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McCaig Centre for Joint Injury and Arthritis Research, University of Calgary, Calgary, Alberta, Canada T2N 4N1
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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We investigated whether high-impact drop jumps could increase bone formation in the middiaphyseal tarsometatarsus of growing rooster. Roosters were designated as sedentary controls (n = 10) or jumpers (n = 10). Jumpers performed 200 drop jumps per day for 3 wk. The mechanical milieu of the tarsometatarsus was quantified via in vivo strain gauges. Indexes of bone formation and mechanical parameters were determined in each of twelve 30° sectors subdividing the middiaphyseal cortex. Compared with baseline walking, drop jumping produced large peak strain rates (+740%) in the presence of moderately increased peak strain magnitudes (+30%) and unaltered strain distributions. Bone formation rates were significantly increased by jump training at periosteal (+40%) and endocortical surfaces (+370%). Strain rate was significantly correlated with the specific sites of increased formation rates at endocortical but not at periosteal surfaces. Previously, treadmill running did not enhance bone growth in this model. Comparing the mechanical milieus produced by running and drop jumps revealed that jumping significantly elevated only peak strain rates. This further emphasized the sensitivity of immature bone to high strain rates.
bone adaptation; mechanical stimuli; cortical bone; modeling; rooster
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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EXERCISE DURING GROWTH can significantly contribute to the enhancement of peak bone mass reached at young adulthood (1). The design of exercise protocols that provide maximal efficacy as a prophylactic tool against bone pathologies later in life, however, requires an understanding of the effects of exercise-related mechanical stimuli on the skeleton. Unfortunately, well-controlled longitudinal exercise studies have produced inconsistent results, perhaps reflecting a lack of this understanding. Running, as an example of a common exercise, reportedly can have positive (3, 26, 33), negligible (15, 16), or detrimental effects (8, 20, 23) on the growing skeleton of animals.
Recent cross-sectional (6, 7, 9, 27) and longitudinal studies (2, 39) suggest that high-impact exercise can be osteogenically more effective than lower impact aerobic exercise. These studies provide encouraging data demonstrating that bone cells are capable of responding to exercise-induced mechanical stimuli with significant bone formation. From a mechanical perspective, high-impact exercise is ill defined, and the specific aspect of the exercise-induced mechanical milieu causing bone hypertrophy has not been identified. In external loading models in which loading conditions can be controlled and adjusted, strain rate (24, 42) and strain magnitude (25, 35, 38) (among others) have been proposed as mechanical parameters that influence the adaptive process. The efficacy of high-impact exercise has often been attributed to the presumed increase in these two parameters, but this has not been confirmed. The lack of data describing bone's mechanical milieu during high-impact exercises makes it difficult to incorporate results from exercise intervention studies into the design of future protocols that could effectively stimulate bone growth. If, for instance, strain rate is more important than strain magnitude, then safe exercises could be devised that apply the loads very quickly but keep the load magnitude to a minimum in the bone and joints. Also, changes in loading directions during landings are characteristic of many high-impact exercises such as badminton or soccer, possibly altering strain distributions in bone. Bone cells may perceive altered strain distributions as an osteogenic stimulus (36), and it is unclear whether these changes are critical for the efficacy of high-impact exercise.
Here, we investigated the effects of mechanical stimuli produced by drop jumping on the middiaphyseal tarsometatarsus (TMT) in growing roosters. In previous studies using this animal model, running for 1 h/day exerted negative effects on TMT cortical bone morphology and biomechanics (23), whereas running for 15 min/day produced no adverse effects but failed to enhance bone growth (15). In this study, three specific research questions were asked: Does high-impact drop jumping produce a distinct mechanical milieu that significantly elevates mechanical parameters previously proposed to drive adaptation? Can 200 cycles per day of this mechanical milieu significantly enhance bone formation in this model? Does a site-specific spatial relation exist between a mechanical parameter and enhanced bone formation within the middiaphysis?
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Research design. Twenty-six 12-wk-old White Leghorn roosters were received (Starline Poultry) and were randomly assigned to strain-gauge (n = 6), jumper (n = 10), or control (n = 10) groups. Physes in rooster close at ~21 wk of age (18), but modeling at endocortical and periosteal surfaces continues beyond physeal closure (21). All roosters were housed in pairs (in 60 × 65 × 70-cm cages) and were given free access to tap water and feed. Roosters of the strain-gauge group were used to quantify the mechanical environment of the TMT during walking (0.51 m/s) and drop jumping. Roosters from this group had strain gauges attached and were recorded at ~16 wk of age. Roosters of the control and jump groups were injected with calcein (15 mg/kg iv) at 16 wk and 17 wk of age (6 days apart). Jumpers started the exercise training 1 day after the second calcein injection (day 0). For a jump, an operator lifted a rooster 50-60 cm off the ground and then moderately accelerated and released it. The acceleration served to increase the impact and to reduce variability across jumps. A thin piece of carpet served as landing mat to prevent slipping. All roosters were able to land safely on both feet. The loading (jump) frequency was ~1 Hz. The same person handled the roosters during the exercise protocol and during strain recordings to minimize variability in jump intensities. The first week of jump training consisted of acclimatization during which the number of daily drop jumps was gradually increased from 50 to 200. For the following 3 wk, jump roosters were subjected to 200 drop jumps per day after a schedule of 3 days on, 1 day off. Jumps were applied in sets of 50 with brief rest periods between sets. All roosters acclimated well to the training without negative side effects. Control roosters were subjected to simulated jumps without making contact with the ground. Qualitative observation revealed that there were no substantial differences in normal (cage) activity patterns between groups. