Full text of DOI:10.1359/jbmr.2001.16.1.166

JOURNAL OF BONE AND MINERAL RESEARCH
Volume 16, Number 1, 2001
© 2001 American Society for Bone and Mineral Research
Effects of Tower Climbing Exercise on Bone Mass,
Strength, and Turnover in Growing Rats
TAKUYA NOTOMI,1 NOBUKAZU OKIMOTO,2 YUICHI OKAZAKI,2 YURI TANAKA,1
TOSHITAKA NAKAMURA,2 and MASASHIGE SUZUKI1
ABSTRACT
To determine the effects of tower climbing exercise on mass, strength, and local turnover of bone, 50
Sprague–Dawley rats, 10 weeks of age, were assigned to five groups: a baseline control and two groups of
sedentary and exercise rats. Rats voluntarily climbed the 200-cm tower to drink water from the bottle set at
the top of it. In 4 weeks, the trabecular bone formation rate (BFR/bone surface [BS]), bone volume (BV/TV),
and trabecular thickness (Tb.Th) of both the lumbar vertebra and tibia and the bone mineral density (BMD)
of the tibia increased, while the osteoclast surface (Oc.S) decreased. The parameter values in the midfemur,
such as the total cross-sectional area, the moment of inertia, the periosteal mineralizing surface (MS/BS),
mineral apposition rate (MAR), BFR/BS, and bending load increased, while the endosteal MAR decreased. In
8 weeks, the increases in the bone mineral content (BMC), BMD of the femur and tibia, and the bending load
values of the femur were significant, but the climbing exercise did not increase BMC, BMD, or the compres-
sion load of the lumbar vertebra. Although the periosteal MS/BS, MAR, and BFR/BS increased, the endosteal
MS/BS, MAR, and BFR/BS decreased. These results show that climbing exercise has a beneficial effect on the
femoral cortex and tibia trabecular, rather than the vertebral trabecular. In the midfemur, effects on bone
formation are site specific, supporting accelerated cortical drift by mechanical stimulation. (J Bone Miner Res
2001;16:166–174)
Key words: climbing, voluntarily exercise, bone formation, osteoclast, cortical drift
In rodent studies, aerobic exercises, including running
and swimming on a nonvoluntary basis, were applied
to study the effects of exercise on bone morphology
and metabolism(8–11) but rarely was resistance training
applied.(12–14) These studies examined the effects of resis-
tance exercise induced by electric stimulation on the floor of
a metal cage and found an increase in the femoral cortical
bone strength(12) and trabecular bone mass of the proximal
INTRODUCTION
WIDELY accepted rationale for the positive effects of
exercise on bone is that mechanical strain plays an
important role in the maintenance of bone mass and
strength,(1,2) and a variety of exercise interventions have
been successful in increasing bone mineral density
(BMD).(3,4) Cross-sectional data in a human study sug-
A
gested that resistance-trained athletes have greater bone tibia.(13) The effects of resistance exercise on local bone
mass than endurance-trained athletes or sedentary control turnover and mechanical properties of bone have yet to be
subjects.(5–7) However, the mechanisms by which exercise studied in detail.(12,13) The rat training models do not seem
leads to changes in bone metabolism and morphology are to exclude the effects from electrical stimulus and/or a
not fully understood.
nonvoluntary training regimen.(8–14)
1Laboratory and Biochemistry of Exercise and Nutrition, Institute of Health and Sport Sciences, University of Tsukuba, Tsukuba,
Japan.
2Department of Orthopedic Surgery, University of Occupational and Environmental Health, Kitakyushu, Japan.
166

EFFECTS OF TOWER CLIMBING EXERCISE ON BONE IN GROWING RATS
167
We modified the resistance exercise models, such as the
rat climbing reported by Yarasheski et al.(15) and Duncan et
al.,(16) who estimated skeletal muscle. In our model, rats
voluntarily climbed the 200-cm tower to drink water from a
bottle set at the top of it. The purpose of this study was to
find out the effects of voluntary resistance exercise on the
mass, strength, and local turnover of bone in growing rats.
MATERIALS AND METHODS
Animals
Male Sprague–Dawley rats were purchased from Japan
FIG. 1. Diagram illustrating the resistance exercise appa-
ratus.
