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Osteoporos Int (2001) 12:104–111

ß 2001 International Osteoporosis Foundation and National Osteoporosis Foundation


Osteoporosis
International

Original Article

Effects of Lifetime Volleyball Exercise on Bone Mineral Densities in


Lumbar Spine, Calcaneus and Tibia for Pre-, Peri- and Postmenopausal
Women
M. Ito1, T. Nakamura2, S. Ikeda2, Y. Tahara8, R. Hashmi1, K. Tsurusaki1, M. Uetani1 and K. Hayashi1
1
Department of Radiology, Nagasaki University School of Medicine; 2Department of Orthopedic Surgery, University of
Occupational and Environmental Health, Kitakyushu; and 3Department of Health and Physical Education, Faculty of Education,
Nagasaki University, Nagasaki, Japan

Abstract. To clarify the effects of habitual volleyball players were significantly smaller than those values in
exercise on bone in women during the menopausal the controls. However, the bone loss rates in the lumbar
periods, we measured bone mineral densities (BMDs) of spine did not differ significantly between the groups. The
the lumbar spine, calcaneus and tibia every 12 months bone loss rate in the calcaneus was significantly related
for 2 years and estimated factors related to the baseline to the current number of training hours per week and
values and annual loss rates. Forty Japanese female YSM. The rate of bone loss in the tibia was related to
volleyball players 42–62 years of age, who had belonged BMI. These data indicated that the total number of years
to the district non-professional club for more than 10 participating in exercise activity during adulthood have
years on average, were recruited. Twenty women had positive effects on lumbar and calcaneus BMDs and the
regular menstruation at the start, but 7 underwent cortical structure of the tibia. Habitual volleyball
menopause during the study. Fifty-nine healthy women exercise apparently did not alleviate the menopause-
who did not participate in habitual exercise, but were related bone loss in the lumbar spine.
otherwise comparable with the players, were recruited as
the controls. The lumbar and calcaneus BMDs were Keywords: Age-related bone loss; DXA; Estrogen;
measured by dual-energy X-ray absorptiometry (DXA), Exercise; pQCT
and both the volumetric BMDs and cross-sectional
geometry at the diaphysis of the tibia were measured
by peripheral quantitative computed tomography. The
baseline BMDs of all measured sites and the values of Introduction
the cortical area and moment of inertia of the tibia in the
players were significantly higher than the values in the High peak bone mass attained in young adulthood and a
control women. In the peri- and postmenopausal players, reduction in the rate of bone loss in the postmenopausal
the baseline values of the lumbar and calcaneus BMDs period are considered major factors in preventing
related to total years of participating in regular exercises osteoporosis. Since bone minieral density (BMD) is
during adulthood including volleyball (TYE), body mass positively associated with the degree of physical activity
index (BMI) and years since menopause (YSM). Tibia and body weight [1,2], high-impact exercises are
cortical area and moment of inertia values related to assumed to increase bone mass. Previous reports have
TYE. Annual bone loss rates in the tibia and calcaneus of demonstrated that resistance exercise increases BMDs of
the axial and appendicular skeletons during adolescence
[3,4] and the premenopausal period [5].
Correspondence and offprint requests to: Masako Ito, MD,
Department of Radiology, Nagasaki University School of Medicine, For peri- and postmenopausal women, however, the
1-7-1 Sakamoto, Nagasaki, 852-8501 Japan. Tel: +81 958 49 7354. effect of the resistance exercise for 1–1.5 years seemed
Fax: +81 958 49 7357. to differ depending on the skeletal site and age of the
Effects of Lifetime Volleyball Exercise on BMD 105

