële Ducher, IPROS-C.H.R. Orléans Hoˆpital Porte Madeleine-1 rue Porte Madeleine, BP 2439, 45032 Orléans cedex 1, France. E-mail: [email protected]
399
400 bone adaptations. Depending on the intensity and direction of the forces applied to the bone, a prolonged mechanical stress might affect several aspects of bone modeling and remodeling (21). This approach requires one to differentiate between trabecular and cortical bone sites in order to compare their peculiar responses to long-term physical training. In addition to the respective percentage of trabecular bone, several other factors might explain why distinct skeletal sites respond differently to tennis-induced mechanical strains. Among the factors influencing the bone responsiveness are the distance of the bone site from the point of application of the mechanical forces, the muscular and tendinous insertions, and the vibrations induced by the impacts of the ball on the racket. The ulna and the radius are likely to be loaded differently during tennis playing. Indeed, the muscle attachments differ between these two bones. One could hypothesize that because the ulna does not touch the carpus, it might be less exposed to vibrations than the radius. Our objective was to study the effects of tennis-induced mechanical strains at the dominant distal radius and ulna and to compare them to the nonplaying arm. We have studied the distal epiphysis of the ulna and radius in each arm. Three regions of interest were determined according to their respective trabecular bone content (22): the ultradistal region (approx 50%), the mid-distal region (approx 1%), and thirddistal region (less than 10%).
Materials and Methods Subjects Fifty-seven regional-level tennis players (33 men and 24 women) were recruited in the neighborhood of Orléans (France). All had been practicing tennis for at least 5 yr. As far as the handedness is concerned, there were 52 right-handed players and only 5 left-handed players. Thirty of the players reported using both hands for backhand stroke, the others using their dominant hand only. Exclusion criteria were any past fracture at the radius or ulna as well as any medical disorder or treatment known to affect bone metabolism (exception made for oral contraceptives in 18 out of 24 women). None of the female subjects reported having experienced amenorrhea during their teenage years or twenties. Each participant gave his informed written consent. The study was approved by the Ethics Committee of the Region of Tours.
Anthropometric Measurements Body weight (in kg) was measured on a balance-beam scale (SECA 709, Germany), the subjects wearing only underwear. Body height (in cm) was measured in the upright position to the nearest 1 mm.
Bone Mineral and Body Composition Measurements Bone area (in cm2), bone mineral content (BMC, in g) and bone mineral density (BMD, in g/cm2) were determined by dual-energy X-ray absorptiometry (DXA, Delphi QDR® Journal of Clinical Densitometry
Ducher et al.
Fig. 1. Regions of interest at the distal radius and ulna, used to measure the bone area, BMC, and BMD in tennis players: UD (ultradistal), MID (mid-distal), and 1/3 (third-distal). The regions of interest were defined by the software supplied by the manufacturer (Delphi QDR® Series; Hologic Inc., Waltham, MA, USA).
Series; Hologic Inc., Waltham, MA, USA). Bone area, BMC, and BMD were measured at the whole body and at both forearms. According to their respective trabecular bone content, three sites were defined along the mid-distal to distal region of the radius. The first region, termed “ultradistal radius,” consisted of a 1.5-cm band adjacent to the end plate of the radius; the second region, named “one-third radius,” consisted of a 2-cm band one-third of the distance between the ulnar styloid and the olecranon; and the last region, labeled “middistal,” comprised the residual distance between the two sites mentioned (Fig. 1). Once these sites were defined at the radius, we expanded these regions of interest toward the ulna by prolonging their horizontal boundaries (Fig. 1). We proceeded to separate measurements of bone parameters at the radius and at the ulna because the results could differ between these two bones (23). The intraobserver reproducibility of BMD was calculated by two repeated measurements in seven different forearms by the root mean square (RMS) coefficient of variation (24). The RMS coefficient of variation was 1.1%, 0.6%, and 6.7% for the ultradistal, mid-distal, and third-distal regions, respectively. Volume 7, 2004
Bone Adaptation Patterns in Tennis Players
401
Table 1 Characteristics of the Tennis Players
Age (yr) Height (cm) Weight (kg) Fat mass (%) Whole-body BMD (g/cm2) Starting age of playing (yr) Years of playing Total training time (hr)
Women (n = 24)
Men (n = 33)
Total (n = 57)
21.5 ± 1.8 165.9 ± 4.9 58.9 ± 5.2 23.1 ± 3.7 1.207 ± 0.062 8.3 ± 2.3 13.3 ± 2.6 2945.7 ± 2199.9
26.6 ± 6.6*** 178.5 ± 5.5*** 74.6 ± 8.1*** 14.2 ± 4.2*** 1.306 ± 0.056*** 7.9 ± 2.8 18.3 ± 6.9*** 4069.8 ± 3536.9
24.5 ± 5.7 173.2 ± 8.2 68.0 ± 10.5 18.0 ± 5.9 1.265 ± 0.076 8.1 ± 2.6 16.1 ± 6.0 3579.3 ± 3054.1
Note: Values are means ± SD. Difference between males and females: ***p < 0.001.
Training History The training history was assessed by questionnaire. The participants recorded their starting age of regular tennis playing (at least 1 h per week), number of years of practice, and training volume (hours per week) for each year. Adding up the whole training volume for each subject yielded the total amount of practice for the entire career (total training time), after taking into account the breaks because of injuries or holidays.
Statistical Analysis All of the data are shown as mean ± standard deviation. The Gaussian distribution of the parameters was tested by the Kolmogorov–Smirnov test. The comparison of the parameters measured at the dominant and nondominant forearms was performed using a parametric paired t-test. The side-to-side differences in bone area, BMC, and BMD were expressed as the percentage of the nondominant value (∆% = [(dominant – nondominant)/nondominant] × 100). The three regions of interest were compared by analysis of variance (ANOVA) with repeated measurements. The Newman–Keuls test was used as a post hoc test. The relationship between the significant variables was tested by the Pearson product moment correlation coefficient. Linear regression between bone area asymmetry and BMC asymmetry was plotted. The correlation coefficient r was evaluated and the parameter r2 gave the percentage of the variation of BMC asymmetry that can be explained by the linear regression.