CLEA, Inc. (Tokyo, Japan) and were acclimatized for 1
week under standard laboratory conditions (22 Ϯ 2°C, 60%
humidity). The light/dark cycle was 12 h with lights on from
6:00 a.m. to 6:00 p.m. All rats were housed in metal cages.
Drinking water was available at all times. The amount of
food taken was equalized among the groups. All rats were
fed commercial rat chow (Japan CLEA; calcium, 1200
mg/100 g; phosphorus, 1080 mg/100 g). The body weight of
the rats was measured weekly. All rats remained healthy.
The protocol was approved by The University of Tsukuba’s
Institutional Animal Care and Use Committee.
third, fourth, and fifth lumbar vertebra (L3, L4, and L5) and
bilateral tibias and femora were harvested. The L3, L4, right
femur (RF), and bilateral tibias were fixed immediately with
4% paraformaldehyde in a 0.1 M phosphate buffer contain-
ing 2% sucrose and stored at 4°C. L5 and the left femur (LF)
were stored at Ϫ80°C until the mechanical tests. Bone
labeling of rats with a subcutaneous injection of calcein (8
mg/kg body weight) was performed 7 days and 3 days
before death.
Fifty rats, 10 weeks of age, were randomized by body
weight to five groups. Group C was the baseline control,
killed at the start. Groups 4S and 4E were the sedentary and
the exercise groups, respectively, killed after 4 weeks of the
experiment. Groups 8S and 8E were killed after 8 weeks.
Mean body weight at 10 weeks of age in groups C, 4S, 4E,
8S, and 8E was 249 Ϯ 7 g, 250 Ϯ 3 g, 252 Ϯ 3 g, 256 Ϯ
4 g, and 255 Ϯ 3 g, respectively. No significant differences
were found among these values (Tukey’s honestly signifi-
cant difference after one-way analysis of variance
[ANOVA]). In the preliminary experiment, 20 male
Sprague–Dawley rats, 10 weeks of age, were assigned ran-
domly to the sedentary and exercise groups by body weight.
At 4 weeks, body weight in the sedentary and exercise
groups was 340 Ϯ 3 g and 337 Ϯ 4 g, respectively, and food
intake during the 4 weeks was 972 Ϯ 24 g and 964 Ϯ 31 g,
respectively. No significant differences in body weight and
food intake values between the sedentary and exercise
groups were found (Student’s t-test after ƒ test). To avoid
any difference in food intake, the sedentary and exercise
groups were given the same amount of food, using the same
methods of feeding as in our previous reports.(17,18) We
measured the minimum amount of food consumed by the
groups, and the amount of food was then reduced to the
minimum amount on the next day. If the food was con-
sumed completely, the amount of food was increased by
4–6 g/day. Therefore, at 4 weeks and 8 weeks, the amount
of food consumed by the sedentary and exercise groups was
equal.
Resistance exercise
The groups of exercise rats were housed in metal cages
with a wire meshed tower with two water bottles set at the
top (Fig. 1). At the beginning, the bottles were set at a height
of 20 cm. The set point of the drink bottles was elevated
gradually to 200 cm over a week. The rats were monitored
for 24 h/day every 2 weeks during the experimental period,
using a charge-coupled device (CCD) camera (CCD-
TRV95; Sony, Tokyo, Japan). The daily distances and times
of climbing activity were obtained from the monitoring
records.
Bone mineral measurement
BMD (mg/cm2) and bone mineral content (BMC; mg)
were measured on the LF and right tibia (RT) using dual-
energy X-ray absorptiometry (DXA; DCS-3000; Aloka, To-
kyo, Japan). The L5 body was prepared by removing the
posterior segment and bone mineral measurements were
performed. The mineralization profiles of the specimens
were stored with the monitoring images, and the BMD and
BMC values for the lumbar body, the femur mid-diaphyseal
region (12 mm in length), and the tibia proximal region (12
mm in length) were obtained.
