Journal of Applied Physiology
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

J Appl Physiol 95: 300-307, 2003. First published February 28, 2003; doi:10.1152/japplphysiol.01076.2002
8750-7587/03 $5.00
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow All Versions of this Article:
95/1/300    most recent
01076.2002v1
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Web of Science (24)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Huang, T. H.
Right arrow Articles by Yang, R. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Huang, T. H.
Right arrow Articles by Yang, R. S.

Effects of different exercise modes on mineralization, structure, and biomechanical properties of growing bone

T. H. Huang,1,2 S. C. Lin,2 F. L. Chang,1,2 S. S. Hsieh,1 S. H. Liu,3 and R. S. Yang2

1Department of Physical Education, National Taiwan Normal University, Taipei, Taiwan 106; and 2Department of Orthopaedics, and 3Institute of Toxicology, National Taiwan University, Taipei, Taiwan 100

Submitted 25 November 2002 ; accepted in final form 27 February 2003


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Weight bearing during exercise plays an important role in improving the mechanical properties of bone. The effect on bone of non-weight-bearing exercise such as swimming remains controversial. To investigate the effects of exercise mode on growing bone, 29 male Wistar rats (7 wk old) were randomly assigned to a running exercise group (Run, n = 9), a swimming exercise group (Swim, n = 10), or a nonexercise control group (Con, n = 10). During an 8-wk training session (20–60 min/day, 5 days/wk), the Run rats were trained at progressively increasing running speeds (12–22 m/min), and weights attached to the tail of the Swim rats were progressively increased from 0 to 2% of their body weight. The bone mineral density of the proximal tibiae of the Run rats was significantly higher than in the Swim (P < 0.05). Femoral wet weights of the two exercise groups were significantly higher than in the control group (P < 0.05). Interestingly, the percent difference between the tissue wet weight and dry weight (water content ratio), which is related to bone mechanical properties, was significantly higher in the tibiae of the Swim rats and the femora of both exercise groups compared with controls (P < 0.05). Extrinsic as well as intrinsic biomechanical material properties were measured in a three-point bending test. Bone mechanical properties of the tibiae and femora of rats in the Swim and Run groups were significantly greater than those in the control group (P < 0.05). In summary, different modes of exercise may benefit bone mechanical properties in different ways. The specific effects of swimming exercise (non-weight-bearing exercise) on bone require further study.

weight-bearing and non-weight-bearing exercise; rat

IT IS WELL KNOWN IN THE LITERATURE that mechanical loading plays an important role in bone development (6, 7, 29, 34). It has been reported that mechanical loading generated by physical activities leads to improvements in skeletal development (8, 21). In human studies, bone mineral density (BMD) is a common indicator reflecting bone development and bone mechanical properties. Physical activity with weight bearing has been shown to improve BMD (15, 17, 23, 27, 31). On the other hand, previous studies have reported that non-weight-bearing exercise such as swimming does not have an equivalent beneficial effect on BMD. The BMD in people who have participated in a non-weight-bearing swimming exercise program has been shown to not be significantly different than the BMD in respective control groups (9, 12, 14, 16, 37, 39).

Because of ethical issues, measurements of bone development in human studies are typically limited to noninvasive radiography or serum bone marker assays. It is difficult to investigate the effects of exercise mode on bone by using these techniques. On the other hand, animal models would be very useful in studying the relationship between exercise mode and bone. There is currently as yet an unmet need to establish an animal model specifically devoted to investigating the effects of exercise with or without mechanical loading on bone.

Direct biomechanical testing is feasible when using animal models and better reflects bone mechanical properties than noninvasive BMD measurements. To our knowledge, there has been only one published study relating the effects of running (weight-bearing) vs. swimming (non-weight-bearing) exercise on bone development (35). However, bone mechanical properties were not measured in this study. One reason for the paucity of such studies is the difficulty in equalizing the energy expenditure or total work of different modes of exercise. Nevertheless, several studies have investigated the effects of either weight-bearing or non-weight-bearing exercise on bone separately. It has been shown that non-weight-bearing exercises, generally swimming, have a positive influence on bone strength in ovariectomized rats (19), osteotomized rats (18), and growing rats (33). Therefore, there is evidence to suggest that non-weight-bearing exercise (swimming) seems to enhance the mechanical properties of bone under specific conditions, and direct comparison of its effects with those of weight-bearing exercise would be useful.