subject [6–10]. Endurance exercise including walking, Materials and Methods


jogging and climbing stairs was able to increase the
lumbar spine and femoral neck BMD in postmenopausal Subjects
non-osteoporotic women 60–70 years old [6,7]. In
perimenopausal healthy women aged 52–53 years, a
similar type of endurance exercise maintained BMD of Forty female volleyball players, belonging to a district
the femoral neck but did not affect the lumbar spine and club of the non-professional Japan national women’s
volleyball society, were included in the study. Twenty
calcaneus [8]. In a study of young premenopausal
premenopausal and 20 postmenopausal women were
volleyball players, the osteogenic effects of volleyball
randomly selected from the players. Menopause was
appeared at weight-bearing bone sites as well as the
defined as no menstruation for at least 6 consecutive
dominant arm [9]. In postmenopausal healthy women in months. The premenopausal women had regular
their fifties, jumping exercise with a height of menstrual cycles at the start. Since 7 of 20 premeno-
approximately 10 cm, producing a ground reaction pausal women experienced menopause during the study
force of 4 times body weight, did not affect the period, they were classified at the end into a new group
BMDs of the lumbar spine or femoral neck [10]. described as the perimenopausal group. Thus, there were
Resistance training in the limb with high load increased three groups according to menstrual status: 13 pre-
the BMD of the hip at the trochanter and Ward’s menopausal women with a regular menstrual cycle, 7
triangle, but not at the femoral neck, in 40- to 70-year- perimenopausal women who underwent menopause
old women [11]. These data suggest that the effects of during the study period, and 20 postmenopausal women.
the loading exercise differ depending on the bones Fifty-nine healthy women who did not participate in
involved [8–11]. habitual exercise were selected for the controls. They
Volleyball is a ground-reaction force exercise with were all residents of the same district, not participating
high strain rates and peak stresses on the skeleton. In in any kind of regular or organized sports activity in the
Japan, the non-professional national women’s volleyball present or past during adulthood. Controls consisted of
society was established to promote women’s health with 24 premenopausal and 35 postmenopausal women at the
the support of the Ministry of Education, organizing start. Eleven of the 24 premenopausal women experi-
women’s volleyball clubs in various districts. Members enced menopause during the study period, and they were
of the clubs participate regularly in training. The purpose classified into the perimenopausal group at the end.
of this study was to clarify the site-specific effects of There were thus three control groups: 13 premenopausal
habitual volleyball practice on bone mass and geometry women with a regular menstrual cycle, 11 perimeno-
in women during the menopausal periods. We long- pausal women and 35 postmenopausal women.
itudinally measured their BMDs and geometry of the Demographics of the subjects and the controls,
lumbar spine, tibia and calcaneus for 2 years. Then, including age at the start of the study, age at menopause,
factors related to the baseline values and annual loss years since menopause (YSM), body weight (BW, kg),
rates were analyzed. Results were compared with those body height (BH, cm) and body mass index (BMI = BW/
in control women who had not participated in habitual BH2, kg/cm2), are presented in Table 1. Since there was
exercise. no significant difference in these parameters between the
Table 1. Demographics of the volleyball players and the controls

Volleyball players Controls

Pre. Peri. Post. Pre. Peri. Post.

No. of subjects 13 7 20 13 11 35
Age (years) 43.4+0.7 50.3+1.5 54.4+1.2 40.1+1.6 49.1+0.7 56.3+0.7
(42–49 years) (51–54) (46–62) (33–48) (47–54) (45–62)
Age at menopause (years) – 50.4+0.8 47.1+1.0 – 49.3+0.8 50.2+0.5
YSM (years) – – 5.3+0.8 – – 6.1+0.6
BW (kg) 61.1+2.5 55.7+1.7 57.2+1.3 55.2+1.9 54.6+1.4 53.7+1.2
BH (cm) 157.6+2.1 157.0+1.1 156.5+1.1 158.0+1.1 156.0+1.4 154.0+0.8
BMI (kg/cm2) 0.24+0.01 0.24+0.01 0.23+0.01 0.22+0.01 0.23+0.01 0.22+0.01
TYP (years) 11.5+1.6 19.0+1.6* 19.8+1.8*
(6–29 years) (10–30) (7–30)
TYE (years) 17.1+2.3 25.4+2.7* 25.0+2.2*
(10–35 years) (16–36) (9–35)
Current training hours per week 4.4+0.3 3.2+0.1 3.5+0.4

Values are the mean and the standard error of the mean (SEM).
Pre., premenopausal women; Peri., perimenopausal women; Post., postmenopausal women; YSM, years since menopause; BW, body weight; BH,
body height; BMI, body mass index; TYP, total years of participation in volleyball; TYE, total years of participation in regular exercise including
periods of past activity and volleyball club participation.
*.Significant difference (p<0.05) versus premenopausal players by Student’s t-test.
106 M. Ito et al.