At the end of the experiments, rats were killed by exsan-
guination under ether anesthesia. Soon after the death, the
hindlimb muscles (gastrocnemius, plantaris, soleus, tibia,
and extensor digitorum longus) and abdominal fats (epididy-
Mechanical testing
Femur: A three-point bending test was performed as
mal fat, perigastric fat, mesenteric fat, and abdominal sub- previously described(19,20) using a load tester (Tensilon
cutaneous fat) were isolated. The combined weight of the UTA-1T; Orientec, Tokyo, Japan). The LF specimen was
hindlimb muscles and abdominal fats was measured. The placed on a holding device with supports located at a

168
NOTOMI ET AL.
distance of 12 mm, with the lesser trochanter proximal to and LT, the osteoclast surface (Oc.S; ␮m) and trabecular BS
and in contact with the proximal transverse bar. The mid- (␮m) were measured.(22–24) TRAP-positive cells that
point served as the anterior (upper) loading point. A bending formed resorption lacunae at the surface of the trabeculae
force was applied by the crosshead at a speed of 10 mm/ and contained one or more nuclei were identified as os-
minute until fracture occurred. The maximum load (N) and teoclasts.(25)
structural stiffness (N/mm) were obtained directly from the
load-deformation curves that were recorded continually in from the site of the middiaphysis of the RF. The specimen
the computerized monitor linked to the load tester. was embedded in MMA without staining to yield a 40-␮m-
Femoral midshaft: An undecalcified section was obtained
Lumbar vertebral body: The L5 body specimen was thick crosscut ground section. Measurements were made on
fixed with a clamp at the bases of the transverse processes a cathode-ray tube monitor with a CCD camera (CCD High
in the holder of a diamond band saw (Exakt, Norderstedt, Gain Camera-1600A; Flovel Co., Tokyo, Japan) setting on
Germany). By removing the cranial and caudal ends of the microscope using a semiautomatic image-analyzing pro-
the specimens, the planoparallel ends at a height of 3.5 gram (Mac Scope; Mitani Corp., Fukui, Japan) on a com-
mm were obtained.(20) The cylinder samples were placed puter.(20) The total cross-sectional area (mm2), cortical bone
centrally on the smooth surface of a steel disk attached to area (mm2), and bone marrow area (mm2) were obtained.
the load tester. A craniocaudal compression force was The endocortical surface was approximated as a regular,
applied to the specimen via a steel disk at a nominal continuous line. The moment of inertia (mm4) of the cortical
deformation rate of 2 mm/minute. The maximum load bone area for the medial-lateral axis was calculated directly
(N) and structural stiffness (N/mm) were obtained, as by the image-analyzing computer.(20) Kinetic parameters
were those of the femur specimens.
such as dLS/BS, sLS/BS, MS/BS, MAR, and BFR/BS were
measured in the periosteal and endocortical envelopes. The
eroded surface (ES/BS; %) also was measured in the en-
docortical perimeter.
Bone histomorphometry
Lumbar vertebral body and proximal tibia: The L4 and
RT specimens were embedded in methylmethacrylate
(MMA) after Villanueva’s bone staining. From the middle
portion of the specimen, 10-␮m-thick undecalcified sagittal
sections were cut on a microtome (Reichert Jung Supercut
2050; Reichert Jung, Heidelberg, Germany). The L3 and left
tibia (LT) specimens were embedded in a mixture of MMA,
hydroxyglycol methacrylate, and 2-hydroxyethylacrylate
polymerized at 4°C. Six-␮m-thick specimens of the L3 and
LT were obtained as described for those of L4 and RT. The
L3 and LT sections were then stained for tartrate-resistant
acid phosphatase (TRAP).(21) Histomorphometry of L3, L4,
and bilateral tibia specimens was performed with a semiau-
tomatic image-analyzing system linked to a light micro-
scope (Cosmozone 1S; Nikon, Tokyo, Japan). For each
section, the area of the secondary spongiosa was measured,
but the region within 1.0 mm of the growth plate/
metaphyseal junction and one cortical shell width of the
endocortical surface was not measured, to exclude the pri-
mary spongiosa.
Statistical analysis
All values are expressed as mean and SEM. One-way
ANOVA with repeated measurement was used to examine
the significance of changes in the climbing distances and
time. Data were assessed by two-way ANOVA for the time
and treatment. When the treatment was found to have a
significant overall effect, the difference between the exer-
cise and sedentary groups was assessed by Student’s t-test
for each time period.(14,26) The analysis of covariance (AN-
COVA) was done to examine the significance of changes in
bone mass and strength, using the hindlimb muscles or the
abdominal adipose tissue values as covariate. Statistical
significance was set at less than 0.05. All the analyses were
performed with a commercially available statistical package
(SPSS Ver 9.0; SPSS, Tokyo, Japan).