In the present study, the relative training intensities of two different exercise modes were controlled in an attempt to equalize the energy expenditure between the two training programs. We hypothesized that 1) weight-bearing exercise would lead to significantly greater levels of BMD, compared with non-weight-bearing exercise, and 2) non-weight-bearing exercise may have some beneficial influence on the mechanical properties of bone.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Animals. Thirty male Wistar rats (3 wk of age) were bred in the Animal Center of National Taiwan University and kept under controlled conditions that included a room temperature of 22 ± 1°C and a 12:12-h light-dark cycle. Animals were fed Purina Laboratory Rodent Diet (PMI, St. Louis, MO; 0.95% calcium) and distilled water ad libitum. The body weight of all animals was measured weekly. The experiment was initiated when the rats reached an age of 7 wk. During the training periods, all the animals were healthy and without infection. One animal was withdrawn from the study because of its unwillingness to run.

Experimental design. Animals were randomly assigned into one of three groups: a weight-bearing running exercise group (Run, n = 9), a non-weight-bearing swimming exercise group (Swim, n = 10), and a nonexercise control group (Con, n = 10).

Exercise training protocol. The training protocol for animals in the Run group was developed in a previously reported study in our laboratory (10). This protocol was modified according to the ~70% maximal O2 uptake running program for Wistar rats (11, 24). Animals of the Run group underwent an exercise training program on the treadmill 5 days/wk for 8 wk. In the first week of training, the animals in the Run group ran for 20 min/day at a speed of 12 m/min on the level treadmill (Table 1). The duration and intensity of the daily exercise session was progressively increased to 60 min at a speed of 22 m/min. The front portion of the lanes of the treadmill was covered with a thick paper to keep the area dark, because rats are more active in darkness. In addition, an electric grid at the rear of the treadmill provided a stimulus for running. An electric stimulus (24–33 volts, 0.4–0.55 amperes) was manually activated on for a period of <2 s when the animals remained on the electric grid for over 10 s. In the initial 2 wk of the study, the rats in the Run group could easily complete the daily training regimen because of the relatively low intensity of the exercise (12–14 m/min). Most all of the animals were compliant and responded to the increase in training intensity. Only one of the Run rats was withdrawn from the study because of its unwillingness to run.


View this table:
[in this window]
[in a new window]
  		Table 1. Training protocols for the 2 exercise groups

 

The animals in the Swim group swam in a large stainless tank filled with water 30 cm in depth and 35 ± 1°C in temperature. The tank was divided into eight equal sections (20 cm width and 40 cm length) by pieces of opaque acrylic. Each animal swam in its own space. Training intensity was varied by increasing the weight attached the animal's tail from 0 to 2% of its body weight. Previous studies used a swimming training protocol with a constant level of weight (2% body wt) attached to the rat's tail (28, 35, 36). The weight attached to the rat's tail in the present study was varied to be able to match the intensity of exercise with the animals in the group Run and to permit the animals to more easily adapt to the increased intensity of the swimming exercise. The Swim animals trained for 5 days/wk for 8 wk, similar to the Run animals. According to our previous study (10), the weight gain of growing rats varied with the intensity of the running exercise. Therefore, body weight was also used as an additional indicator to help equalize the energy expenditure and training intensities of the Run and Swim groups. All animals were weighed weekly to make sure that there was no significant difference between the two exercise groups. Under the conditions prescribed above, body weights of the animals in the two exercise groups were in fact matched during the training period.

Bone sample collection and measurement. According to APS's "Guiding Principles in the Care and Use of Animals," all the animals were anesthetized by administration of pentobarbital sodium (50 mg/kg) and euthanized by decapitation 72 h after termination of the training period. The animals were 15 wk of age at this time. The left tibia and femur were harvested. All soft tissues were removed from the bones. The bones were weighed (wet weight), their lengths were measured, and they were wrapped in aluminum foil and kept at -20°C for future densitometric and biomechanical testing. After completion of biomechanical testing, the fractured bone specimens were dehydrated in 100% alcohol for 48 h, air dried, and weighed (dehydrated dry weight). These weights served as the dry weights of the bone tissues. The percent difference between a bone's wet weight and dehydrated dry weight was computed and reflected the water content ratio of bone tissues.

