Osteoporosis International

, Volume 19, Issue 7, pp 1011–1018 | Cite as

Trabecular bone microarchitecture in female collegiate gymnasts

Original Article

Abstract

Summary

Using high-resolution magnetic resonance imaging, we observed more developed trabecular bone microarchitecture in the proximal tibia of female collegiate gymnasts vs. matched controls. This suggests that high-load physical activity may have a positive effect on the trabecular microarchitecture in weight-bearing bone.

Introduction

Participation in physical activities that overload the skeleton, such as artistic gymnastics, is associated with increased areal bone mineral density (aBMD); however, the status of trabecular microarchitecture in the weight-bearing bone of gymnasts is unknown.

Methods

Eight female collegiate artistic gymnasts and eight controls matched for age, height, body mass, gender and race were recruited for the study. Apparent trabecular bone volume to total volume (appBV/TV), trabecular number (appTb.N), thickness (appTb.Th) and trabecular separation (appTb.Sp) were determined using high resolution magnetic resonance imaging. Areal bone mineral density, bone mineral content (BMC) and bone area in the proximal tibia were determined using dual-energy X-ray absorptiometry. Group differences were determined using t-tests. The magnitude of group differences was expressed using Cohen’s d (d).

Results

Gymnasts had higher appBV/TV (13.6%, d = 1.22) and appTb.N (8.4%, d = 1.45), and lower appTb.Sp (13.7%, d = 1.33) than controls (p < 0.05). Gymnasts had higher aBMD and BMC in the proximal tibia, although the differences were smaller in magnitude (d = 0.75 and 0.74, respectively) and not statistically significant (p > 0.05).

Conclusion

The findings suggest that high-load physical activity, such as performed during gymnastics training, may enhance the trabecular microarchitecture of weight-bearing bone.

Keywords

Exercise Gymnastics Magnetic resonance imaging Mechanical loading Physical activity 

Introduction

Physical activity, especially activity that includes high-load movements, is regarded as a powerful environmental determinant of bone mass. This idea is supported by cross-sectional studies demonstrating elevated levels of bone mass in athletes involved in high-load physical activity [1, 2, 3] and longitudinal studies demonstrating increases in areal bone mineral density (aBMD) and bone mineral content following jump training [4], weight lifting [5, 6] and artistic gymnastics participation [7, 8]. While physical activity clearly has a positive effect on measures of bone mass, such as aBMD, its effect on trabecular bone microarchitecture is less understood [9]. Trabecular bone microarchitecture is an important skeletal feature that identifies those with fracture as well as, or better than, aBMD [10, 11]. Furthermore, when measures of trabecular bone microarchitecture are combined with aBMD, the prediction of bone mechanical strength is improved [11, 12, 13]. Thus, understanding the effect of physical activity on trabecular bone microarchitecture is of interest.

The importance of physical activity in the optimization or maintenance of the network of trabecular bone is supported by immobilization studies of lower mammals in which marked reductions in trabecular bone volume to total volume, trabecular number and increases in trabecular separation have been observed [14, 15, 16, 17, 18]. Similarly, trabecular bone microarchitecture is drastically deteriorated in adults with complete spinal cord injury [19, 20], and it is severely underdeveloped in children with cerebral palsy who are unable to ambulate independently [21]. While studies in rats suggest physical activity can enhance the trabecular structure in healthy bone [22] and can restore lost trabeculae due to unloading [23], the effect on human bone has not been determined. One approach to studying the potential effects of physical activity on trabecular bone microarchitecture is to examine athletes that participate in unusually high levels of physical activity, such as artistic gymnasts. This unique population performs maneuvers that place loads on the skeleton up to 10 times body weight [24]. Young female artistic gymnasts also exhibit high levels of bone mass, as indicated by aBMD as much as 45% higher than matched controls [25]. However, the status of trabecular bone microarchitecture in artistic gymnasts, and other athletic groups, has not been investigated. If it is determined that the microarchitecture of trabecular bone is enhanced in artistic gymnasts relative to non-athlete controls, it would suggest that human trabeculae have a certain degree of plasticity and respond positively to high-load physical activity.