players and control women of either menstrual status, Annual Rates of Bone Loss
comparative analyses between the subjects and controls
appeared to be justified. Linear regression analyses were performed to obtain
Regular menstrual cycles were confirmed in the annual rates of bone loss (%/year) on the BMD values at
premenopausal women by questionnaire. The average the measured sites for each subject. For each site, the
daily intake of milk and dairy products did not differ measured values at the start and at the first and second
significantly in each menstrual group between the player 12-month periods were used to calculate the slope of the
and control groups. Women who were taking or had regression line. The slope value was then divided by the
taken estrogen or other drugs that influence bone value at the start and multiplied by 100, estimating
metabolism were excluded. Women with a history of changes in the percent values per year (%/year) [15–18].
previous fracture were not included. Informed consent
for the study was obtained from each subject. Years
during which the players participated to the volleyball
club before the start of the study, total years of Factors Related to the Baseline Values of BMDs and
participating in regular exercise including past activity Cortical Geometry of the Tibia in Premenopausal and
and volleyball, and current number of training hours per Menopausal Women
week (52 week/year) are presented in Table 1.
In the players, the total years of participation in regular
exercise including past periods of activity and playing
volleyball (TYE), current weekly training hours for
Bone Density and Size Measurements volleyball, YSM and BMI were selected for analyses. In
the controls, YSM and BMI were selected. Menopausal
Measurements of bone density and size were performed women included both peri- and postmenopausal women.
three times at intervals of 12 months between 1996 and Their relationships with the values of the initial BMDs,
1998. Dual-energy X-ray absorptiometry (DXA) of the cortical area and the moment of inertia of the tibia were
lumbar spine and calcaneus and peripheral quantitative estimated by multiple regression analyses in the
computed tomography (pQCT: Densiscan 1000, Scanco premenopausal players.
Medical, Zurich, Switzerland) of the tibia were
performed.
Factors Related to Annual Rates of Bone Loss in the
DXA Measurement of the Lumbar Spine and Calcaneus. Menopausal Women
BMD (g/cm2) values and projection area (cm2) of the
lumbar spine (L2–L4) in anteroposterior (AP) projection In the players, TYE, current weekly training hours for
were determined using DXA (EXP 5000, Lunar, volleyball, the baseline value of bone measurements,
Madison, WI). The lateral side projection area (cm2) BMI and YSM were used to estimate the relationship
and BMD (g/cm2) values of the right calcaneus were with the annual rates of loss of the measured bone mass
measured using DXA (HeelScan DX-2000, KDK, by multiple regression analyses in the peri- and
Kyoto, Japan) [12]. Coefficient of variation (CV) postmenopausal players. In the controls, the baseline
values of the BMD measurements for the lumbar spine values of bone measurements, BMI and YSM were
and calcaneus were 1.1% and 0.8%, respectively. examined in relation to the annual loss rates. Menopau-
sal women included both peri- and postmenopausal
Peripheral QCT of the Tibia. Six consecutive slices of women for these analyses.
tomographic measurements were obtained from the mid-
diaphysis. Each measurement included an area of 1 mm
thickness with 1.5 mm intervals [13,14]. Total volu-
metric BMD values were obtained from BMD values for Statistics
the total cross-sectional area. The cross-sectional cortical
area was obtained by subtracting the medullary cavity Data were expressed as the mean and standard error of
area from the total cross-sectional area. The cross- the mean (SEM). Statistical analyses were performed
sectional moment of inertia (MI) was calculated using the StatView version 4.51.2 statistical package.
according to the following equation: MI = Sai(yi 7 Linear regression analyses were used to obtain the
ye)2, where ai is the voxel area and (yi 7 ye) is the annual rates of bone loss (%/year). Differences in
distance in the vertical direction from each voxel to the baseline BMDs, geometric parameters and annual rates
horizontal axis passing through the center of the area. of bone loss between the players and controls were
Summation was performed over the voxels that were compared by Student’s t-test for each menstrual group,
defined as cortical bone by the attenuation threshold. Multiple regression analyses were used to obtain
These parameter values were calculated on a pQCT regression coefficients, t values and the significance
high-resolution image of the diaphysis of the tibia with level, to determine significant factors affecting the
an attenuation threshold value of 120 using the NIH baseline BMDs, geometry and annual rates of bone
image analysis system (version 1.61). loss. The significance level was set at less than 0.05.
Effects of Lifetime Volleyball Exercise on BMD 107