BMD analysis. The BMD of the tibiae and femora was measured with a Norland XR-26 dual-energy X-ray absorptiometer (DEXA, Fort Atkinson, WI) according to a technique reported in our laboratory's previous work (10). The bone tissues of all animals were measured by using DEXA's small-subjects mode. A coefficient of variation of 0.7% was computed from daily measurements of BMD on a lumbar phantom for >1 yr. Bone tissues were thawed at room temperature before BMD measurement. Each entire left tibia and femur was scanned, and the images were divided into three segments: proximal quarter, distal quarter, and diaphyseal portion. Each area was analyzed separately to capture the variation in cortical and cancellous bone density. This division of the images was done according to that reported in previous studies (5, 10, 20). All bone tissues were then repackaged in aluminum foil and kept at -20°C until subsequent biomechanical testing.

Biomechanical three-point bending testing. Mechanical properties of bone tissues were measured in three-point bending in a materials testing system (MTS-858, MTS System, Minneapolis, MN). The span of the two support points was 20 mm, and the deformation rate was 1 mm/min. Load-deformation curves were transported to a personal computer and acquired by Team 490 software (version 4.10, Nicolet Instrument Technologies, Madison, WI). Sigma Plot 7.0 software (SPSS, Chicago, IL) was used to smooth the load-deformation curve and compute the extrinsic material properties of the bone samples, including the maximal load, ultimate load to failure, energy to maximal load, energy to ultimate load, and linear stiffness. Energies to maximal load and ultimate load were computed as the areas under the load-deforming curves as described in Fig. 1. Stiffness was computed as the slope of the linear portion of the load-deformation curve. After testing of the specimens in three-point bending, the failure sites of all bone specimens were photographed, together with a measurement standard, by a high-resolution digital camera at a standardized distance (Fig. 2). Cross-sectional parameters were measured from the photographs and used in the calculation of the cross-sectional moment of inertia. The cross-sectional moment of inertia was calculated under the assumption that the cross sections were elliptically shaped (40)

where I is the cross-sectional moment of inertia, a is the width of the cross section in the mediolateral direction, b is the width of the cross section in the anteroposterior direction, and t is the average of the cortical thickness. All of these parameters were obtained by using the image software Image Pro Plus 4.1 for Windows (Media Cybernetics, Silver Spring, MD). The maximal stress, ultimate stress, and elastic modulus (Young's modulus) were calculated by using the following equations (41)

where {sigma} is ultimate stress, c is the distance from the center of mass (equal to 1/2b as described above), F is the applied load (N), E is elastic modulus, d is the displacement (mm), and L is the span between the two support points of the bending fixture (mm). In addition, the energies to maximal stress and ultimate stress were also measured by computing the respective areas under the stress-strain curve.



View larger version (12K):
[in this window]
[in a new window]
  		Fig. 1. Loading-deformation curve. Max, value of the maximal load; Ultimate, load value before complete tissue failure; Max energy, energy to maximal load, which was the area under the curve up to the point of maximal load; Ultimate energy, energy to complete tissue failure, which was the total area under the curve.

 


View larger version (127K):
[in this window]
[in a new window]
  		Fig. 2. Cross-sectional photograph of the bending failure site.

 

Statistical analysis. One-way analysis of variance was used to analyze the weekly body weight changes among the three test groups. To eliminate the body weight-related effects, an analysis of covariance was used to adjust and analyze the mean values of all the experimental data. Pairwise comparisons were made by using the Scheffé's method. All data were expressed as means ± SD, and differences were considered significant if P < 0.05.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Body weight. During the 8-wk training period, the increase in body weight of both exercise groups was less than the increase in body weight of the control group (Fig. 3). After the third week of training, the mean body weights of the rats in the Run and Swim groups were significantly less than the weights of the control (Con) animals at each time point (P < 0.05). The differences in mean body weight between the exercise groups and control group progressively increased during the training period. At the end of training period, the rats in the exercise groups exhibited mean body weights that were 15–16% less than those of the Con rats (P < 0.05). There were no significant differences in mean body weight between the two exercise groups at all time points during the training period.