Results Baseline Characteristics of the Subjects The characteristics of the subjects are given in Table 1. The male subjects were significantly older, taller, and heavier than their female counterparts. They also reported a longer tennis practice. They showed a lower percentage of fat mass and a higher whole-body BMD (p < 0.001). All of the subjects were within the norms for fat mass and whole-body BMD, according to the reference databases (including NHANES dataset) supplied by the manufacturer of the densitometer. Journal of Clinical Densitometry
Asymmetry Between the Dominant and Nondominant Forearm The BMC values of the ultradistal, mid-distal, and thirddistal sites are given for both radii and ulnas in Table 2, with the side-to-side difference indicated for each site. For each region of the radius and ulna, the asymmetries in bone area and BMD are shown in Table 3. Bone area, BMC, and BMD were significantly higher at the dominant forearm (p < 0.0001). The players using only the dominant hand for backhand stroke displayed a greater side-to-side difference than those using both hands at the following sites: the ultradistal radius for BMD, the ultradistal ulna for BMC and BMD, and the third-distal radius for BMC (p < 0.05). The largest difference between these two groups was seen at the ultradistal ulna (p < 0.01), with a sideto-side difference reaching up to 19.8% for BMC and 10.9% for BMD in the one-handed backhand players vs 10.0% for BMC and 5.1% for BMD in the two-handed backhand players. After adjustment for the number of playing years and total training time, the difference between the two groups remained significant only at the third-distal ulna. A greater asymmetry was found in men than in women at the ultradistal radius for BMC and BMD and at the third-distal radius for bone area and BMC (p < 0.05). The differences disappeared after adjustment for number of playing years. We investigated whether there was any correlation between the bone asymmetries and the training history. The side-to-side difference in BMD in every site of the radius was associated with the number of years of practice (with an r value ranging from 0.27 to 0.43 according to the site studied) as well as with the total training time (r = 0.29–0.40, p < 0.05). The starting age of tennis playing correlated with the side-to-side difference in BMD of the ultradistal radius (r = –0.29, p < 0.05), as well as of the mid-distal and third-distal ulna (r = –0.38 and –0.33, respectively, p < 0.05).
Side-to-Side Difference in BMC In order to check which of the examined sites had been the most responsive to long-term tennis playing, we compared the Volume 7, 2004
402
Ducher et al. Table 2 BMC at the Dominant and Nondominant Radius and Ulna of the Tennis Players
BMC radius (g) UD MID 1/3 Total BMC ulna (g) UD MID 1/3 Total
Dominant
Nondominant
Side-to-side difference (%)
2.06 ± 0.36 5.19 ± 1.30 2.31 ± 0.42 9.56 ± 2.03
1.81 ± 0.30 4.47 ± 1.06 2.03 ± 0.33 8.31 ± 1.64
13.71 ± 6.77a 16.17 ± 8.30a 13.83 ± 7.40a 14.98 ± 7.03a
UD < MID** 1/3 < MID**
1.00 ± 0.17 3.49 ± 0.80 1.95 ± 0.31 6.42 ± 1.23
0.88 ± 0.14 2.98 ± 0.69 1.81 ± 0.30 5.67 ± 1.09
14.65 ± 12.16a 17.61 ± 10.59a 7.79 ± 6.93a 13.44 ± 7.36a
1/3 < UD** 1/3 < MID**
Note: Three distal regions of interest were analyzed, from the most distal to the most proximal: ultradistal region (UD), mid-distal region (MID), and third-distal region (1/3). The relative side-to-side differences are expressed in percentage of the nondominant value. Values are means ± SD. a Dominant > nondominant, p < 0.0001. ** p < 0.01.
bone asymmetry of each region of interest separately. The mid-distal region showed a greater side-to-side difference in BMC than the ultradistal or third-distal regions at the radius (p < 0.01). Similar results were observed at the ulna, although the difference between the mid-distal and ultradistal sites was not significant (Table 2). ANOVA with repeated measurements revealed that, among all sites, the third-distal ulna had the lowest asymmetry in BMC (p < 0.01).
Side-to-Side Difference in Bone Area and BMD At the radius, the side-to-side difference in bone area was significantly greater at the mid-distal and third-distal regions than at the ultradistal region (p < 0.01, Table 3). Conversely, the BMD asymmetry was more pronounced at the ultradistal radius than at the mid-distal and third-distal sites (p < 0.01). At the ulna, the bone area asymmetry was the highest at the mid-distal site and the lowest at the third-distal site. The only site revealing a difference between the radius and ulna was the third-distal region, with a lower value in bone area asymmetry at the ulna (p < 0.01). The asymmetry was more marked in BMD than in bone area at the ultradistal radius (p < 0.01) and ulna (not significant). The opposite was found at the cortical sites, with a greater side-to-side difference in bone area than in BMD (p < 0.01, except the third-distal ulna: not significant). At the radius, the side-to-side difference in bone area explained 33% of the variance of the BMC asymmetry at the ultradistal site, 66% at the mid-distal site, and 53% at the thirddistal site. At the ulna, r2 values were 47%, 45%, and 59%, respectively.
Discussion This study showed that the bone response to mechanical loading is site-specific. The modality of the bone response difJournal of Clinical Densitometry
fers according to whether the site contains mainly trabecular (ultradistal regions) or cortical bone (mid-distal and third-distal regions). Asymmetry in bone area is considered to reflect asymmetry in bone size. The asymmetry of the cortical regions was more pronounced in bone area than in BMD. Interestingly, the opposite is observed in trabecular sites. Our results suggest that trabecular bone reacts to mechanical strains mainly by increasing its density, whereas cortical bone mainly reacts by increasing its size. These results corroborate with those of other studies using peripheral quantitative computed tomography (pQCT) (19,20). In 16 tennis players, Ashizawa et al. (19) observed that the increase in periosteal area was more important at the mid-distal radius (cortical site) than at the ultradistal radius (trabecular site). In 36 female tennis and squash players, Kontulainen et al. (20) reported a 5% difference in trabecular BMD at the distal radius (trabecular site) in favor of the dominant side, whereas no difference was found in cortical wall thickness. Our results yielded a 8.4% asymmetry in BMD at the ultradistal radius, whereas in the two aforementioned studies, the asymmetry in trabecular BMD at the distal radius was less than 6%. The asymmetry in bone area underestimates the true asymmetry in bone size because DXA is a surfacic method (25,26). As a consequence, the asymmetry in bone density may have been overestimated in the present study. The percentage of trabecular bone reaches up to 85–90% at the ultradistal radius, with a mean slice thickness of 0.2 cm (22). In the present study, the mean trabecular percentage at the ultradistal site might, in fact, be closer to 50% because this site is 1.5 cm in size. It drops to 10% at the mid-distal radius and to 1% at the third-distal radius. Similar values were observed at the ulna (22). The ultradistal site was, hence, considered as being “trabecular,” whereas the mid-distal and thirddistal sites were labeled as “cortical sites.” Volume 7, 2004
Bone Adaptation Patterns in Tennis Players
403
Table 3 Side-to-Side Differences in Bone Area and BMD at the Radius and Ulna Differences between the sites
UD
MID
1/3
Bone area (cm2) ∆ at the radius (%)
4.93 ± 4.03
11.66 ± 6.78
8.43 ± 6.18
UD < MID** UD < 1/3** 1/3 < MID**
∆ at the ulna (%)
6.25 ± 6.74
10.28 ± 6.26
4.16 ± 5.93
UD < MID** 1/3 < MID**
BMD (g/cm2) ∆ at the radius (%)
8.38 ± 5.21
4.04 ± 4.26
5.05 ± 4.80
MID < UD** 1/3 < UD**
∆ at the ulna (%)
7.84 ± 8.14
5.90 ± 4.95
3.47 ± 4.29
1/3 < UD** MID < UD* 1/3 < MID*
Note: The relative side-to-side differences (∆) are expressed in percentage of the nondominant value, and compared between three distal regions of interest: ultra distal region (UD), mid-distal region (MID), and third-distal region (1/3). Values are means ± SD. All of the side-to-side differences are significant (p < 0.0001). * p < 0.05. ** p < 0.01.