RESULTS
For the structure parameters, the trabecular bone volume
(BV; ␮m2), trabecular tissue volume (TV; ␮m2), and tra-
becular bone surface (BS; ␮m) were measured. The trabec-
ular thickness (Tb.Th; ␮m), trabecular number (Tb.N;
1/mm), and trabecular bone separation (Tb.Sp; ␮m) were
calculated by a parallel plate model assuming constant
geometry.(22,23) For the bone formation parameters of L4
and RT, the single-labeled surface (sLS; ␮m), double-
labeled surface (dLS; ␮m), trabecular bone surface (B.S:
␮m), and the mean distance between double labels (Ir.L.th;
␮m) were measured. The mineral apposition rate (MAR;
␮m/day) was calculated as the Ir.L.th multiplied by ␲/4.
The mineralizing surface per BS (MS/BS; %) was obtained
by adding the values of the dLS/BS and half of the sLS/BS
Climbing distances and time periods
The daily climbing distances in the exercise group after 2,
4, 6, and 8 weeks were 141 Ϯ 1.6 m/day, 148 Ϯ 2.6 m/day,
151 Ϯ 3.9 m/day, and 137 Ϯ 2.4 m/day, respectively. The
respective time periods for the activity were 26.2 Ϯ 1.2
minutes/day, 25.3 Ϯ 0.2 minutes/day, 26.5 Ϯ 0.9 minutes/
day, and 24.5 Ϯ 0.8 minutes/day. No significant differences
were found among these values.
Body weight, hindlimb muscles, abdominal fats, and
bone mineral measurements
Body weights did not significantly differ between the
value. The surface referent bone formation rate (BFR/BS; exercise and sedentary groups throughout the experimental
␮m%/day), was calculated by multiplying the MS/BS value period (Table 1). The hindlimb muscles value in the exer-
by the MAR.(22–24) For the bone resorption parameters of L3 cise group was significantly higher than that in the sedentary

EFFECTS OF TOWER CLIMBING EXERCISE ON BONE IN GROWING RATS
169
group after 4 weeks but not after 8 weeks. The abdominal
fats value in the exercise group was lower than those in the
sedentary group after both 4 weeks and 8 weeks. Except for
the BMD value of the proximal tibia after 4 weeks, no
difference was found between the two groups for these
parameters. However, after 8 weeks the BMC and BMD
values of the midfemur and the proximal tibia in the exer-
cise group were significantly higher than the values in the
sedentary group. After 4 weeks or 8 weeks, the parameters
of BMC and BMD in the lumbar vertebra did not signifi-
cantly differ between the exercise and sedentary groups.
The test of regression in ANCOVA showed no significance
in all the BMC or BMD values, using the hindlimb muscles
or abdominal fats values as covariate.
Mechanical properties of the midfemur and lumbar
vertebra, and the geometry of the femoral cortex
After 4 weeks, the values of the maximum load of the
midfemur, total cross-sectional area, and moment of inertia
in the exercise group were significantly higher than those in
the sedentary group (Table 2). After 8 weeks, the maximum
load and structural stiffness of the midfemur and total
cross-sectional area, cortical bone area, and moment of
inertia values in the exercise group were higher than those
in the sedentary group. The maximum load or structural
stiffness values of the lumbar vertebra did not significantly
differ throughout the experimental period. The test of re-
gression in ANCOVA showed no significance in all the
maximum load or structural stiffness values, using the hind-
limb muscles or abdominal fats values as covariate.
Kinetic parameters of the periosteal and endosteal
surfaces
Periosteal surface: After both 4 weeks and 8 weeks, the
values of MS/BS, MAR, and BFR/BS in the exercise group
were significantly higher than those in the sedentary group
(Table 3).
Endosteal surface: After 4 weeks, the MAR values in the
exercise group were significantly lower in the sedentary
group. However, after 8 weeks the MS/BS, MAR, and
BFR/BS values in the exercise group were significantly
lower than the values in the sedentary group. The ES/BS
values did not significantly differ throughout the experimen-
tal period.