View larger version (17K):
[in this window]
[in a new window]
  		Fig. 3. Change in body weight during the experimental period. *P < 0.05, control (Con) group had a significantly higher body weight than the 2 exercise groups.

 

BMD measurements. The mean BMD of the proximal tibiae in the Run group rats was significantly greater than the respective mean BMD in the Swim group (P < 0.05) (Table 2). In addition, the rats in the Run group also exhibited higher mean total tibia BMD and distal femur BMD, compared with the Swim and Con groups, although these differences were not statistically significant.


View this table:
[in this window]
[in a new window]
  		Table 2. BMD in total and 3 segments of tibiae and femora

 

Bone weight, geometry, and biomechanical three-point-bending measurements. The two exercise groups had a higher mean femoral wet weight compared with the controls (P < 0.05) (Table 3). The mean water content ratio of the tibiae of the Swim animals was significantly greater than the mean water content ratio of the tibiae of the Run animals (P < 0.05). The mean water content ratio of the femora in the Swim and Run rats was significantly greater than the water content ratio of the control animal femora (P < 0.05). There were no statistically significant differences in cross-sectional area measurements between the test groups.


View this table:
[in this window]
[in a new window]
  		Table 3. Wet weight, dry weight, and geometric measurements of bone tissues

 

In the three-point bending testing, the mean maximal load of the tibiae and femora in the two exercise groups tended to be greater than the respective mean maximal load in the control animals (Table 4). Statistical analysis showed that the tibiae in the Swim rats exhibited a significantly higher mean maximal load than the tibiae in the Con group (P < 0.05). On the other hand, the mean ultimate load of the tibiae of the control rats was significantly greater than the mean ultimate load of the tibiae of the Swim animals (P < 0.05). In the bending energy analysis, the Swim group's tibiae showed the highest mean energy to maximal load compared with the Run and Con groups, although this difference was not significant. The two exercise groups demonstrated higher mean femoral energy to maximal load compared with the controls, and the difference between the Run and Con animal femora was significant (P < 0.05). In energy to ultimate load, the tibiae and femora of the two exercise groups exhibited greater values compared with the control group. Further statistical analysis showed that the mean energy to ultimate load in the tibiae of the Run and Swim animals was significantly greater than in the tibiae of the Con rats (P < 0.05). In addition, the mean energy to ultimate load of the Run group's femora was significantly greater than the controls (P < 0.05).


View this table:
[in this window]
[in a new window]
  		Table 4. Extrinsic biomechanical testing results of tibia and femur in 3-point bending

 

In addition to the extrinsic load-deformation parameters, the intrinsic material properties of the tibiae and femora were also obtained in this study (Table 5). The two exercise groups exhibited higher mean maximal stress of their tibiae and femora compared with the Con animals. The mean maximal stress of the tibiae of the Swim group was significantly greater than the respective control tibiae, and the mean maximal stress of the femora in both exercise groups was significantly greater than the control femora (P < 0.05). Similar to the extrinsic analysis, the mean ultimate stress in the tibiae of the Swim group was significantly lower than the mean ultimate stress of the Run and the Con tibiae, whereas the mean ultimate stress of the Run group's femora was significantly greater than in the control femora (P < 0.05). The mean Young's modulus of the Run tibiae and Swim femora were significantly greater than the mean Young's modulus of the Con animals (P < 0.05). The energies to maximal stress and ultimate stress were greater in both exercise groups than in the control group, with the difference between the femora of the Run and Con groups being significant (P < 0.05).


View this table:
[in this window]
[in a new window]
  		Table 5. Intrinsic biomechanical testing results of tibia and femur in 3-point bending

 


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ACKNOWLEDGMENTS
 REFERENCES
 
The purpose of this experiment was to investigate the effects of exercise with or without weight bearing on the mineral and mechanical properties of growing bone. Only rats subjected to the running exercise protocol exhibited a higher site-specific BMD compared with the swimming and control groups. However, both running and swimming resulted in increased long bone biomechanical properties compared with controls.