It has been suggested that the trabecular and cortical bone tissues do not show the same sensitivity to mechanical loading, possibly the result of the different metabolic activities of these two bone components (27). Because trabecular bone is known to have a rapid turnover, there might be a time gap between trabecular and cortical bone responses. In a short-term longitudinal study on rats, the trabecular sites showed an increase in BMC after a few weeks of training, whereas the effects were not significant at cortical sites (28). In the present study, the side-to-side difference in BMC was the same in cortical and trabecular sites. Except for the thirddistal ulna, where the asymmetry was much lower, all of the regions showed a BMC asymmetry reaching at least 10% and even 15% for the mid-distal sites. These results confirm that cortical bone is highly responsive to long-term mechanical stress (17,29–32). The complexity of mechanical loading forces during tennis playing might explain why the asymmetry was so pronounced at both cortical and trabecular bone sites. It has been shown that the mechanical stress was more efficient when the strain distribution is different from the normal strains to which the bone had adapted (7,8). In prepubertal girls, Heinonen et al. (33) showed that there is a regional, site-specific interplay between muscles and bone in the lower limb. Hitting the tennis ball involved several muscles, including the pronator teres and the brachioradialis (34), which display large insertions on the distal radius. The pronator teres shows only a marginal insertion on the distal ulna. This could explain why the third-distal ulna showed a weaker asymmetry than the other sites. Journal of Clinical Densitometry
During tennis strokes, the forearm must counteract the backward movement of the racket at the impact. From a mechanical point of view, a bending force applied on a hollow cylindrical bone imposes a high stress on the external cortical shell (35). The further the point from the force application, the higher the stress (18). High bending forces during weight-lifting tend to enlarge bones (15). Likewise, a marked increase in bone area at the mid-distal and third-distal regions was observed in the present study. The repeated impacts of the ball on the strings lead to racket vibrations, which are transmitted to forearm bones. Hennig et al. (36) fastened strain-gage-type sensors on the skin and found wrist and elbow vibratory accelerations of 6.81 and 1.53 g, respectively (g = 9.81 m/s2) for center ball impacts. This result suggests that vibrations are damped along the bone as the distance to the point of impact increases. Sedentary subjects display side-to-side differences in bone area, BMC (37), BMD (38), and also trabecular bone structure (39). Therefore, all of the asymmetries described in the present study cannot be completely attributed to tennis playing. However, the asymmetry is much weaker in control subjects (less than 5% on average) than in tennis players (16,17,40). In conclusion, these data suggest that the cortical and trabecular bone tissues respond differently to mechanical loading, the first one mainly increasing its size and the second one preferentially increasing its density. This assumption might not necessarily be valid for mature bones, which show a reduced ability to increase their size in response to mechanical loading (20,41). The ability of cortical bone to grow periosteally in response to mechanical loading improves the Volume 7, 2004
404 ability of bone to resist bending and torsional forces. The increase in bone density at trabecular sites enhances the ability of bone to withstand compressive forces (35). Thus, the specificity of the bone response at cortical and trabecular sites is of critical importance when considering the effects of physical activity on the mechanical competence of bones.
Acknowledgments This research was supported by a grant from the Région Centre and the Inserm (Institut National de la Santé Et de la Recherche Médicale). The authors confirm that all of the experiments comply with the current French laws.
References 1. Cassell C, Benedict M, Specker B. 1996 Bone mineral density in elite 7- to 9-yr-old female gymnasts and swimmers. Med Sci Sports Exerc 28:1243–1246. 2. Dyson K, Blimkie CJ, Davison KS, Webber CE, Adachi JD. 1997 Gymnastic training and bone density in pre-adolescent females. Med Sci Sports Exerc 29:443–450. 3. Courteix D, Lespessailles E, Peres SL, Obert P, Germain P, Benhamou CL. 1998 Effect of physical training on bone mineral density in prepubertal girls: a comparative study between impactloading and non-impact-loading sports. Osteoporos Int 8:152–158. 4. Lima F, De Falco V, Baima J, Carazzato JG, Pereira RMR. 2001 Effect of impact load and active load on bone metabolism and body composition of adolescent athletes. Med Sci Sports Exerc 33:1318–1323. 5. Duncan CS, Blimkie CJ, Cowell CT, Burke ST, Briody JN, Howman-Giles R. 2002 Bone mineral density in adolescent female athletes: relationship to exercise type and muscle strength. Med Sci Sports Exerc 34:286–294. 6. Duncan CS, Blimkie CJ, Kemp A, et al. 2002 Mid-femur geometry and biomechanical properties in 15- to 18-yr-old female athletes. Med Sci Sports Exerc 34:673–681. 7. Burr DB, Robling AG, Turner CH. 2002 Effects of biomechanical stress on bones in animals. Bone 30:781–786. 8. Ehrlich PJ, Lanyon LE. 2002 Mechanical strain and bone cell function: a review. Osteoporos Int 13:688–700. 9. Karlsson MK, Hasserius R, Obrant KJ. 1996 Bone mineral density in athletes during and after career: a comparison between loaded and unloaded skeletal regions. Calcif Tissue Int 59:245–248. 10. Magnusson H, Linden C, Karlsson C, Obrant KJ, Karlsson MK. 2001 Exercise may induce reversible low bone mass in unloaded and high bone mass in weight-loaded skeletal regions. Osteoporos Int 12:950–955. 11. Courteix D, Lespessailles E, Obert P, Benhamou CL. 1999 Skull bone mass deficit in prepubertal highly-trained gymnast girls. Int J Sports Med 20:328–333. 12. Suominen H. 1993 Bone mineral density and long term exercise. An overview of cross-sectional athlete studies. Sports Med 16:316–330. 13. Forwood MR, Burr DB. 1993 Physical activity and bone mass: exercises in futility? Bone Miner 21:89–112. 14. Augat P, Fuerst T, Genant H. 1998 Quantitative bone mineral assessment at the forearm: a review. Osteoporos Int 8:299–310. 15. Heinonen A, Sievanen H, Kannus P, Oja P, Vuori I. 2002 Sitespecific skeletal response to long-term weight-training seems to
Journal of Clinical Densitometry
Ducher et al.