Results between the players and controls in either menstrual


group. In the premenstrual group, the respective values
Baseline Values of Bone Density and Geometry for the players and control women were 70.05 and
0.94 (Table 4). The values were 2.74 and 2.87 in the
Baseline BMD values of the lumbar spine, calcaneus and perimenopausal group, and 2.29 and 2.75 in the
tibia in the player groups were higher than the respective postmenopausal group.
values in the control groups (Table 2). The values of the In the calcaneus and tibia, however, the bone loss
lumbar area or calcaneus area in DXA measurements did rates for players were significantly smaller than the
not differ between the players and controls (Table 3). In
values for the controls in all menstrual groups. In the
the tibia, the total cross-sectional area or medullary
cavity area did not differ significantly either. However, calcaneus, the respective values for the players and
the values of the tibia cortical area and cross-sectional controls were 70.04 and 0.93 (p50.05) in the
moment of inertia in the players were significantly premenopausal group. They were 0.83 and 1.97
higher than the values in the controls. (p50.05) in the perimenopausal group, and 0.62 and
2.29 (p50.0001) in the postmenopausal group. In the
tibia, the respective values for the players and controls
Annual Loss rates for the Densities of the Lumbar were 70.45 and 1.16 (p50.0001) in the premenopausal
Spine, Calcaneus and Tibia group, 1.49 and 2.85 in the perimenopausal group
Mean percentage values of the annual loss rates in the (p50.05) and 1.10 and 2.24 (p50.005) in the
lumbar spine BMDs, did not differ significantly postmenopausal group.

Table 2. Baseliine BMD values of lumbar spine, calcaneus and tibial diaphysis of the volleyball players and the controls

n Lumbar spine BMD Calcaneus BMD Tibial diaphyseal BMD


(g/cm2) (g/cm2) (pQCT) (mg/cm3)

Volleyball players
Pre. 13 1.330+0.042 0.920+0.020 1096.8+26.2
Peri. 7 1.311+0.046 0.901+0.024 1118.9+37.2
Post. 20 1.253+0.048 0.858+0.016 1051.0+30.6
Controls
Pre. 13 1.202+0.037 0.846+0.023 976.2+42.1
Peri. 11 1.121+0.084 0.791+0.021 1023.8+21.6
Post. 35 0.950+0.022 0.740+0.014 939.7+24.6
Comparisona
Pre. 0.05 0.05 0.05
Peri. 0.05 0.005 0.05
Post. 0.0001 0.0001 0.01

Values are the mean and the standard error of the mean (SEM) with significant difference by Student’s t-test.
Pre., premenopausal women; Peri., perimenopausal women; Post., postmenopausal women.
a
.Data of comparison: values for the significance by Student’s t-test, compared the values of the players and controls of the same menstrual status.

Table 3. Baseline values of bone geometries in the volleyball players and the controls

n Spinal area Calcaneal area Tibial cross- Tibial medullary Tibial cortical Moment of inertia
sectional area cavity area area

Volleyball player
Pre. 13 43.0+3.4 11.04+0.48 7942+246 3578+220 4363+109 0.854+0.143
Peri. 7 42.5+2.1 10.18+1.59 7728+327 3762+319 3966+94 0.789+0.162
Post. 20 40.7+7.5 11.24+0.37 7390+264 3374+211 4016+88 0.730+0.027
Controls
Pre. 13 43.0+2.9 10.74+0.36 7489+244 3913+207 3577+96 0.702+0.120
Peri. 11 42.3+4.6 10.38+0.51 6828+230 3358+609 3470+85 0.592+0.039
Post. 35 41.7+5.6 10.58+0.27 7009+157 3786+149 3223+78 0.606+0.021
Comparisona
Pre. ns ns ns ns 0.0001 0.01
Peri. ns ns ns ns 0.005 0.05
Post. ns ns ns ns 0.0001 0.001

Values are the mean and the standard error of the mean (SEM) with significant difference by Student’s t-test.
Pre., premenopausal women; Peri., perimenopausal women; Post., postmenopausal women.
a
.Data of comparison: values for the significance by Student’s t-test, compared the values of the players and controls of the same menstrual status.
108 M. Ito et al.

Table 4. Annual rates of bone loss of the volleyball players and the controls

n Lumbar spine BMD Calcaneus BMD Tibial diaphyseal BMD


(g/cm2) (g/cm2) (pQCT) (%/year)
(mg/cm3)

Volleyball players
Pre. 13 70.05+0.51 70.04+0.31 70.45+0.13
Peri. 7 72.74+0.88 70.83+0.54 71.49+0.67
Post. 20 72.29+0.34 70.62+0.26 71.10+0.18
Controls
Pre. 13 70.94+0.31 70.93+0.34 71.16+0.27
Peri. 11 72.87+0.98 71.97+0.16 72.85+0.26
Post. 35 72.75+0.57 72.29+0.27 72.24+0.26
Comparisona
Pre. 7ns 70.05 70.0001
Peri. 7ns 70.05 70.05
Post. 7ns 70.0001 70.005

Values are the mean and the standard error of the mean (SEM) with significant difference by Student’s t-test.
Pre., premenopausal women; Peri., perimenopausal women; Post., postmenopausal women.
a
.Data of comparison: values for the significance by Student’s t-test, compared the values of the players and controls of the same menstrual status.