Our exercise-training regimen reduced the weight gains of the animals compared with the nonexercised controls, similar to that reported in the literature (2, 3, 10, 11, 24). Our training protocols were based on previous studies and used body weight as an additional indicator for monitoring and adjusting the training intensity of the Swim group to match that of the Run group (10). By doing this, we made body weights of the two exercise groups equivalent during the training period. In physiological terms, it is well known that similar body weight does not necessarily mean similar energy metabolism and body composition. Nevertheless, the possible differences between the two exercise groups should be the exercise mode and training intensity under our experimental conditions. Our previous work showed that different endurance training intensity levels would lead to different changes in body weight (10). Therefore, it is reasonable to speculate that our running and swimming training protocols resulted in similar energy metabolic rates, making comparisons between the two exercise groups feasible.

In the BMD analysis, the highest levels of BMD were found in the proximal tibia and distal femur of the Run rats. In addition, the Run animals exhibited higher levels of total tibia BMD than the animals in the Swim and Con groups, although these comparisons were not significant. Similar to studies in the human (13, 25, 38), the higher BMD in the knee would be due to the site-specific effects of the weight-bearing exercise. On the other hand, swimming exercise, because of its non-weight-bearing mode, showed the lowest BMD value in the proximal tibia and distal femur but not significantly lower than animals in the control group. This phenomenon was also similar to that previously reported in human studies in which the BMD in swimmers and other exercise participants was compared (9, 12, 14, 16, 37, 39). DEXA measurement has become a major tool of osteoporosis risk assessment. However, DEXA measurements do not take bone size (such as the cross-sectional area) into account, which is an independent and important determinant of the bone compression strength (1, 4, 26). Therefore, measurements of extrinsic and intrinsic biomechanical properties would be more useful for further understanding the adaptation of bone to exercise training.

In the present study, the two exercise groups exhibited superior bone mechanical properties compared with the control animals. The tibiae of the Run and Swim animals demonstrated increased maximal load and energy to ultimate load. Interestingly, these two biomechanical parameters were the highest (significantly) in the Swim group. The Run group's high maximal load and energy to ultimate load might be the result of the greater BMD induced by weight bearing in the proximal, diaphyseal, and total tibia. However, swimming exercise might lead to improved bone mechanical properties through a pathway other than increasing the BMD. As showed in Table 3, the Swim group animals showed the highest water content ratio in tibiae. Although the exact role of water content in bone tissue is not fully understood, its contribution to stabilizing collagen (22, 32) might exert an influence on the mechanical properties of bone. In addition, in vitro studies have show that hydration level of bone greatly influences its biomechanical properties (30, 42). On the other hand, improved mechanical properties may be due, in part, to geometric factors. Although the Swim animals' tibiae exhibited the highest maximal load of the three test groups, the Swim group's tibiae also demonstrated the lowest ultimate load. Having the significantly highest energy to ultimate load seems to imply that the Swim group's tibiae sustained more deformation or strain before failure. Further studies should be undertaken to determine whether this phenomenon is caused by the high water content ratio or some other factors associated with swimming exercise. The rats in the Run and Swim groups similarly showed a higher energy to maximal load and ultimate load compared with animals in the control group, although significant differences only occurred between the Run and Con groups. As suggested above, a significantly greater water content ratio in both exercise groups seemed to be related to superior mechanical properties.

In addition to water content ratio, several differences in cross-sectional parameters may have affected, in part, the extrinsic load-deformation properties. The cross-sectional parameters measured in this study were not significantly different among the three test groups. However, these geometric parameters seemed to advantageously affect the Swim group's load-deformation properties. After computation of the respective stress-strain data, the Swim group's mean level of maximal stress was modified and no longer statistically the highest. Interestingly, the Swim group still showed the lowest mean value of ultimate stress, significantly lower than the Run and Con groups. Further study would be valuable to investigate this particular adaptation. The femora in the Run group consistently exhibited the highest intrinsic and extrinsic biomechanical parameters. The femora in the Swim group also showed improved intrinsic mechanical properties, compared with the controls, although significance was not always achieved. In addition, the two exercise groups demonstrated a higher mean Young's modulus. Both swimming and running exercise protocols seemed to benefit intrinsic and extrinsic bone mechanical properties. Moreover, swimming and running training, respectively, benefited more on rats' tibiae and femur. According to the exercise specific, different exercise modes would generate different loading or strain on bone, which may cause site-specific adaptations (Swim's tibia and Run's femur) to occur.