16. 17.
18.
19. 20.
21.
22.
23. 24.
25. 26. 27.
28.
29. 30. 31.
32.
33.
be attributable to principal loading modality: a pQCT study of female weightlifters. Calcif Tissue Int 70:469–474. Kannus P, Haapasalo H, Sievänen H, Oja P, Vuori I. 1994 The site-specific effects of long-term unilateral activity on bone mineral density and content. Bone 15:279–284. Haapasalo H, Sievänen H, Kannus P, Heinonen A, Oja P, Vuori I. 1996 Dimensions and estimated mechanical characteristics of the humerus after long-term tennis loading. J Bone Miner Res 11:864–872. Etherington J, Harris PA, Nandra D, et al. 1996 The effect of weight-bearing exercise on bone mineral density: a study of female ex-elite athletes and the general population. J Bone Miner Res 11:1333–1338. Ashizawa N, Nonaka K, Michikami S, et al. 1999 Tomographical description of tennis-loaded radius: reciprocal relation between bone size and volumetric BMD. J Appl Physiol 86:1347–1351. Kontulainen S, Sievänen H, Kannus P, Pasanen M, Vuori I. 2002 Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquet-sports players: a peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res 17:2281–2289. Adami S, Gatti D, Braga V, Bianchini D, Rossini M. 1999 Sitespecific effects of strength training on bone structure and geometry of ultradistal radius in postmenopausal women. J Bone Miner Res 14:120–124. Schlenker RA, VonSeggen WW. 1976 The distribution of cortical and trabecular bone mass along the lengths of the radius and ulna and the implications for in vivo bone mass measurements. Calcif Tissue Int 20:41–52. Martin AR, Holder LE, Buie V, et al. 1999 Measurement of distal forearm bone mineral density. J Clin Densitom 2:381–387. Glüer C-C, Blake G, Lu Y, Blunt BA, Jergas M, Genant H. 1995 Accurate assessment of precision errors: how to measure the reproducibility of bone densitometry techniques. Osteoporos Int 5:262–270. Seeman E. 2002 An exercise in geometry. J Bone Miner Res 17:373–380. Seeman E. 1997 From density to structure: growing up and growing old on the surfaces of bone. J Bone Miner Res 12:509–521. Rico H, Gonzales-Riola J, Revilla M, Villa LF, GomesCastresana F, Escribano J. 1994 Cortical versus trabecular bone mass: influence of activity on both bone components. Calcif Tissue Int 54:470–472. Westerlind KC, Fluckey JD, Gordon SE, Kraemer WJ, Farrell PA, Turner RT. 1998 Effect of resistance exercise training on cortical and cancellous bone in mature male rats. J Appl Physiol 84:459–464. Todorov T. 1975 Tennis de haut niveau, modifications osseuses et articulaires du membre supérieur actif du joueur. Ann ENSEPS, 8:21–25. Ruff CB, Walker A, Trinkaus E. 1994 Postcranial robusticity in Homo. III. Ontogeny. Am J Phys Anthropol 93:35–54. Haapasalo H, Kontulainen S, Sievänen H, Kannus P, Järvinen M, Vuori I. 2000 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 players. Bone 27:351–357. Bass SL, Saxon L, Daly RM, et al. 2002 The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: a study in tennis players. J Bone Miner Res 17:2274–2280. Heinonen A, McKay HA, Whittall KP, Forster BB, Khan KM. 2001 Muscle cross-sectional area is associated with specific site
Volume 7, 2004
Bone Adaptation Patterns in Tennis Players
34. 35. 36. 37.
of bone in prepubertal girls: a quantitative magnetic resonance imaging study. Bone 29:388–392. Morris M, Jobe FW, Perry J, Pink M, Healy BS. 1989 Electromyographic analysis of elbow function in tennis players. Am J Sports Med 17:241–247. Turner CH, Burr DB. 1993 Basic biomechanical measurements of bone: a tutorial. Bone 14:595–608. Hennig EM, Rosenbaum D, Milani TL. 1992 Transfer of tennis racket vibrations onto the human forearm. Med Sci Sports Exerc 24:1134–1140. Walters J, Koo WWK, Bush A, Hammami M. 1998 Effect of hand dominance on bone mass measurement in sedentary individuals. J Clin Densitom 1:359–367.
Journal of Clinical Densitometry
405 38. Proctor KL, Adams WC, Shaffrath JD, Van Loan MD. 2002 Upper-limb bone mineral density of female collegiate gymnasts versus controls. Med Sci Sports Exerc 34:1830–1835. 39. MacIntyre NJ, Adachi JD, Webber CE. 1999 In vivo detection of structural differences between dominant and nondominant radii using peripheral quantitative computed tomography. J Clin Densitom 2:413–422. 40. Kannus P, Haapasalo H, Sankelo M, et al. 1995 Effect of starting age of physical activity on bone mass in the dominant arm of tennis and squash players. Ann Intern Med 123:27–31. 41. Nara-Ashizawa N, Liu LJ, Higuchi T, et al. 2002 Paradoxical adaptation of mature radius to unilateral use in tennis playing. Bone 30:619–623.
Volume 7, 2004
Original Article
Cortical and Trabecular Bone at the Forearm Show Different Adaptation Patterns in Response to Tennis Playing Gaële Ducher, Stéphanie Prouteau, Daniel Courteix, and Claude-Laurent Benhamou Laboratoire Architecture du lisse Osseux et Exercise Physique, UFR STAPS, Université d’Orléans et Inserm ERIT-M0101, CHR Orléans, Orléans, France
Abstract Bone responds to impact-loading activity by increasing its size and/or density. The aim of this study was to compare the magnitude and modality of the bone response between cortical and trabecular bone in the forearms of tennis players. Bone area, bone mineral content (BMC), and bone mineral density (BMD) of the ulna and radius were measured by dual-energy X-ray absorptiometry (DXA) in 57 players (24.5 ± 5.7 yr old), at three sites: the ultradistal region (50% trabecular bone), the mid-distal regions, and third-distal (mainly cortical bone). At the ultradistal radius, the side-to-side difference in BMD was larger than in bone area (8.4 ± 5.2% and 4.9 ± 4.0%, respectively, p < 0.01). In the cortical sites, the asymmetry was lower (p < 0.01) in BMD than in bone area (mid-distal radius: 4.0 ± 4.3% vs 11.7 ± 6.8%; third-distal radius: 5.0 ± 4.8% vs 8.4 ± 6.2%). The asymmetry in bone area explained 33% of the variance of the asymmetry in BMC at the ultradistal radius, 66% at the mid-distal radius, and 53% at the third-distal radius. The ulna displayed similar results. Cortical and trabecular bone seem to respond differently to mechanical loading. The first one mainly increases its size, whereas the second one preferentially increases its density. Key Words: Bone geometry; trabecular and cortical adaptations; tennis players; bone mineral density.