Factors Related to the Baseline BMDs and Geometry cortical area and moment of inertia values were
Values in the Players and Control Women of related to TYE. The cortical area was also related to
Premenopausal and Menopausal Status BMI,
In premenopausal control women, there was no
In premenopausal players, only tibial cortical area significant relation among these parameters. In meno-
was significantly related to BMI (t value 2.763, r = pausal controls, BMDs of the lumbar spine and tibia and
0.71, p50.05). In menopausal players, however, the the tibial cortical area were significantly related to YSM
baseline values of the lumbar and calcaneus BMDs (Table 6). Calcaneus BMD and the values of the tibia
were related to TYE, BMI, and YSM (Table 5). Tibia cortical area and moment of inertia were significantly
BMD values were related to BMI and YSM. Tibia related to BMI.

Table 5. Factors related to baseline values of BMDs and geometry in the menopausal volleyball players

Dependent variables Independent variables Coefficient t value p r

Lumbar spine BMD TYE (years) 7 0.01+0.01 73.285 0.005 0.71


Current training (h/week) 7 0.02+0.02 70.630 ns
BMI (kg/cm2) 7 3.18+1.21 72.626 0.05
YSM (years) 70.04+0.01 73.463 0.005
Calcaneus BMD TYE (years) 7 0.01+0.01 72.060 0.05 0.72
Current training (h/week) 7 0.01+0.01 70.157 ns
BMI (kg/cm2) 7 1.40+0.43 73.252 0.005
YSM (years) 70.01+0.01 73.975 0.001
Tibial diaphyseal TYE (years) 7 1.40+2.85 70.492 ns 0.50
BMD (pQCT) Current training (h/week) 7 3.29+16.80 70.196 ns
BMI (kg/cm2) 1883.4+883.5 72.132 0.05
YSM (years) 716.27+7.46 72.181 0.05
Tibial cortical area TYE (years) 714.79+8.11 72.123 0.05 0.49
Current training (h/week) 7 8.64+47.9 70.180 ns
BMI (kg/cm2) 4790.4+251.8 72.202 0.05
YSM (years) 712.25+21.27 70.576 ns
Moment of inertia TYE (years) 70.01+0.01 71.945 0.05 0.42
Current training (h/week) 70.02+0.02 70.888 ns
BMI (kg/cm2) 70.57+0.99 70.572 ns
YSM (years) 70.01+0.01 70.206 ns

Multiple regression analyses were performed with BMD or geometrical parameters as the dependent variables, and TYE, current training (h/
week), BMI and YSM as the independent variables.
Coefficient, the mean and the standard error of the mean (SEM) for multiple regression analyses; p, values for the significant level; r, regression
coefficients, TYE, the total years of exercise, BMI, body mass iindex; YSM, years since menopause.
Effects of Lifetime Volleyball Exercise on BMD 109

Table 6. Factors related to baseline values of BMDs and geometry in the menopausal controls

Dependent variables Independent variables Coefficient t value p r

Lumbar spine BMD BMI (kg/cm2) 7 1.77+0.91 71.939 ns 0.43


YSM (years) 70.02+0.01 72.298 0.05
Calcaneus BMD BMI (kg/cm2) 7 1.60+0.55 72.926 0.01 0.47
YSM (years) 70.01+0.01 71.426 ns
Tibial diaphyseal BMI (kg/cm2) 825.5+1022.17 70.808 ns 0.42
BMD (pQCT) YSM (years) 718.45+7.14 72.585 0.05
Tibial cortical area TBMI (kg/cm2) 6952.5+3198.2 72.174 0.05 0.43
YSM (years) 747.81+22.33 72.141 0.05
Moment of inertia BMI (kg/cm2) 72.56+0.84 73.031 0.005 0.48
YSM (years) 70.01+0.01 70.901 ns

Multiple regression analyses were performed with BMD or geometrical parameters as the dependent variable and TYE, current training (h/week),
BMI and YSM as the independent variables.
Coefficient, the mean and the standard error of the mean (SEM) for multiple regression analyses; p, values for the significant level; r, regression
coefficients, BMI, body mass iindex; YSM, years since menopause.