The purpose of the present study was to determine if the trabecular bone microarchitecture in the proximal tibia of female collegiate artistic gymnasts is enhanced compared to controls of similar age, height, body mass and race. Based on previous studies in lower mammals, we hypothesized that apparent trabecular number would be higher and apparent trabecular separation would be lower in the proximal tibia of gymnasts than controls.

Materials and methods

Subjects

Eight NCAA Division I female collegiate gymnasts and eight females who had never participated in collegiate athletics and never participated in competitive gymnastics were recruited for the study. Women were excluded from the study if they had a history of chronic medication use, other than low-dose oral contraceptives, or if they had a previous fracture in a nondominant extremity. Gymnasts and controls were matched for age (±5 years), height (±4 cm), body mass (±6 kg) and race. Controls were recruited from the university community using flyers. The study was approved by the university institutional review board and written consent was given by each subject before data collection.

Anthropometrics

Standing height and body mass were measured by the same investigator with subjects wearing light clothing and without footwear. Height was measured using a stadiometer to the nearest 0.1 cm (Seca model 222, Novel Products, Rockton, IL). Body mass was measured to the nearest 0.2 kg using a double-beam balance (Fairbanks Scales, Kansas City, MO).

Physical activity

Physical activity, total energy expenditure and energy expenditure from exercise were estimated using an interviewer administered 7-day recall of physical activity [26]. Subjects reported the amount of time spent sleeping and participating in moderate, hard and very hard physical activities. All remaining time was classified as light physical activity. The 7-day recall of physical activity has established reliability and validity in college students [27].

Diet

Diet information was collected using an interviewer administered 24-hour recall of food intake from the previous day. Food models were used to aid subjects in the estimation of portion sizes. Total energy intake, percent energy from fat, carbohydrates and protein and calcium intake were estimated using the USDA Food and Nutrient Database for Dietary Studies, 1.0 [28]. Energy availability was determined by subtracting energy expenditure from exercise (estimated using the 7-day recall of physical activity) from total energy intake and dividing the difference by total fat-free mass (determined using dual-energy X-ray absorptiometry; DXA).

Magnetic resonance imaging

The nondominant leg was placed in a dedicated holder constructed in-house. In gymnasts, the dominant leg was the leg they used for take-off or preferably landed on when performing vault, floor routines, etc. In controls, the dominant leg was the leg they preferred to use when kicking a ball. The proximal tibia was identified using a sagittal localizer and imaged using a GE 1.5 T magnetic resonance imager and a bilateral dual phased array coil. Sixty high resolution axial images of the proximal tibia were collected using a 3D fast gradient echo sequence with a partial echo acquisition (echo time = 4.5 ms; repetition time = 30 ms; 40° flip angle; 15.6 kHz bandwidth), a 10 cm field of view and an imaging matrix of 512 × 384 zero-filled to 512 yielding a voxel size of 195 × 195 × 1000 μm3.

Measures of trabecular bone microarchitecture, such as apparent trabecular bone volume to total volume (appBV/TV), trabecular number (appTb.N, mm−1), trabecular thickness (appTb.Th, mm), and trabecular separation (appTb.Sp, mm), were determined using the following procedure [29, 30]. Reconstructed volumetric data was transferred to a Sun workstation (Sun Microsystems, Mountainview, CA). A 3-D low-pass filter-based correction was applied to images to eliminate potential inhomogeneity caused by the surface coils. The first and last 5 sets of images were removed from the analysis to minimize artifacts from slice selection profile imperfection. Images were displayed in the reverse gray scale to facilitate visualization. Regions of interest containing the trabecular bone and marrow portions of the proximal tibia were drawn manually over approximately 30 images per bone. To quantify the trabecular network, images were segmented into bone and marrow phases and appBV/TV, appTb.N, appTb.Th and appTb.Sp were determined as previously described [19, 29, 30].