Introduction
than compact bone, therapeutic effects can be detected earlier in these regions (14). This does not imply, however, that trabecular bone is more sensitive than cortical bone to long-term mechanical loading. Heinonen et al. (15) found that the cortical cross-sectional area at the distal and diaphyseal radii were larger in weight lifters than in nonactive students. Additionally, studies in racket sports revealed that the cortical sites of the diaphyseal humerus display a marked side-to-side difference (also referred to as “asymmetry”) in BMC and cortical wall thickness (16,17). The study of former tennis players led by Etherington et al. (18) reports a significant side-to-side difference in radial BMD at cortical sites (mid and third radius) but not at trabecular sites (ultradistal radius), showing the ability of cortical bone to respond to long-term tennis playing. Although the site-specific effects of mechanical stress have been described on the dominant limb of tennis players (19,20), the authors did not focus on specific trabecular and cortical
Physical activities involving impact and loading forces are known to exert positive effects on bone (1–6). It has been convincingly shown that the bone response to mechanical loading is site-specific, depending on the rate, magnitude, and orientation of the mechanical strains (7,8). Conversely, the skeletal sites that are not loaded during the physical practice tend to show a “deficit” in bone mass (9,10), notably the skull (11). Cross-sectional studies evidenced a higher bone mineral content (BMC) and bone mineral density (BMD) in adult athletes than in sedentary subjects, especially at trabecular bone sites (12,13). Cancellous bone being metabolically more active Received 04/30/04; Revised 07/02/04; Accepted 07/02/04. * Address correspondence to Gaële Ducher, IPROS-C.H.R. Orléans Hoˆpital Porte Madeleine-1 rue Porte Madeleine, BP 2439, 45032 Orléans cedex 1, France. E-mail: [email protected]
399
400 bone adaptations. Depending on the intensity and direction of the forces applied to the bone, a prolonged mechanical stress might affect several aspects of bone modeling and remodeling (21). This approach requires one to differentiate between trabecular and cortical bone sites in order to compare their peculiar responses to long-term physical training. In addition to the respective percentage of trabecular bone, several other factors might explain why distinct skeletal sites respond differently to tennis-induced mechanical strains. Among the factors influencing the bone responsiveness are the distance of the bone site from the point of application of the mechanical forces, the muscular and tendinous insertions, and the vibrations induced by the impacts of the ball on the racket. The ulna and the radius are likely to be loaded differently during tennis playing. Indeed, the muscle attachments differ between these two bones. One could hypothesize that because the ulna does not touch the carpus, it might be less exposed to vibrations than the radius. Our objective was to study the effects of tennis-induced mechanical strains at the dominant distal radius and ulna and to compare them to the nonplaying arm. We have studied the distal epiphysis of the ulna and radius in each arm. Three regions of interest were determined according to their respective trabecular bone content (22): the ultradistal region (approx 50%), the mid-distal region (approx 1%), and thirddistal region (less than 10%).
Materials and Methods Subjects Fifty-seven regional-level tennis players (33 men and 24 women) were recruited in the neighborhood of Orléans (France). All had been practicing tennis for at least 5 yr. As far as the handedness is concerned, there were 52 right-handed players and only 5 left-handed players. Thirty of the players reported using both hands for backhand stroke, the others using their dominant hand only. Exclusion criteria were any past fracture at the radius or ulna as well as any medical disorder or treatment known to affect bone metabolism (exception made for oral contraceptives in 18 out of 24 women). None of the female subjects reported having experienced amenorrhea during their teenage years or twenties. Each participant gave his informed written consent. The study was approved by the Ethics Committee of the Region of Tours.
Anthropometric Measurements Body weight (in kg) was measured on a balance-beam scale (SECA 709, Germany), the subjects wearing only underwear. Body height (in cm) was measured in the upright position to the nearest 1 mm.
Bone Mineral and Body Composition Measurements Bone area (in cm2), bone mineral content (BMC, in g) and bone mineral density (BMD, in g/cm2) were determined by dual-energy X-ray absorptiometry (DXA, Delphi QDR® Journal of Clinical Densitometry
Ducher et al.
Fig. 1. Regions of interest at the distal radius and ulna, used to measure the bone area, BMC, and BMD in tennis players: UD (ultradistal), MID (mid-distal), and 1/3 (third-distal). The regions of interest were defined by the software supplied by the manufacturer (Delphi QDR® Series; Hologic Inc., Waltham, MA, USA).
Series; Hologic Inc., Waltham, MA, USA). Bone area, BMC, and BMD were measured at the whole body and at both forearms. According to their respective trabecular bone content, three sites were defined along the mid-distal to distal region of the radius. The first region, termed “ultradistal radius,” consisted of a 1.5-cm band adjacent to the end plate of the radius; the second region, named “one-third radius,” consisted of a 2-cm band one-third of the distance between the ulnar styloid and the olecranon; and the last region, labeled “middistal,” comprised the residual distance between the two sites mentioned (Fig. 1). Once these sites were defined at the radius, we expanded these regions of interest toward the ulna by prolonging their horizontal boundaries (Fig. 1). We proceeded to separate measurements of bone parameters at the radius and at the ulna because the results could differ between these two bones (23). The intraobserver reproducibility of BMD was calculated by two repeated measurements in seven different forearms by the root mean square (RMS) coefficient of variation (24). The RMS coefficient of variation was 1.1%, 0.6%, and 6.7% for the ultradistal, mid-distal, and third-distal regions, respectively. Volume 7, 2004
Bone Adaptation Patterns in Tennis Players
401
Table 1 Characteristics of the Tennis Players
Age (yr) Height (cm) Weight (kg) Fat mass (%) Whole-body BMD (g/cm2) Starting age of playing (yr) Years of playing Total training time (hr)
Women (n = 24)
Men (n = 33)
Total (n = 57)
21.5 ± 1.8 165.9 ± 4.9 58.9 ± 5.2 23.1 ± 3.7 1.207 ± 0.062 8.3 ± 2.3 13.3 ± 2.6 2945.7 ± 2199.9
26.6 ± 6.6*** 178.5 ± 5.5*** 74.6 ± 8.1*** 14.2 ± 4.2*** 1.306 ± 0.056*** 7.9 ± 2.8 18.3 ± 6.9*** 4069.8 ± 3536.9
24.5 ± 5.7 173.2 ± 8.2 68.0 ± 10.5 18.0 ± 5.9 1.265 ± 0.076 8.1 ± 2.6 16.1 ± 6.0 3579.3 ± 3054.1
Note: Values are means ± SD. Difference between males and females: ***p < 0.001.