Table 7. Factors related to the annual rates of bone loss of the lumbar spine, calcaneus and tibial diaphysis in the menopausal volleyball players

Dependent variables Independent variables Coefficient t value p r

Calcaneus BMD TYE (years) 7 0.05+0.03 71.612 ns 0.64


Current training (h/week) 72.08+0.10 71.886 0.05
BMI (kg/cm2) 710.39+10.21 71.018 ns
YSM (years) 70.20+0.09 72.143 0.05
Baseline BMD of calcaneus 72.87+4.15 70.693 ns
(g/cm2)
Tibial diaphyseal TYE (years) 7 0.01+0.03 70.330 ns 0.47
BMD (pQCT) Current training (h/week) 7 0.06+0.15 70.371 ns
BMI (kg/cm2) 716.63+8.87 71.875 0.05
YSM (years) 70.03+0.08 70.300 ns
Baseline BMD of tibial 70.01+0.01 70.375 ns
diaphyseal BMD (mg/cm3)

Multiple regression analyses were performed with BMD or geometrical parameters as the dependent variables, and TYE, current training (h/
week), BMI, YSM and BMD at the initial measurement as the independent variables.
Coefficient, the mean and the standard error of the mean (SEM) for multiple regression analyses; p, values for the significant level; r, regression
coefficients, TYE, the total years of exercise, BMI, body mass iindex; YSM, years since menopause.

Factors Related to the Annual Bone Loss Rates in the in the annual rates of bone loss in the calcaneus and tibia
Menopausal Players and Control Women were significantly alleviated, but the effect was not
significant in the lumbar spine.
In the players, the rates of bone loss in the lumbar spine The baseline BMD values of the measured sites were
did not significantly relate to any of the factors apparently associated with BMI in the menopausal
examined. The rate of bone loss in the calcaneus BMD women. In the players, the lumbar spine, calcaneus and
was significantly related to the current number of tibia BMDs were related to BMI. It has been well
training hours per week and YSM (Table 7). Values of recognized that lumbar BMD is associated with BMI in
tibia BMD were related to BMI. The annual loss rates women before and after menopause [12,16,19,20]. We
did not significantly relate to baseline BMD values in previously observed that BMI was related to lumbar
either measurement site. In the control women, none of BMDs in a study of 67 menopausal women without
the factors was related to bone loss rate at any site. habitual exercise [11]. Thus, BMI seems to be a
determinant factor of lumbar spine, tibia and calcaneus
BMD in women participating in exercise as well as in
Discussion women without habitual exercise. However, since only
calcaneus BMD was related to BMI in the control
This study has demonstrated that female habitual women in this study, the association could be stronger in
volleyball players participating in sports activity for 20 the players than in control women. Though part of this
years on average obtained higher bone mass in the association may be related to the influence of BMI on
lumbar spine, calcaneus and tibia than women who did peak bone mass, the effect of BMI on bone mass seems
not participate in habitual exercise during adulthood. In to dominate even after menopause on BMDs in the trunk
the volleyball players, the menopause-related increases and lower extremities. The values of tibia cortical area
110 M. Ito et al.