The coefficient of variation for repeat assessment of appBV/TV, appTb.N, appTb.Th and appTb.Sp in the proximal tibia is 4.0, 3.3, 1.4 and 4.6%, respectively [30].

Dual-energy X-ray absorptiometry

Dual-energy X-ray absorptiometry (Delphi A; Hologic, Inc, Bedford, MA) was used to assess total body fat percentage, fat mass and fat-free soft tissue mass and proximal tibia, total body, nondominant upper extremity and nondominant lower extremity aBMD, BMC and bone area. The proximal tibia was evaluated using the radius protocol and a high resolution scan that was 94 mm in length. A region within the total image approximating the region assessed using MRI (30 mm) was analyzed using the Global Region of Interest Analysis software. The total body and the nondominant upper and lower extremity were evaluated using a standard total body scan. The upper and lower extremities were separated from the total body using the manufacturer-defined analysis procedure. Quality control was checked before each test session by scanning a lumbar spine phantom consisting of calcium hydroxyapatite embedded in a cube of thermoplastic resin (model DPA/QDR-1; Hologic x-caliber anthropometric spine phantom). To assess the short-term reliability of proximal tibia aBMD, BMC and bone area, six individuals were tested twice on separate days or on the same day after repositioning. The coefficients of variation for aBMD, BMC and bone area were 1.3, 1.3 and 1.6%, respectively.

Statistics

Data were analyzed using SPSS, version 14.0 (Chicago, IL). The Shapiro–Wilk test was used to check data for normal distribution. If data were normally distributed (p > 0.05), independent t-tests were used to determine group differences. Mann–Whitney U tests were used if data were not normally distributed. An alpha level of 0.05 was used to detect statistical differences between groups. Mean±SD was reported for all data. If data were not normally distributed, medians and ranges were also reported. An alpha level of 0.05 was used to detect statistical differences between groups. The magnitude of effects was assessed using Cohen’s d (d), with values of 0.2, 0.5 and 0.8 indicating small, medium and large effects [31].

Results

All data were normally distributed except age, number of menstrual cycles during the past year, oral contraceptive use during the past year (yes = 1, no = 0), very hard physical activity, calcium intake, appTb.N in the proximal tibia and nondominant upper extremity BMC (Shapiro–Wilk test <0.05).

Each group consisted of seven Caucasian women and one African American woman. Physical characteristics of the two groups are reported in Table 1. There were no differences in age (gymnast median = 20.0 y, range = 19 – 22 y; control median = 21.0 y, range = 19 – 25 y), height and body mass between the two groups. Gymnasts had a lower total body fat percentage (d = 3.08), lower fat mass (d = 2.44), and higher fat-free mass (d = 1.69) than controls (p < 0.05). Reported age at menarche was higher in gymnasts than controls (d = 1.37, p < 0.05). There was no group difference in the number of menstrual cycles during the past year (gymnasts median = 12 cycles, range = 4 to 12 cycles; control median = 12 cycles, no range; p = 0.176). While all controls and six of the eight gymnasts reported experiencing all menstrual periods during the past year, one gymnast reported having only four periods and another gymnast reported having only eight periods. There was no group difference (p < 0.05) in low-dose oral contraceptive use during the past year (gymnasts median = 1, range = 0 to 1; controls median = 0; range = 0 to 1). All of the gymnasts (n = 4) and controls (n = 3) who used low-dose oral contraceptives during the past year used combined oral contraceptives (i.e., contain estrogen and progestin). On average, gymnasts were participating in organized gymnastics for >15 years.
Table 1

General characteristics of female collegiate artistic gymnasts and non-athlete controls

 

Gymnasts (n = 8)

Controls (n = 8)

Age

19.9 ± 1.0

21.1 ± 1.8

Height (cm)

160.1 ± 3.3

159.4 ± 5.6

Total body

 %Fat

17.8 ± 2.0*

28.2 ± 4.8

 Fat mass (kg)

10.0 ± 1.0*

16.2 ± 4.0

 Fat-free mass (kg)

46.5 ± 3.6*

40.7 ± 3.4

Menarche (y)