Training History The training history was assessed by questionnaire. The participants recorded their starting age of regular tennis playing (at least 1 h per week), number of years of practice, and training volume (hours per week) for each year. Adding up the whole training volume for each subject yielded the total amount of practice for the entire career (total training time), after taking into account the breaks because of injuries or holidays.
Statistical Analysis All of the data are shown as mean ± standard deviation. The Gaussian distribution of the parameters was tested by the Kolmogorov–Smirnov test. The comparison of the parameters measured at the dominant and nondominant forearms was performed using a parametric paired t-test. The side-to-side differences in bone area, BMC, and BMD were expressed as the percentage of the nondominant value (∆% = [(dominant – nondominant)/nondominant] × 100). The three regions of interest were compared by analysis of variance (ANOVA) with repeated measurements. The Newman–Keuls test was used as a post hoc test. The relationship between the significant variables was tested by the Pearson product moment correlation coefficient. Linear regression between bone area asymmetry and BMC asymmetry was plotted. The correlation coefficient r was evaluated and the parameter r2 gave the percentage of the variation of BMC asymmetry that can be explained by the linear regression.
Results Baseline Characteristics of the Subjects The characteristics of the subjects are given in Table 1. The male subjects were significantly older, taller, and heavier than their female counterparts. They also reported a longer tennis practice. They showed a lower percentage of fat mass and a higher whole-body BMD (p < 0.001). All of the subjects were within the norms for fat mass and whole-body BMD, according to the reference databases (including NHANES dataset) supplied by the manufacturer of the densitometer. Journal of Clinical Densitometry
Asymmetry Between the Dominant and Nondominant Forearm The BMC values of the ultradistal, mid-distal, and thirddistal sites are given for both radii and ulnas in Table 2, with the side-to-side difference indicated for each site. For each region of the radius and ulna, the asymmetries in bone area and BMD are shown in Table 3. Bone area, BMC, and BMD were significantly higher at the dominant forearm (p < 0.0001). The players using only the dominant hand for backhand stroke displayed a greater side-to-side difference than those using both hands at the following sites: the ultradistal radius for BMD, the ultradistal ulna for BMC and BMD, and the third-distal radius for BMC (p < 0.05). The largest difference between these two groups was seen at the ultradistal ulna (p < 0.01), with a sideto-side difference reaching up to 19.8% for BMC and 10.9% for BMD in the one-handed backhand players vs 10.0% for BMC and 5.1% for BMD in the two-handed backhand players. After adjustment for the number of playing years and total training time, the difference between the two groups remained significant only at the third-distal ulna. A greater asymmetry was found in men than in women at the ultradistal radius for BMC and BMD and at the third-distal radius for bone area and BMC (p < 0.05). The differences disappeared after adjustment for number of playing years. We investigated whether there was any correlation between the bone asymmetries and the training history. The side-to-side difference in BMD in every site of the radius was associated with the number of years of practice (with an r value ranging from 0.27 to 0.43 according to the site studied) as well as with the total training time (r = 0.29–0.40, p < 0.05). The starting age of tennis playing correlated with the side-to-side difference in BMD of the ultradistal radius (r = –0.29, p < 0.05), as well as of the mid-distal and third-distal ulna (r = –0.38 and –0.33, respectively, p < 0.05).
Side-to-Side Difference in BMC In order to check which of the examined sites had been the most responsive to long-term tennis playing, we compared the Volume 7, 2004
402
Ducher et al. Table 2 BMC at the Dominant and Nondominant Radius and Ulna of the Tennis Players
BMC radius (g) UD MID 1/3 Total BMC ulna (g) UD MID 1/3 Total
Dominant
Nondominant
Side-to-side difference (%)
2.06 ± 0.36 5.19 ± 1.30 2.31 ± 0.42 9.56 ± 2.03
1.81 ± 0.30 4.47 ± 1.06 2.03 ± 0.33 8.31 ± 1.64
13.71 ± 6.77a 16.17 ± 8.30a 13.83 ± 7.40a 14.98 ± 7.03a
UD < MID** 1/3 < MID**
1.00 ± 0.17 3.49 ± 0.80 1.95 ± 0.31 6.42 ± 1.23
0.88 ± 0.14 2.98 ± 0.69 1.81 ± 0.30 5.67 ± 1.09
14.65 ± 12.16a 17.61 ± 10.59a 7.79 ± 6.93a 13.44 ± 7.36a
1/3 < UD** 1/3 < MID**
Note: Three distal regions of interest were analyzed, from the most distal to the most proximal: ultradistal region (UD), mid-distal region (MID), and third-distal region (1/3). The relative side-to-side differences are expressed in percentage of the nondominant value. Values are means ± SD. a Dominant > nondominant, p < 0.0001. ** p < 0.01.
bone asymmetry of each region of interest separately. The mid-distal region showed a greater side-to-side difference in BMC than the ultradistal or third-distal regions at the radius (p < 0.01). Similar results were observed at the ulna, although the difference between the mid-distal and ultradistal sites was not significant (Table 2). ANOVA with repeated measurements revealed that, among all sites, the third-distal ulna had the lowest asymmetry in BMC (p < 0.01).
Side-to-Side Difference in Bone Area and BMD At the radius, the side-to-side difference in bone area was significantly greater at the mid-distal and third-distal regions than at the ultradistal region (p < 0.01, Table 3). Conversely, the BMD asymmetry was more pronounced at the ultradistal radius than at the mid-distal and third-distal sites (p < 0.01). At the ulna, the bone area asymmetry was the highest at the mid-distal site and the lowest at the third-distal site. The only site revealing a difference between the radius and ulna was the third-distal region, with a lower value in bone area asymmetry at the ulna (p < 0.01). The asymmetry was more marked in BMD than in bone area at the ultradistal radius (p < 0.01) and ulna (not significant). The opposite was found at the cortical sites, with a greater side-to-side difference in bone area than in BMD (p < 0.01, except the third-distal ulna: not significant). At the radius, the side-to-side difference in bone area explained 33% of the variance of the BMC asymmetry at the ultradistal site, 66% at the mid-distal site, and 53% at the thirddistal site. At the ulna, r2 values were 47%, 45%, and 59%, respectively.