were also related in the players and controls. Thus, it is 11]. These reported data along with ours suggest that
expected that the cortical bone architecture also depends impact loading by habitual volleyball exercise specifi-
on BMI in menopausal women. The values of lumbar cally counteracts bone loss in the calcaneus and tibia but
spine, calcaneus and tibia BMDs were negatively does not compensate for the estrogen-dependent bone
associated with YSM in the players, as often reported loss that is dominant in the lumbar spine.
in postmenopausal women [21–23]. This study has two limitations regarding extrapolating
The positive effects of the total years of participation the results to postmenopausal women with osteoporosis:
in exercise (TYE) were obvious on the baseline values of one is the selection of subjects with bone mass higher
lumbar spine and calcaneus BMDs in the players. The than the level of osteoporosis and the other is the lack of
data support the hypothesis that habitual exercise during hip BMD data. In this study we selected the lumbar spine
adulthood is effective in obtaining higher bone mass in and calcaneus as sites with predominantly trabecular
the lumbar spine and calcaneus. In the tibia, while the t bone and the diaphysis of the tibia as a site with
value for BMD was not significant, the values of the predominantly cortical bone. Since the proximal femur is
cortical area and the moment of inertia were significantly assumed to contain approximately similar amounts of
related to TYE, thus indicating that the diaphysis of the trabecular and corticla bone in normal subjects [26], we
tibia responded to exercise by improving the cross- did not measure hip BMD. However, hip BMD has been
sectional cortical structure during adulthood. Since the known to be a good predictor of fragility fracture [27].
total cross-sectional areas were similar in the players and Further, it may be expected that the loading pattern of
control women, the periosteal surface is apparently less the skeleton differs markedly between healthy bone and
sensitive to exercise than the endosteal surface in our osteoporotic bone whose microarchitecture has deterio-
subjects. Since TYE and BMI were both significantly rated [28]. Therefore, this study does not necessarily
related to BMDs of the lumbar spine and calcaneus and underscore the effect of impact exercise in the
the parameters of the geometry of tibia as well, history of prevention of fragility fracture in osteoporosis. To
the exercise activity and BMI seem to affect these bone resolve that question, a different study design is
parameters independently. necessary.
In women without habitual exercise, postmenopausal In conclusion, this study indicated that the total years
bone loss rates increased in both the lumbar spine of participating in exercise activity including volleyball
(11,15,22–24] and calcaneus [11,25], as has often been during adulthood have a positive effect on the bone mass
observed. Increases in the bone loss rate for the of the lumbar spine and calcaneus and on tibia cortical
diaphysis of tibia by pQCT measurements were also structure. Habitual volleyball exercise was apparently
confirmed in a previous report [11]. However, the annual effective in alleviating menopause-related bone loss in
loss rates of lumbar BMD in the peri- and postmeno- the tibia and calcaneus, but not in the lumbar spine. The
pausal control women in our study were larger than the effect on the tibia was BMI-dependent in the players.
values previously reported for Japanese women [11,22].
In our previous study, the annual loss rates of the lumbar Acknowledgement. This study was supported by a Grant-in-Aid for
BMD were 2.59%/year on average of perimenopausal Scientific Research from the Ministry of Education in Japan.
women and 1.88%/year for early postmenopausal
women [11]. The rates of bone loss in lumbar BMD
determined by a nationwide study in Japan were 1.91%/
year for perimenopausal women and 0.99%/year for References
postmenopausal women [22]. The rates in Caucasian
women were 2.35%/year and 1.24%/year for peri- and 1. Pocock N, Eisman J, Gwinn T, et al. Muscle strength, physical
postmenopausal women, respectively [15]. Since the fitness, and weight but not age predict femoral neck bone mass. J
annual bone loss rates of the calcaneus and tibia in the Bone Miner Res 1989;4:441–8.
2. Bevier WC, Wiswell RA, Pyka GA, Kozak KC, Newhall KM,
controls were similar to the level in our previous report Marcus R. Relationship of body composition, muscle strength,
and those of others [11,22], the controls in this study and aeroboic capacity to bne mineral density in older men and
may represent the loss rates in the lumbar spine of fast women. J Bone Miner Res 1989;4:515–22.
bone losers. Baseline values for the lumbar BMD in 3. Snow-Harter C, Bouzsein ML, Lewis BT, Carter DR, Marcus R.
Effects of resistance and endurance exercise on bone mineral
control women were above the level of osteoporosis in status of young men: a randomized exercise intervention trial. J
this study. However, multiple regression analyses did not Bone Miner Res 1992;7:761–9.
indicate any relationship with factors including baseline 4. Bass S, Peace G, Bradney M, et al. Exercise before puberty may
BMD values. Thus, the annual loss rates do not seem to confer residual benefits in bone density in adulthood: studies in
depend on the baseline BMD values in these women. active prepubertal and retired female gymnasts. J Bone Miner Res
1998;13:500–7.
In the habitual volleyball players, the alleviation of 5. Lohman T, Going S, Pamenter R, et al. Effect of resistance
menopause-related bone loss was apparent in the BMDs training on regional and total bone mineral density in
of the calcaneus and tibia when compared with women premenopausal women: a randomized prospective study. J Bone
without habitual exercise. Reportedly, resistance ex- Miner Res 1995;10:1015–24.
6. Kohrt WM, Snead DB, Slatopolosky E, Birge SJ. Additive effects
ercise including jumping and jogging was not able to of weight-bearing exercise and estrogen on bone mineral density
reduce lumbar bone loss in postmenopausal women in older women. J Bone Miner Res 1995;10:1303–11.
whose bone mass was above the osteoporotic level [8– 7. Kohrt WM,Ehsani AA, Birge SJ. Effects of exercise involving
Effects of Lifetime Volleyball Exercise on BMD 111