15.0 ± 1.9*

12.8 ± 1.3

Menstrual cycles/y

10.5 ± 3.0

12.0 ± 0.0

OC use during the past year (no/yes)

4/4

5/3

Years of gymnastics training

15.8 ± 1.7*

0.0 ± 0.0

Values are means±SD except oral contraceptive (OC) use during the past year

*Different from controls (p < 0.05)

Physical activity and diet data are reported in Table 2. There was no group difference in hours of sleep per day. There was a trend for less light (d = 1.08) and moderate (d = 0.99) physical activity in gymnasts than controls, but the differences were not statistically significant (p = 0.062 and 0.068, respectively). Gymnasts compared to controls participated in a significantly more hard (d = 1.20) and very hard (d = 6.97; gymnast median = 1.9 hours/d, range = 0.6 to 2.1 hours/d; control median = 0.0, no range) physical activity (p < 0.05). Total estimated energy expenditure was higher in gymnasts than controls (d = 2.34, p < 0.05). Estimated energy expenditure from exercise was also higher in gymnasts than controls (d = 4.30, p < 0.05). There were no differences (p > 0.05) in estimated energy intake, percent of energy from protein, percent of energy from fat, percent of energy from carbohydrate or calcium intake (gymnast median  =  804 mg/d, range  =  329 to 2330 mg/d; control median = 803 mg/d, range = 242 to 1339 mg/d). Estimated energy availability was lower in gymnasts than controls (p < 0.05).
Table 2

Physical activity and diet of female collegiate artistic gymnasts and non-athlete controls

 

Gymnasts (n = 8)

Controls (n = 8)

Physical activity

 Sleep (hours/d)

7.2 ± 1.4

7.7 ± 0.9

 Light (hours/d)

14.1 ± 1.5

15.4 ± 0.9

 Moderate (hours/d)

0.4 ± 0.2

0.6 ± 0.2

 Hard (hours/d)

0.6 ± 0.2*

0.3 ± 0.3

 Very hard (hours/d)

1.6 ± 0.6*

0.0 ± 0.0

Total estimated energy expenditure (kcal)

2778 ± 320

1975 ± 265

Estimated energy expenditure from exercise (kcal)

1098 ± 338

109 ± 122

Estimated energy intake (kcal/d)

1899 ± 578

2021 ± 192

Energy from protein (%)

15.7 ± 6.0

15.0 ± 6.4

Energy from fat (%)

32.5 ± 5.0

31.3 ± 9.5

Energy from carbohydrate (%)

51.8 ± 6.8

53.7 ± 14.0

Calcium (mg/d)

963 ± 610

856 ± 419

Estimated energy availability (kcal/kg fat-free mass)

17.7 ± 12.5*

48.0 ± 5.0

Values are means±SD

*Different from controls (p < 0.05)

Measures of trabecular bone microarchitecture in the proximal tibia are reported in Table 3. Gymnasts had 13.6% higher appBV/TV (d = 1.22), 8.4% higher appTb.N (d = 1.45; gymnast median = 1.42 mm−1, range = 1.31–1.49 mm−1; control median = 1.33 mm−1, range = 1.12–1.37 mm−1) and 13.7% lower appTb.Sp (d = 1.33) than controls (p < 0.05). There was a trend for higher appTb.Th (6.3%, d = 0.83), although the difference was not statistically significant (p = 0.121).
Table 3

Measures of trabecular bone microarchitecture in the proximal tibia of female collegiate artistic gymnasts and non-athlete controls

 

Gymnasts (n = 8)

Controls (n = 8)

appBV/TV

0.318 ± 0.040*

0.274 ± 0.032

appTb.N (mm−1)

1.411 ± 0.057*

1.309 ± 0.084

appTb.Th (mm)

0.222 ± 0.018

0.209 ± 0.013

appTb.Sp (mm)

0.484 ± 0.051*

0.561 ± 0.065

Values are means±SD

*Different from controls (p < 0.05)

apparent trabecular bone volume to total volume = appBV/TV, trabecular number = appTb.N, thickness = appTb.Th = and trabecular separation = appTb.Sp