Discussion This study showed that the bone response to mechanical loading is site-specific. The modality of the bone response difJournal of Clinical Densitometry
fers according to whether the site contains mainly trabecular (ultradistal regions) or cortical bone (mid-distal and third-distal regions). Asymmetry in bone area is considered to reflect asymmetry in bone size. The asymmetry of the cortical regions was more pronounced in bone area than in BMD. Interestingly, the opposite is observed in trabecular sites. Our results suggest that trabecular bone reacts to mechanical strains mainly by increasing its density, whereas cortical bone mainly reacts by increasing its size. These results corroborate with those of other studies using peripheral quantitative computed tomography (pQCT) (19,20). In 16 tennis players, Ashizawa et al. (19) observed that the increase in periosteal area was more important at the mid-distal radius (cortical site) than at the ultradistal radius (trabecular site). In 36 female tennis and squash players, Kontulainen et al. (20) reported a 5% difference in trabecular BMD at the distal radius (trabecular site) in favor of the dominant side, whereas no difference was found in cortical wall thickness. Our results yielded a 8.4% asymmetry in BMD at the ultradistal radius, whereas in the two aforementioned studies, the asymmetry in trabecular BMD at the distal radius was less than 6%. The asymmetry in bone area underestimates the true asymmetry in bone size because DXA is a surfacic method (25,26). As a consequence, the asymmetry in bone density may have been overestimated in the present study. The percentage of trabecular bone reaches up to 85–90% at the ultradistal radius, with a mean slice thickness of 0.2 cm (22). In the present study, the mean trabecular percentage at the ultradistal site might, in fact, be closer to 50% because this site is 1.5 cm in size. It drops to 10% at the mid-distal radius and to 1% at the third-distal radius. Similar values were observed at the ulna (22). The ultradistal site was, hence, considered as being “trabecular,” whereas the mid-distal and thirddistal sites were labeled as “cortical sites.” Volume 7, 2004
Bone Adaptation Patterns in Tennis Players
403
Table 3 Side-to-Side Differences in Bone Area and BMD at the Radius and Ulna Differences between the sites
UD
MID
1/3
Bone area (cm2) ∆ at the radius (%)
4.93 ± 4.03
11.66 ± 6.78
8.43 ± 6.18
UD < MID** UD < 1/3** 1/3 < MID**
∆ at the ulna (%)
6.25 ± 6.74
10.28 ± 6.26
4.16 ± 5.93
UD < MID** 1/3 < MID**
BMD (g/cm2) ∆ at the radius (%)
8.38 ± 5.21
4.04 ± 4.26
5.05 ± 4.80
MID < UD** 1/3 < UD**
∆ at the ulna (%)
7.84 ± 8.14
5.90 ± 4.95
3.47 ± 4.29
1/3 < UD** MID < UD* 1/3 < MID*
Note: The relative side-to-side differences (∆) are expressed in percentage of the nondominant value, and compared between three distal regions of interest: ultra distal region (UD), mid-distal region (MID), and third-distal region (1/3). Values are means ± SD. All of the side-to-side differences are significant (p < 0.0001). * p < 0.05. ** p < 0.01.
It has been suggested that the trabecular and cortical bone tissues do not show the same sensitivity to mechanical loading, possibly the result of the different metabolic activities of these two bone components (27). Because trabecular bone is known to have a rapid turnover, there might be a time gap between trabecular and cortical bone responses. In a short-term longitudinal study on rats, the trabecular sites showed an increase in BMC after a few weeks of training, whereas the effects were not significant at cortical sites (28). In the present study, the side-to-side difference in BMC was the same in cortical and trabecular sites. Except for the thirddistal ulna, where the asymmetry was much lower, all of the regions showed a BMC asymmetry reaching at least 10% and even 15% for the mid-distal sites. These results confirm that cortical bone is highly responsive to long-term mechanical stress (17,29–32). The complexity of mechanical loading forces during tennis playing might explain why the asymmetry was so pronounced at both cortical and trabecular bone sites. It has been shown that the mechanical stress was more efficient when the strain distribution is different from the normal strains to which the bone had adapted (7,8). In prepubertal girls, Heinonen et al. (33) showed that there is a regional, site-specific interplay between muscles and bone in the lower limb. Hitting the tennis ball involved several muscles, including the pronator teres and the brachioradialis (34), which display large insertions on the distal radius. The pronator teres shows only a marginal insertion on the distal ulna. This could explain why the third-distal ulna showed a weaker asymmetry than the other sites. Journal of Clinical Densitometry
During tennis strokes, the forearm must counteract the backward movement of the racket at the impact. From a mechanical point of view, a bending force applied on a hollow cylindrical bone imposes a high stress on the external cortical shell (35). The further the point from the force application, the higher the stress (18). High bending forces during weight-lifting tend to enlarge bones (15). Likewise, a marked increase in bone area at the mid-distal and third-distal regions was observed in the present study. The repeated impacts of the ball on the strings lead to racket vibrations, which are transmitted to forearm bones. Hennig et al. (36) fastened strain-gage-type sensors on the skin and found wrist and elbow vibratory accelerations of 6.81 and 1.53 g, respectively (g = 9.81 m/s2) for center ball impacts. This result suggests that vibrations are damped along the bone as the distance to the point of impact increases. Sedentary subjects display side-to-side differences in bone area, BMC (37), BMD (38), and also trabecular bone structure (39). Therefore, all of the asymmetries described in the present study cannot be completely attributed to tennis playing. However, the asymmetry is much weaker in control subjects (less than 5% on average) than in tennis players (16,17,40). In conclusion, these data suggest that the cortical and trabecular bone tissues respond differently to mechanical loading, the first one mainly increasing its size and the second one preferentially increasing its density. This assumption might not necessarily be valid for mature bones, which show a reduced ability to increase their size in response to mechanical loading (20,41). The ability of cortical bone to grow periosteally in response to mechanical loading improves the Volume 7, 2004
404 ability of bone to resist bending and torsional forces. The increase in bone density at trabecular sites enhances the ability of bone to withstand compressive forces (35). Thus, the specificity of the bone response at cortical and trabecular sites is of critical importance when considering the effects of physical activity on the mechanical competence of bones.
Acknowledgments This research was supported by a grant from the Région Centre and the Inserm (Institut National de la Santé Et de la Recherche Médicale). The authors confirm that all of the experiments comply with the current French laws.