Structural and kinetic parameters of the lumbar
vertebra
Structural indices: After both 4 weeks and 8 weeks, the
parameters of BV/TV and Tb.Th in the exercise group were
significantly higher than those in the sedentary group (Table
4). The Tb.N or Tb.Sp values did not significantly differ in
either period.
Bone formation and resorption: After 4 weeks, the value
of BFR/BS in the exercise group was significantly higher
and the Oc.S/BS value was significantly lower than those in
the sedentary groups. However, after 8 weeks the values of
MS/BS, MAR, and BFR/BS in the exercise groups were

170
NOTOMI ET AL.
␮
␮
␮
␮

EFFECTS OF TOWER CLIMBING EXERCISE ON BONE IN GROWING RATS
171
significantly larger, and the Oc.S/BS values were signifi-
cantly lower, than those in the sedentary groups.
Structural and kinetic parameters of the tibia
Structural indices: After both 4 weeks and 8 weeks, the
parameters of BV/TV and Tb.Th in the exercise group were
significantly higher than those in the sedentary group (Table
5). The Tb.N or Tb.Sp values did not significantly differ in
either period.
␮
Bone formation and resorption: Except for the MS/BS
value after 4 weeks, the values of MS/BS, MAR, and
BFR/BS in the exercise groups were significantly higher
and the Oc.S/BS values were significantly lower, compared
with those values in the sedentary groups after both 4 weeks
and 8 weeks.
␮
DISCUSSION
This study showed that voluntary climbing exercise for
24–27 minutes/day accelerates age-dependent increases in
mass and strength of the femur and trabecular bone mass of
the lumbar vertebra and tibia in growing rats. After 4 weeks,
the parameters of trabecular and periosteal bone formation
increased and those of trabecular osteoclasts decreased.
Although the increases in the BMC and BMD values of the
femur and tibia and the bending load values of the femur
were significant, exercise did not significantly increase the
BMC, BMD, or compressive load of the lumbar vertebra.
Climbing exercise had a beneficial effect on femoral cortex
and tibia trabecular, rather than the vertebral trabecular. In
the femur, the parameters of cortical bone structure and
bending load values both significantly increased after 4
weeks. The endocortical BSs were less sensitive to exercise.
It has been suggested that treadmill-running exercise in-
creases trabecular bone formation and decreases resorption
in the tibia.(27,28) Our present findings on the local turnovers
of the lumbar vertebra and tibia are consistent with these
findings. Because the parameters of osteoclasts were re-
duced, resistance exercise seems to increase bone mass by
both increasing bone formation and reducing bone resorp-
tion in the trabecular bone. However, in the femoral cortex,
the ES at the endocortical surface did not change after
exercise. Thus, the effects of climbing exercise on the
cortical envelopes were mainly on periosteal bone forma-
tion. Because the cortical bone structure and the bending
load increased together after 4 weeks, the parameters of
cortical bone structure seem to be sensitive enough to detect
the morphological changes induced by climbing exercise in
the early stages.
␮
␮
The climbing exercise increased the total cross-sectional
area and cortical area of the midfemur. The data are con-
sistent with previous reports on the effect of electrically
stimulated jumping exercise on the femur in growing and
mature rats.(12–14) In mature rats, there was a trend toward a
greater value in both the total cross-sectional area and the
cortical area in the exercise group, with a significant in-
crease in osteocalcin messenger RNA (mRNA) content in
the bone matrix.(13) Thus, resistance exercises such as jump-

172
NOTOMI ET AL.