Several previously reported studies involving rat models have demonstrated that training with swimming improved bone strength (18, 19, 33). Only one study compared the relative effects of running and swimming exercises on bone (35), but examination of bone mechanical properties was not included. To the best of our knowledge, this present study is the first to report the relative effects of weight-bearing and non-weight-bearing exercises on bone mechanical properties. The increase in some bone mechanical properties with swimming does not mean that non-weight-bearing exercise would improve all bone mechanical properties more than weight-bearing exercise. However, contrary to traditional attitudes, this study demonstrated that there were positive effects of non-weight-bearing exercise on some bone mechanical properties. Further studies are needed to investigate the effects of muscle contraction and systemic activation (e.g., growth hormone-insulin like growth factors pathway) on bone strength. Moreover, exercise might benefit bone mechanical properties by changing the composition of the bone (e.g., water content ratio, collagen formation) in addition to the bone mineral density.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
REFERENCES
 
English reediting assistance from William D. Lew was deeply appreciated.

This study was supported by a grant from the National Science Council (NSC-89-2314-B-002-380, Taiwan).


   FOOTNOTES
 

Address for reprint requests and other correspondence: R. S. Yang, Dept. of Orthopaedics, National Taiwan Univ. Hospital, No. 7, Chung-Shan South Rd., Taipei, Taiwan 100 (E-mail: fatsea.huang{at}msa.hinet.net).