predominantly either joint-reaction or ground-reaction forces on 18. Riggs BL, Wahner HW, Melton LJ III, Richelson LS, Judd HL,
bone mineral density in older women. J Bone Miner Res Offord KP. Rates of bone loss in the appendicular and axial
1997;12:1253–61. skeletons of women. J Clin Invest 1986;77:1487–91.
8. Heinonen A, Oja P, Sievanen H, Pasanen M, Vuori I. Effect of 19. Ortolani S, Trevisan C, Bianchi ML, Gandolini G, Cherubini R,
two training regimens on bone mineral density in healthy Polli EE. Influence of body parameters on female peak bone mass
perimenopausal women: a randomized controlled trial. J Bone and bone loss. Osteoporos Int 1993;(Suppl 1):S61–66.
Miner Res 1998;13:483–90. 20. Harris S, Dallal GE, Dawson-Hughes B. Influence of body weight
9. Alfredson H, Nordstrom P, Lorentzen R. Bone mass in female in rates of change in bone density of the spine, hip, and radius in
volleyball players: a comparison of total and regional bone mass postmenopausal women. Calcif Tissue Int 1992;50:19–23.
in female volleyball players and nonactive females. Calcif Tissue 21. Ashizawa N, Nonaka K, Michikami S, et al. Tomographical
Int 1997;60:338–42. description of tennis-loaded radius: reciprocal relation between
10. Bassey EJ, Rothwell MC, Littlewood JJ, Pye DW. Pre- and post- bone size and volumetric BMD. J Appl Physiol 1999;86:1347–51.
menopausal women have different bone mineral density 22. Fujiwara S, Fukunaga M, Nakamura T, et al. Rates of changes in
responses to the same high-impact exercise. J Bone Miner Res spinal bone density among Japanese women. Calcif Tissue Int
1998;13:1805–13. 1998;63:202–7.
11. Kerr D, Morton A, Dick I, Prince R. Exercise effects on bone 23. Luckey MM, Wallenstein S, Lapinski R, Meier DE. A
mass in postmenopausal women are site-specific and load- prospective study of bone loss in African-American and white
dependent. J Bone Miner Res 1996;11:218–25. women – a clinical research center study. J Clin Endocrinol
12. Ito M, Nakamura T, Tsurusaki K, Uetani M, Hayashi K. Effects Metab 1996;81:2948–56.
of menopause on age-dependent bone loss in axial and 24. Pouilles JM, Tremollières F, Ribot C. Effect of menopause on
appendicular skeletons in healthy japanese women. Osteoporos femoral and vertebral bone loss. J Bone Miner Res
Int 1999;10:377–87. 1995;10:1531–6.
13. Ito M, Tsurusaki K, Hayashi K. Peripheral QCT for the diagnosis 25. Ensrud KE, Palermo L, Black DM, et al. Hip and calcaneal bone
of osteoporosis. Osteoporos Int 1997;7(Suppl 3):S120–7. loss increase with advancing age: longitudinal results from the
14. Rugsegger P. The use of peripheral QCT in the evaluation of bone study of osteoporotic fractures. J Bone Miner Res 1995;10:1778–
remodeling. Endocrinologist 1994;4:167–76. 87.
15. Pouilles JM, Tremollières R, Riot C. The effects of menopause on 26. Kuiper JW, Kuijk CV, Grashuis JL. Distribution of trabecular and
longitudinal bone loss from the spine. Calcif Tissue Int cortical bone related to geometry. A quantitative computed
1993;52:340–3. tomography study of the femoral neck. Invest Radiol 1997;32:83–
16. Tremollières FA, Pouikkes J, Ribot C. Vertebral postmenopausal 9.
bone loss is reduced in overweight women: a longitudinal study in 27. De Laet CEDH, Van Hout BA, Burger H, Weel AEAM, Hofman
155 early postmenopausal women. J Clin Endocrinol Metab A, Pols HAP. Hip fracture prediction in elderly men and women:
1993;77:683–6. validation in the Rotterdam study. J Bone Miner Res
17. Riis BJ, Hansen MA, Jensen AM, Overgaard JK, Christiansen C. 1998;13:1587–93.
Low bone mass and fast rate of bone loss at menopause: equal 28. Hayes WC, Myers ER, Robinovitch SN, Kroonenberg AVD,
risk factors for future fracture. A 15-year follow-up study. Bone Courtney AC, McMahon TA. Etiology and prevention of age-
1996;19:9–12. related hip fractures. Bone 1996;18:S77–86.

Received for publication 3 September 1999


Accepted in revised form 10 July 2000