ing and climbing seem to be potent for stimulating perios-
teal bone formation. In our experiment, although neither the
femoral BMC nor the BMD significantly increased, the
parameters of total cross-sectional area, moment of inertia,
and bending load increased after 4 weeks. These observa-
tions are in agreement with previous observations that the
biomechanical properties of the femur were improved de-
spite a lack of increase in BMC.(14,29,30)
The BMC, BMD, and compressive load values of the
lumbar vertebra did not seem to be caused by the trabecular
bone mass and structure, because the parameters of BV/TV,
Tb.Th significantly increased after both 4 weeks and 8
weeks. The relationship between mechanical stress and
structure is not a one to one simple correspondence.(31,32)
The lumbar vertebrae are likely to receive less mechanical
stress than the tibia during climbing exercise, because the
BMD values of the proximal tibia were significantly in-
creased after both 4 weeks and 8 weeks. Changes in the
thickness of the cortical shell, which we did not measure,
could be another possibility.(20)
␮
␮
Bone formation was augmented in the early stages of
exercise in both the cortical and the trabecular bones, as was
suggested in previous studies.(9,14,33) The resistance exercise
significantly increased the parameters of periosteal bone
formation in the midfemur. However, endocortical bone
formation parameters decreased. Thus, the effects of climb-
ing exercise on bone formation were site specific in the
femoral cortex, supporting accelerated cortical drift by me-
chanical stimulation. It has been shown that treadmill-
running exercise significantly increased the endocortical
BFR of the tibial shaft.(9) Our findings are inconsistent with
a previous report. One putative explanation is that different
mechanical thresholds exist on cortical envelopes, as pro-
posed by Frost.(1,2)
␮
Concerning exercise and bone, most animal studies have
used treadmill exercise on a nonvoluntary basis.(9–11,27,28,34)
Some studies found a beneficial effect on femoral and tibial
bone, but not vertebrae,(9,10) or a beneficial effect on those
bones(34) with a training regimen including daily running of
approximately 1.4–1.5 km for 12 weeks,(9) 1.0–1.1 km for
16 weeks,(10) and 2.0–2.1 km for 24 weeks.(34) Our volun-
tary exercise included the daily climbing of approximately
0.12–0.16 km for 4 weeks and 8 weeks and had beneficial
effects on bone in growing rats. These data suggest that the
effect of exercise on bone mass and strength does not
depend on the distance or duration of the exercise, but may
depend on the magnitude of the workload on bone while
exercising. It also has been suggested that increased bone
formation after exercise is not caused by simply the inten-
sity and/or duration of the exercise, but rather to the change
in the exercise level that is necessary to stimulate bone
formation.(35) Therefore, the greater mechanical load in-
duced by resistance exercise affected bone in this study,
more than that of treadmill running.
␮
Body weight did not differ between the sedentary and
exercise groups. However, the lean body mass in the exer-
cise group would be increased, because the exercise in-
creased muscle mass and decreased abdominal adipose tis-
sue. In this experiment, the test of regression in ANCOVA
showed no differences in the bone mass and strength, using

EFFECTS OF TOWER CLIMBING EXERCISE ON BONE IN GROWING RATS
173
8. Bourrin S, Ghaemmaghami F, Vico L, Chappard D, Gharib C,
Alexandre C 1992 Effect of a five-week swimming program
on rat bone: A histomorphometric study. Calcif Tissue Int
51:137–142.
9. Iwamoto J, Yeh JK, Aloia JF 1999 Differential effect of
treadmill exercise on three cancellous bone sites in the young
growing rat. Bone 24:163–169.
10. Yeh JK, Aloia JF, Chen M 1994 Growth hormone adminis-
tration potentiates the effect of treadmill exercise on long bone
formation but not vertebrae in middle-aged rats. Calcif Tissue
Int 54:38–43.
11. Bourrin S, Genty C, Palle S, Gharib C, Alexandre C 1994
Adverse effects of strenuous exercise: A densitometric and
histomorphometric study in the rat. J Appl Physiol 76:1999–
2005.
12. Umemura Y, Toshihiro I, Takeshi Y, Masashi K, Shoji M
1997 Five jumps per day increase bone mass and breaking
force in rats. J Bone Miner Res 12:1480–1485.
13. Westerlind KC, Fluckey JD, Gordon ST, Kraemer WJ, Farrell
PA, Turner RT 1998 Effect of resistance exercise training on
cortical and cancellous bone in mature rats. J Appl Physiol
84:459–464.
14. Notomi T, Lee SJ, Okimoto N, Okazaki Y, Takamoto T,
Nakamura T, Suzuki M 2000 Effects of resistance exercise
training on mass, strength, and turnover of bone in growing
rats. Eur J Appl Physiol 82:268–274.