Areal bone mineral density, BMC and bone area of the nondominant proximal tibia, nondominant upper extremity, nondominant lower extremity and total body are presented in Table 4. While moderate to large effect sizes suggest gymnasts had higher aBMD (10.4%, d = 0.75) and BMC (9.5%, d = 0.74) than controls in the proximal tibia, they were not statistically significant (p = 0.156 and 0.180, respectively). There was no group difference in proximal tibia bone area. Gymnasts had higher nondominant upper extremity aBMD (15.3%, d = 1.68), BMC (26.2%, d = 1.55; gymnast median = 157.2 g, range = 115.1–190.2 g; control median = 115.1 g, range = 108.0–155.7 g) and bone area (9.4%, d = 1.12) than controls (p < 0.05). Gymnasts also had higher aBMD (14.0%, d = 1.45), BMC (23.2%, d = 1.79) and bone area (8.0%, d = 1.29) in the nondominant lower extremity (p < 0.05). In the total body, higher BMC (15.8%, d = 1.20) and bone area (6.9%, d = 1.28) were observed in gymnasts (p < 0.05). There was not a statistically significant group difference in total body aBMD (p = 0.129), although a large effect size (d = 0.87) suggests it was 8.3% higher in gymnasts.
Table 4

Areal bone mineral density (aBMD), bone mineral content and bone area in the extremities and in the total body of female collegiate artistic gymnasts and non-athlete controls

 

Gymnasts (n = 8)

Controls (n = 8)

Nondominant proximal tibia

 aBMD (g/cm2)

0.998 ± 0.122

0.904 ± 0.127

 Bone mineral content (g)

15.3 ± 1.4

14.0 ± 2.2

 Bone area (cm)

15.4 ± 1.2

15.6 ± 1.4

Nondominant upper extremity

 aBMD (g/cm2)

0.793 ± 0.084*

0.688 ± 0.041

 Bone mineral content (g)

152.5 ± 24.9*

120.8 ± 16.1

 Bone area (cm)

191.4 ± 14.4*

174.9 ± 15.1

Nondominant lower extremity

 aBMD (g/cm2)

1.237 ± 0.117*

1.085 ± 0.093

 Bone mineral content (g)

420.8 ± 46.2*

341.6 ± 42.1

 Bone area (cm)

339.9 ± 14.1*

314.7 ± 25.1

Total body

 aBMD (g/cm2)

1.184 ± 0.146

1.093 ± 0.063

 Bone mineral content (g)

2295 ± 311*

1983 ± 210

 Bone area (cm)

1936 ± 81*

1811 ± 117

Values are means±SD

*Different from controls (p < 0.05)

Representative proximal tibia magnetic resonance images are presented in Fig. 1. Consistent with the results of the study, more trabecular bone (black) and less marrow (white) is depicted in the gymnast image on the left vs. the control image on the right.
Fig. 1

High-resolution magnetic resonance images of the proximal tibia of a female collegiate artistic gymnast (a) and a female control (b). There is a greater amount of trabecular bone (black) and less marrow (white) in the gymnast’s proximal tibia, which is highlighted by the magnified subregions presented at the top right of each image

Discussion

The purpose of the present study was to determine if the trabecular bone microarchitecture in the proximal tibia of female collegiate artistic gymnasts, a group noted for their very high bone mass, is enhanced relative to controls not different in age, height, body mass, gender and race. The finding that gymnasts had higher appBV/TV and appTb.N and lower appTb.Sp in the proximal tibia than controls suggests high-load physical activity has a positive influence on the trabecular network of weight bearing bone. Specifically, the higher appTb.N and lower appTb.Sp suggests gymnasts had a greater number of trabeculae that were closer together.