References 1. Cassell C, Benedict M, Specker B. 1996 Bone mineral density in elite 7- to 9-yr-old female gymnasts and swimmers. Med Sci Sports Exerc 28:1243–1246. 2. Dyson K, Blimkie CJ, Davison KS, Webber CE, Adachi JD. 1997 Gymnastic training and bone density in pre-adolescent females. Med Sci Sports Exerc 29:443–450. 3. Courteix D, Lespessailles E, Peres SL, Obert P, Germain P, Benhamou CL. 1998 Effect of physical training on bone mineral density in prepubertal girls: a comparative study between impactloading and non-impact-loading sports. Osteoporos Int 8:152–158. 4. Lima F, De Falco V, Baima J, Carazzato JG, Pereira RMR. 2001 Effect of impact load and active load on bone metabolism and body composition of adolescent athletes. Med Sci Sports Exerc 33:1318–1323. 5. Duncan CS, Blimkie CJ, Cowell CT, Burke ST, Briody JN, Howman-Giles R. 2002 Bone mineral density in adolescent female athletes: relationship to exercise type and muscle strength. Med Sci Sports Exerc 34:286–294. 6. Duncan CS, Blimkie CJ, Kemp A, et al. 2002 Mid-femur geometry and biomechanical properties in 15- to 18-yr-old female athletes. Med Sci Sports Exerc 34:673–681. 7. Burr DB, Robling AG, Turner CH. 2002 Effects of biomechanical stress on bones in animals. Bone 30:781–786. 8. Ehrlich PJ, Lanyon LE. 2002 Mechanical strain and bone cell function: a review. Osteoporos Int 13:688–700. 9. Karlsson MK, Hasserius R, Obrant KJ. 1996 Bone mineral density in athletes during and after career: a comparison between loaded and unloaded skeletal regions. Calcif Tissue Int 59:245–248. 10. Magnusson H, Linden C, Karlsson C, Obrant KJ, Karlsson MK. 2001 Exercise may induce reversible low bone mass in unloaded and high bone mass in weight-loaded skeletal regions. Osteoporos Int 12:950–955. 11. Courteix D, Lespessailles E, Obert P, Benhamou CL. 1999 Skull bone mass deficit in prepubertal highly-trained gymnast girls. Int J Sports Med 20:328–333. 12. Suominen H. 1993 Bone mineral density and long term exercise. An overview of cross-sectional athlete studies. Sports Med 16:316–330. 13. Forwood MR, Burr DB. 1993 Physical activity and bone mass: exercises in futility? Bone Miner 21:89–112. 14. Augat P, Fuerst T, Genant H. 1998 Quantitative bone mineral assessment at the forearm: a review. Osteoporos Int 8:299–310. 15. Heinonen A, Sievanen H, Kannus P, Oja P, Vuori I. 2002 Sitespecific skeletal response to long-term weight-training seems to
Journal of Clinical Densitometry
Ducher et al.
16. 17.
18.
19. 20.
21.
22.
23. 24.
25. 26. 27.
28.
29. 30. 31.
32.
33.
be attributable to principal loading modality: a pQCT study of female weightlifters. Calcif Tissue Int 70:469–474. Kannus P, Haapasalo H, Sievänen H, Oja P, Vuori I. 1994 The site-specific effects of long-term unilateral activity on bone mineral density and content. Bone 15:279–284. Haapasalo H, Sievänen H, Kannus P, Heinonen A, Oja P, Vuori I. 1996 Dimensions and estimated mechanical characteristics of the humerus after long-term tennis loading. J Bone Miner Res 11:864–872. Etherington J, Harris PA, Nandra D, et al. 1996 The effect of weight-bearing exercise on bone mineral density: a study of female ex-elite athletes and the general population. J Bone Miner Res 11:1333–1338. Ashizawa N, Nonaka K, Michikami S, et al. 1999 Tomographical description of tennis-loaded radius: reciprocal relation between bone size and volumetric BMD. J Appl Physiol 86:1347–1351. Kontulainen S, Sievänen H, Kannus P, Pasanen M, Vuori I. 2002 Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquet-sports players: a peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res 17:2281–2289. Adami S, Gatti D, Braga V, Bianchini D, Rossini M. 1999 Sitespecific effects of strength training on bone structure and geometry of ultradistal radius in postmenopausal women. J Bone Miner Res 14:120–124. Schlenker RA, VonSeggen WW. 1976 The distribution of cortical and trabecular bone mass along the lengths of the radius and ulna and the implications for in vivo bone mass measurements. Calcif Tissue Int 20:41–52. Martin AR, Holder LE, Buie V, et al. 1999 Measurement of distal forearm bone mineral density. J Clin Densitom 2:381–387. Glüer C-C, Blake G, Lu Y, Blunt BA, Jergas M, Genant H. 1995 Accurate assessment of precision errors: how to measure the reproducibility of bone densitometry techniques. Osteoporos Int 5:262–270. Seeman E. 2002 An exercise in geometry. J Bone Miner Res 17:373–380. Seeman E. 1997 From density to structure: growing up and growing old on the surfaces of bone. J Bone Miner Res 12:509–521. Rico H, Gonzales-Riola J, Revilla M, Villa LF, GomesCastresana F, Escribano J. 1994 Cortical versus trabecular bone mass: influence of activity on both bone components. Calcif Tissue Int 54:470–472. Westerlind KC, Fluckey JD, Gordon SE, Kraemer WJ, Farrell PA, Turner RT. 1998 Effect of resistance exercise training on cortical and cancellous bone in mature male rats. J Appl Physiol 84:459–464. Todorov T. 1975 Tennis de haut niveau, modifications osseuses et articulaires du membre supérieur actif du joueur. Ann ENSEPS, 8:21–25. Ruff CB, Walker A, Trinkaus E. 1994 Postcranial robusticity in Homo. III. Ontogeny. Am J Phys Anthropol 93:35–54. Haapasalo H, Kontulainen S, Sievänen H, Kannus P, Järvinen M, Vuori I. 2000 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 players. Bone 27:351–357. Bass SL, Saxon L, Daly RM, et al. 2002 The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: a study in tennis players. J Bone Miner Res 17:2274–2280. Heinonen A, McKay HA, Whittall KP, Forster BB, Khan KM. 2001 Muscle cross-sectional area is associated with specific site
Volume 7, 2004
Bone Adaptation Patterns in Tennis Players
34. 35. 36. 37.
of bone in prepubertal girls: a quantitative magnetic resonance imaging study. Bone 29:388–392. Morris M, Jobe FW, Perry J, Pink M, Healy BS. 1989 Electromyographic analysis of elbow function in tennis players. Am J Sports Med 17:241–247. Turner CH, Burr DB. 1993 Basic biomechanical measurements of bone: a tutorial. Bone 14:595–608. Hennig EM, Rosenbaum D, Milani TL. 1992 Transfer of tennis racket vibrations onto the human forearm. Med Sci Sports Exerc 24:1134–1140. Walters J, Koo WWK, Bush A, Hammami M. 1998 Effect of hand dominance on bone mass measurement in sedentary individuals. J Clin Densitom 1:359–367.
Journal of Clinical Densitometry
405 38. Proctor KL, Adams WC, Shaffrath JD, Van Loan MD. 2002 Upper-limb bone mineral density of female collegiate gymnasts versus controls. Med Sci Sports Exerc 34:1830–1835. 39. MacIntyre NJ, Adachi JD, Webber CE. 1999 In vivo detection of structural differences between dominant and nondominant radii using peripheral quantitative computed tomography. J Clin Densitom 2:413–422. 40. Kannus P, Haapasalo H, Sankelo M, et al. 1995 Effect of starting age of physical activity on bone mass in the dominant arm of tennis and squash players. Ann Intern Med 123:27–31. 41. Nara-Ashizawa N, Liu LJ, Higuchi T, et al. 2002 Paradoxical adaptation of mature radius to unilateral use in tennis playing. Bone 30:619–623.
Volume 7, 2004