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


   REFERENCES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 

  1. Augant P, Reeb H, and Claes LE. Prediction of fracture load at different skeletal sites by geometric properties of the cortical shell. J Bone Miner Res 11: 1356-1363, 1996.[Web of Science][Medline]
  2. Bigard AX, Brunet A, Guezennec CY, and Monod H. Effects of chronic hypoxia and endurance training on muscle capillarity in rats. Pflügers Arch 419: 225-229, 1991.[Web of Science][Medline]
  3. Bigard AX, Brunet A, Guezennec CY, and Monod H. Skeletal muscle changes after endurance training at high altitude. J Appl Physiol 71: 2114-2121, 1991.[Abstract/Free Full Text]
  4. Biggemann M, Hilweg D, and Brinckmann P. Prediction of the compressive strength of vertebral bodies of the lumbar spine by quantitative computed tomography. Skeletal Radiol 17: 264-269, 1988.[Web of Science][Medline]
  5. Bourrin S, Genty C, Palle S, Gharib C, and Alexandre C. Adverse effects of strenuous exercise: a densitometric and histomorphometric study in the rat. J Appl Physiol 76: 1999-2005, 1994.[Abstract/Free Full Text]
  6. Carter DR and Orr TE. Skeletal development and bone functional adaptation. J Bone Miner Res S2: 389-395, 1992.
  7. Carter DR. Mechanical loading history and skeletal biology. J Biomech 20: 1095-109, 1987.[Web of Science][Medline]
  8. Carter DR, van Der Meulen MCH, and Beaupre GS. Physical factors in bone growth and development. Bone S18: 5-10, 1996.
  9. Cassell C, Benedict M, and Specker B. Bone mineral density in elite 7- to 9-yr-old female gymnasts and swimmers. Med Sci Sports Exerc 28: 1243-1246, 1996.[Web of Science][Medline]
  10. Chang FL, Huang TH, Hsieh SS, Yang RS, and Lin CC. The effects of different endurance training intensity on systematic and peripheral citrate synthase activity (Abstract). Med Sci Sports Exerc S33: 295, 2001.
  11. Chen HI and Chiang IP. Chronic exercise decreases adrenergic agonist-induced vasoconstriction in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 271: H977-H983, 1996.[Abstract/Free Full Text]
  12. Courteix D, Lespessailles E, Peres SL, Obert P, Germain P, and Benhamou CL. Effect of physical training on bone mineral density in prepubertal girls: a comparative study between impact-loading and non-impact-loading sports. Osteoporos Int 8: 152-158, 1998.[Web of Science][Medline]
  13. Duncan CS, Blimkie CJ, Cowell CT, Burke ST, Briody JN, and Howman-Giles R. Bone mineral density in adolescent female athletes: relationship to exercise type and muscle strength. Med Sci Sports Exerc 34: 286-294, 2002.[Web of Science][Medline]
  14. Emslander HC, Sinaki M, Muhs JM, Chao EY, Wahner HW, Bryant SC, Riggs BL, and Eastell R. Bone mass and muscle strength in female college athletes (runners and swimmers). Mayo Clin Proc 73: 1151-1160, 1998.[Abstract]
  15. Etherington J, Harris PA, Nandra D, Hart DJ, Wolman RL, Doyle DV, and Spector TD. The effect of weight-bearing exercise on bone mineral density: a study of female ex-elite athletes and the general population. J Bone Miner Res 11: 1333-1338, 1996.[Web of Science][Medline]
  16. Fehling PC, Alekel L, Clasey J, Rector A, and Stillman RJA. Comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone 17: 205-210, 1995.[Medline]
  17. Grimston SK, Willows ND, and Hanley DA. Mechanical loading regime and its relationship to bone mineral density in children. Med Sci Sports Exerc 25: 1203-1210, 1993.[Web of Science][Medline]
  18. Guerino MR, Luciano E, Goncalves M, and Leivas TP. Effects of chronic physical activity and of ultrasound treatment on bone consolidation. Physiol Chem Phys Med NMR 31: 131-138, 1993.
  19. Hart KJ, Shaw JM, Vajda E, Hegsted M, and Miller SC. Swim-trained rats have greater bone mass, density, strength, and dynamics. J Appl Physiol 91: 1663-1668, 2001.[Abstract/Free Full Text]
  20. Huang TH, Yang RS, Hsieh SS, and Liu SH. Effects of caffeine and exercise on the development of bone: a densitometric and histomorphometric study in young Wistar rats. Bone 30: 293-299, 2002.[Medline]
  21. Kannus P, Sievanen H, and Vuori I. Physical loading, exercise and bone. Bone S18: 1-3, 1996.
  22. Lazarev IuA, Lazareva AV, and Grechishko VS. Effect of the length of molecular chain on the formation of triple-helical collagen-like complex in solutions. The role of water in the formation of triple helix [in Russian, English summary]. Biofizika 42: 54-67, 1997.[Medline]
  23. Lehtonen-Veromaa M, Mottonen T, Svedstrom E, Hakola P, Heinonen OJ, and Viikari J. Physical activity and bone mineral acquisition in peripubertal girls. Scand J Med Sci Sports 10: 236-243, 2000.[Web of Science][Medline]
  24. Lin YS, Jan MS, Tsai TJ, and Chen HI. Immunomodulatory effects of acute exercise bout in sedentary and trained rats. Med Sci Sports Exerc 27: 73-78, 1995.[Web of Science][Medline]
  25. Morel J, Combe B, Francisco J, and Bernard J. Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporos Int 12: 152-157, 2001.[Web of Science][Medline]
  26. Myers ER, Hecker AT, Rooks DS, Hipp JA, and Hayes WC. Geometric variables from DXA of the radius predict forearm fracture load in vitro. Calcif Tissue Int 52: 199-204, 1993.[Web of Science][Medline]
  27. Nordstrom P, Nordstrom G, Thorsen K, and Lorentzon R. Local bone mineral density, muscle strength, and exercise in adolescent boys: a comparative study of two groups with different muscle strength and exercise levels. Calcif Tissue Int 58: 402-408, 1996.[Web of Science][Medline]
  28. Nyska M, Nyska A, Swissa-Sivan A, and Samueloff S. Histomorphometry of long bone growth plate in swimming rats. Int J Exp Pathol 76: 241-245, 1995.[Web of Science][Medline]
  29. Parfitt AM. The two faces of growth: benefits and risks to bone integrity. Osteoporos Int 4: 382-398, 1994.[Web of Science][Medline]
  30. Pelker RR, Friedlaender GE, Markham TC, Panjabi MM, and Moen CJ. Effects of freezing and freeze-drying on the biomechanical properties of rat bone. J Orthop Res 1: 405-411, 1984.[Medline]
  31. Pettersson U, Nordstrom P, Alfredson H, Henriksson-Larsen K, and Lorentzon R. Effect of high impact activity on bone mass and size in adolescent females: a comparative study between two different types of sports. Calcif Tissue Int 67: 207-214, 2000.[Web of Science][Medline]
  32. Rochdi A, Foucat L, and Renou JP. Effect of thermal denaturation on water-collagen interactions: NMR relaxation and differential scanning calorimetry analysis. Biopolymers 50: 690-696, 1999.[Web of Science][Medline]
  33. Simkin A, Leichter I, Swissa A, and Samueloff S. The effect of swimming activity on bone architecture in growing rats. J Biomech 22: 845-851, 1989.[Web of Science][Medline]
  34. Skerry TM. Mechanical loading and bone: what sort of exercise is beneficial to the skeleton? Bone 20: 179-181, 1997.[Medline]
  35. Snyder A, Zierath JR, Hawley JA, Sleeper MD, and Craig BW. The effects of exercise mode, swimming vs. running, upon bone growth in the rapidly growing female rat. Mech Ageing Dev 66: 59-69, 1992.[Web of Science][Medline]
  36. Swissa-Sivan A, Azoury R, Statter M, Leichter I, Nyska A, Nyska M, Menczel J, and Samueloff S. The effect of swimming on bone modeling and composition in young adult rats. Calcif Tissue Int 47: 173-177, 1990.[Web of Science][Medline]
  37. Taaffe DR and Marcus R. Regional and total body bone mineral density in elite collegiate male swimmers. J Sports Med Phys Fitness 39: 154-159, 1999.[Web of Science][Medline]
  38. Taaffe DR, Robinson TL, Snow CM, and Marcus R. High-impact exercise promotes bone gain in well-trained female athletes. J Bone Miner Res 12: 255-260, 1997.[Web of Science][Medline]
  39. Taaffe DR, Snow-Harter C, Connolly DA, Robinson TL, Brown MD, and Marcus R. Differential effects of swimming versus weight-bearing activity on bone mineral status of eumenorrheic athletes. J Bone Miner Res 10: 586-593, 1995.[Web of Science][Medline]
  40. Turner CH, Akhter MP, and Heaney RP. The effects of fluoridated water on bone strength. J Orthop Res 10: 581-587, 1992.[Web of Science][Medline]
  41. Turner CH and Burr DB. Basic biomechanical measurements of bone: a tutorial. Bone 14: 595-608, 1993.[Medline]
  42. Yeni YN, Brown CU, and Norman TL. Influence of bone composition and apparent density on fracture toughness of the human femur and tibia. Bone 22: 79-84, 1998.[Medline]