To our knowledge, this is the first study to assess trabecular bone microarchitecture using high-resolution magnetic resonance imaging in a group of athletes participating in high-load physical activity and known for extreme levels of bone mass. It is not known if the more developed trabecular bone microarchitecture in the gymnasts is due to the gymnastics activity or due to self-selection of those with better bone structure into the sport of gymnastics; however, the findings are consistent with reports in rats. Treadmill training has been shown to increase the number and thickness of trabeculae in the distal femur [22] and to restore reductions in BV/TV and Tb.N in the proximal tibia of young rats [15]. The findings from the present study are also consistent with the observation that gymnasts have higher broadband ultrasonic attenuation than non-athlete controls [32]. There is evidence that broadband ultrasonic attenuation is an indicator of trabecular bone microarchitecture [33, 34]. Moreover, broadband ultrasonic attenuation has been found to increase to a greater extent in male elite gymnasts during 18 month months of gymnastics training than in controls [35]. The importance of loading in the maintenance of trabecular structure is further demonstrated by the markedly deteriorated trabecular bone microarchitecture in individuals with complete spinal cord injury [19, 20]. Compared to controls, there was ∼20% lower apparent trabecular bone number and more than 30% greater apparent trabecular separation in the distal femur and proximal tibia of men with complete and long-term spinal cord injury [19]. Together, these findings suggest the trabecular microarchitecture in human bone has a certain degree of plasticity and responds to changes in loading patterns.

It is plausible that other factors could have contributed to the difference in trabecular bone microarchitecture and aBMD in gymnasts compared to controls. Irregular menstruation [36], delayed menarche [37], use of combined oral contraceptives [38, 39], low calcium intake [40] and low energy availability [41] have been linked to poor bone mineral accretion, reduced bone formation, low bone mass and/or thin bones. In the present study, it is unlikely that menstrual irregularity during the past year contributed significantly to the bone disparity between gymnasts and controls because only two gymnasts and no controls reported missing a menstrual cycle. Current use of combined oral contraceptives probably did not contribute to the bone disparity between gymnasts and controls because a similar number of gymnasts (n = 4) and controls (n = 3) reported using combined oral contraceptives during the past year. It is also unlikely that current calcium intake contributed to the bone disparity because calcium intake in gymnasts was not different from controls. On the other hand, age at menarche was higher in gymnasts than controls, which is consistent with previous observations [42]. Delayed menarche is associated with lower aBMD from DXA and lower stiffness, speed of sound and broadband ultrasound attenuation from quantitative ultrasound [37]. Furthermore, estimated energy availability was lower in gymnasts than controls and it was lower than the threshold (<30 kcal/kg fat-free mass) associated with decreased bone formation [41]. Despite their older age at menarche and signs of low energy availability, gymnasts had higher aBMD and BMC at most sites studied and had greater development of trabecular bone microarchitecture in the proximal tibia. This suggests the mechanical loading associated with gymnastics may override the delayed menarche and energy restriction that is present in some high-level artistic gymnasts.

Although differences in aBMD and BMC from DXA in the proximal tibia of gymnasts and controls were not significantly significant (p > 0.05), moderate to large effect sizes suggest they were higher in gymnasts. It is likely that statistically significant differences would have been observed if larger sample sizes were studied. This idea is consistent with previous reports demonstrating higher aBMD and BMC in gymnasts than controls at sites that are heavily loaded during gymnastics activity [25, 43]. Kirchner et al. [42] reported 18 to 25% higher aBMD in the lumbar spine, total proximal femur, femoral neck and Ward’s triangle of 26 collegiate artistic gymnasts compared to 26 controls. In addition to a larger sample, the effect sizes (d range = 1.84 to 2.15) indicate a larger group effect for lumbar spine, femoral neck and proximal femur aBMD in the Kirchner study than observed for proximal tibia aBMD in the present study. Helge et al. [25] reported 24% to 45% higher aBMD in the lumbar spine, femoral neck, trochanter and radius of young artistic gymnasts 15 to 20 years of age compared to controls. Despite a small sample of gymnasts and controls (n = 6/group), the differences were statistically significant (p < 0.05) suggesting that the effect sizes were large. In the present study, more substantial differences in aBMD were observed in the nondominant upper and lower extremity than in the proximal tibia of gymnasts, as indicated by higher effect sizes (d = 1.68 and 1.45, respectively, vs. 0.75). The effect sizes for appBV/TV, appTb.N and appTb.Sp were also higher than the effect sizes for the DXA-derived aBMD and BMC in the proximal tibia suggesting that MRI-derived measures of trabecular bone microarchitecture may be more sensitive to differences in bone at the proximal tibia in artistic gymnasts. This is important because aBMD is widely used as a surrogate of bone health and fracture risk. Thus, the potential benefits of gymnastics exercise on the proximal tibia would be underestimated if only DXA-derived measures of bone status were studied.