15. Yarasheski KE, Lemon WR, Gilloteaux 1990 Effect of heavy-
resistance exercise training on muscle fiber composition in
young rats. J Appl Physiol 69:434–437.
muscle or fat mass as covariate. These results suggested that
the increased bone mass and strength mainly were caused
by the loading by the exercise, but not the secondary effects
of an increase in muscle mass or lean body mass (LBM).
In human study, resistance training is more effective than
aerobic training for increasing the bone mass.(5–7) Resis-
tance training increases bone formation and decreases re-
sorption in young males as assessed from serum osteocalcin
and urinary deoxypyridinoline, as we previously reported.(6)
The local turnover of the lumbar and femur in rat are
consistent with these findings. Although the studies use
different species, this exercise model has the potential to
facilitate understanding of the role that resistance exercise
might have in preventing bone loss and potentially to in-
crease bone gain.
In conclusion, voluntary climbing exercise accelerated
the radial cortical growth of the midfemur by stimulating
the periosteal bone formation. The cortical bone formation
induced by the climbing exercise seemed to strengthen the
structure of the midfemur. The increase in trabecular bone
mass of the lumbar vertebrae and tibia was caused by both
increased bone formation and reduced bone resorption. The
effect of the exercise was site specific on the cortical enve-
lope in the midfemur, supporting accelerated cortical drift
by mechanical stimulation.
16. Duncan ND, Williams DA, Lynch GS 1998 Adaptation in rat
skeletal muscle following long-term resistance exercise train-
ing. Eur J Appl Physiol 77:372–378.
17. Matsuo T, Suzuki M 1997 Brain ␤-adrenergic receptor binding
in rats with obesity induced by a beef tallow diet. Metabolism
46:18–22.
18. Matsuo T, Sumida H, Suzuki M 1995 Effects of chemical
sympathectomy on lipoprotein lipase activities in peripheral
tissues of rats fed high fat diets consisting of different fats. J
Nutr Sci Vitaminol 41:377–386.
ACKNOWLEDGMENTS
The authors thank Mr. Yushi Kato, KOKUYO Corp.,
Osaka, Japan, for help with making the resistance exercise
apparatus and Dr. Tatsuhiro Matsuo, University of Kagawa,
and Mr. Yasuhiro Mizushima, University of Tsukuba, for
helpful discussion.
19. Tanaka Y, Nakamura T, Nishida S, Suzuki K, Takeda S, Sato
K, Nishi Y 1996 Effects of a synthetic vitamin D analog,
ED-71, on bone dynamics and strength in cancellous and
cortical bone in prednisolone-treated rats. J Bone Miner Res
11:325–336.
20. Ohnishi H, Nakamura T, Narusawa K, Murakami H, Abe M,
Barbier A, Suzuki K 1997 Bisphosphonate tiludronate in-
creases bone strength by improving mass and structure in
established osteopenia after ovariectomy in rats. Bone 21:335–
343.
21. Tsurukami H, Nakamura T, Suzuki K, Sato K, Higuchi Y,
Nishii Y 1994 A novel synthetic vitamin D analogue, 2␤-(3-
hydroxypropoxy) 1␣,25-dihydroxyvitamin D3 (ED-71), in-
creases bone mass by stimulating the bone formation in normal
and ovariectomized rats. Calcif Tissue Int 54:142–149.
22. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H,
Muenier PJ, Ott SM, Recker RR 1987 Bone histomorphom-
etry: Standardization of nomenclature, symbols and units. Re-
port of the ASBMR Histomorphometry Nomenclature Com-
mittee. J Bone Miner Res 2:595–610.
REFERENCES
1. Frost HM 1997 On our age-related bone loss: Insights from a
new paradigm. J Bone Miner Res 12:1539–1546.
2. Schissl H, Frost HM, Jee WSS 1998 Estrogen and bone-
muscle strength and mass relationships. Bone 22:1–6.
3. Davee AM, Rosen CJ, Adler RA 1990 Exercise patterns and
trabecular bone density in college women. J Bone Miner Res
5:245–250.
4. Menkes A, Mazel S, Redmond RA, Koffler K, Libanati CR,
Gundberg CM, Zizic TM, Hagberg JM, Partley RE, Hurley BF
1993 Strength training increases regional bone mineral density
and bone remodeling in middle-aged and older men. J Appl
Physiol 74:2478–2484.