This article has been cited by other articles:


Home page
 Am. J. Physiol. Endocrinol. Metab.Home page
J. Teerapornpuntakit, N. Dorkkam, K. Wongdee, N. Krishnamra, and N. Charoenphandhu
Endurance swimming stimulates transepithelial calcium transport and alters the expression of genes related to calcium absorption in the intestine of rats
Am J Physiol Endocrinol Metab, April 1, 2009; 296(4): E775 - E786.
[Abstract] [Full Text] [PDF]

Home page
 Br. J. Sports. Med.Home page
P Zhang, G M Malacinski, and H Yokota
Joint loading modality: its application to bone formation and fracture healing
Br. J. Sports Med., July 1, 2008; 42(7): 556 - 560.
[Abstract] [Full Text] [PDF]

Home page
 Br. J. Sports. Med.Home page
R A Santos-Rocha, C S Oliveira, A P Veloso, M Espanha, and R Dyson
Osteogenic index of step exercise depending on choreographic movements, session duration, and stepping rate * COMMENTARY * COMMENTARY
Br. J. Sports Med., October 1, 2006; 40(10): 860 - 866.
[Abstract] [Full Text] [PDF]

Home page
 J. Appl. Physiol.Home page
J. M. Welch, C. M. Weaver, and C. H. Turner
Adaptations to free-fall impact are different in the shafts and bone ends of rat forelimbs
J Appl Physiol, November 1, 2004; 97(5): 1859 - 1865.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow All Versions of this Article:
95/1/300    most recent
01076.2002v1
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Web of Science (24)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Huang, T. H.
Right arrow Articles by Yang, R. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Huang, T. H.
Right arrow Articles by Yang, R. S.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Visit Other APS Journals Online
Copyright © 2003 by the American Physiological Society.