There are limitations to the study that should be considered. It is possible that females with better trabecular bone microarchitecture choose to participate in and are successful at high-level gymnastics activity, a common bias in cross-sectional studies. Another limitation of the study is that if mechanical loading associated with gymnastics exercise enhances the trabecular microarchitecture in weight bearing bone, it is not clear when the changes occur. There is evidence that the most substantial effect of exercise on bone occurs during childhood and adolescence, with a more limited effect during adulthood [43, 44]. However, mechanical loading has been shown to increase trabecular number and thickness in immature [15, 22] and mature [45, 46, 47] animals. A third limitation of the study is the methods used to assess hormonal status and diet. While delayed menarche was reported in gymnasts, and delayed menarche is negatively associated with bone [37], direct measures of current hormone status were not assessed. Although estimated energy availability was lower in gymnasts than controls, the method used to assess diet in the present study (i.e., 24-hour dietary recall) provides a limited representation of current dietary intake and poorly reflects diet history [48]. Furthermore, it is possible that gymnasts underreported their energy intake [49]. A fourth limitation of the study is the inclusion of combined oral contraceptive users. The effect of low-dose combined oral contraceptives on bone is still unclear; however, there is evidence that aBMD is lower and bone accretion is suppressed in adolescents and young adult women who use combined oral contraceptives compared to nonusers [38, 39]. Fortunately, a similar number of gymnasts and controls were using combined oral contraceptives. A fifth limitation of the study is that appBV/TV and appTb.N overestimate actual BV/TV and Tb.N, respectively, and appTb.Sp underestimates actual Tb.Sp; however, these apparent measures and their intended measures are strongly correlated [50]. Moreover, the apparent measures can discriminate between those with and without fracture [51]. Although appTb.Th from MRI was higher in gymnasts than controls, the difference was not statistically significant. The lack of a significant difference is not surprising because the study was underpowered to detect differences in appTb.Th. Furthermore, appTb.Th is less strongly correlated with the true measure of trabecular thickness than other apparent measures of trabecular bone microarchitecture (i.e., appBV/TV, appTb.N and appTb.Sp) are correlated with their true measures [50]. The lack of a statistically significant difference in appTb.Th between gymnasts and controls is consistent with previous studies reporting no difference in appTb.Th in those with and without osteoporotic fracture [11]. The findings are also consistent with the limited difference in distal femur appTb.Th and no difference in proximal tibia appTb.Th reported in men with spinal cord injury versus men without spinal cord injury [19].

In summary, female collegiate artistic gymnasts were found to have a higher apparent number of trabeculae with a lower apparent separation in the proximal tibia than non-athlete controls matched for age, height, body mass and race. While these observations support the notion that participation in high-load physical activity can enhance the trabecular microarchitecture in weight-bearing bone, randomized controlled trials are needed to substantiate this contention.

Notes

Acknowledgements

We thank the subjects for their participation. The study was funded by the National Institutes of Health (HD40323) and the Center for Research Development in the College of Health Sciences at the University of Delaware.

Conflicts of interest

None.

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Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2007

Authors and Affiliations

  1. 1.Department of Health, Nutrition and Exercise SciencesUniversity of DelawareNewarkUSA
  2. 2.Magnetic Resonance Science Center, Department of RadiologyUniversity of California, San FranciscoSan FranciscoUSA
  3. 3.Department of KinesiologyUniversity of GeorgiaAthensUSA

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