5. Dalsky GP, Stocke KS, Ehsani AA, Slatopolsky E, Lee WC,
Birge SJ 1988 Weight bearing training and bone mineral
content in postmenopausal women. Ann Intern Med 108:824–
828.
23. Parfitt AM, Mathews CH, Villanueva AR, Kleerkoper M,
Frame B, Rao DS 1983 Relationship between surface, volume,
and thickness of iliac trabecular bone in aging and in osteo-
porosis: Implications for the micro anatomic and cellular
mechanisms for bone loss. J Clin Invest 72:1396–1409.
24. Frost HM 1983 Bone histomorphometry: Analysis of trabec-
ular bone dynamics. In: Recker RR (ed.) Bone Histomorphom-
etry: Techniques and Interpretations. CRC Press Boca Raton,
FL, USA, pp. 109–131.
6. Fujimura R, Ashizawa N, Watanabe M, Mukai N, Amagai H,
Fukubayashi T, Hayashi K, Tokuyama K, Suzuki M 1997
Effect of resistance exercise training on bone formation and
resorption in young male subjects assessed by biomarkers of
bone metabolism. J Bone Miner Res 12:656–662.
7. Heinrich CH, Going SB, Pamenter RW, Perry CD, Boyden
TW, Lohman TG 1990 Bone mineral content of cyclically
menstruating female resistance and endurance trained athletes.
Med Sci Sports Exerc 22:558–563.

174
NOTOMI ET AL.
25. Murakami H, Nakamura T, Tsurukami H, Abe M, Barbier A,
Suzuki K 1994 Effect of tiludronate on bone mass, structure,
cortical bone mass, dimensions and strength-assessed in a
sexually mature, ovariectomized rat model. Bone 16:223–230.
and turn over at the epiphyseal, primary, and secondary spon- 33. Kristoffersson A, Hultdin J, Holmlund I, Thorsen K, Lorent-
giosa in the proximal tibia of growing rats after sciatic neurec-
tomy. J Bone Miner Res 9:1355–1364.
26. Samuels A, Perry MJ, Tobias JH 1999 High-dose estrogen
induces de novo medullary bone formation in female mice.
J Bone Miner Res 14:178–186.
27. Bourrin S, Palle S, Pupier R, Vico L, Alexandre C 1995
Effects of physical exercise training on bone adaptation in
three zone of rat tibia. J Bone Miner Res 10:1745–1752.
zon R 1995 Effects of short-term maximal work-on plasma
calcium, parathyroid hormone, osteocalcin and biochemical
markers of collagen metabolism. Int J Sports Med 16:145–
149.
34. Mosekilede L, Danielsen CC, Sogaard CH, Thorling R 1994
The effect of long-term exercise on vertebral and femoral bone
mass, dimension and strength-assessed in a rat model. Bone
15:293–301.
28. Yeh JK, Aloia JF, Chen MM, Tierney JM, Sprintz S 1993 35. Raab DM, Smith EL, Crenshaw TD, Thomas DP 1994 Bone
Influence of exercise on cancellous bone of the aged female
rat. J Bone Miner Res 8:1117–1125.
response to alternate-day mechanical loading of the rat tibia.
J Bone Miner Res 9:203–211.
29. Barrengolts EI, Curry DJ, Bapna MS, Kukreja SC 1993 Effects
of endurance exercise on bone mass and mechanical properties
in intact and ovariectomized rats. J Bone Miner Res 8:937–
942.
30. Raab DM, Smith EL, Crenshaw TD, Thomas DP 1990 Bone
mechanical properties after exercise training in young and old
rats. J Appl Physiol 68:130–134.
31. Landis WJ, Librizzi JJ, Dunn MG, Silver FH 1995 A study of
the relationship between mineral content and mechanical prop-
erties of turkey gastrocnemius tendon. J Bone Miner Res
10:859–867.
Address reprint requests to:
Masashige Suzuki
Institute of Health and Sports Sciences
University of Tsukuba
Tsukuba-shi
Ibaragi-ken 305-8574, Japan
32. Mosekilde L, Danielsen CC, Sogaard CH, Mcosker JE, Wron- Received in original form February 17, 2000; in revised form July
ski TJ 1995 The anabolic effects of parathyroid hormone on 10, 2000; accepted August 22, 2000.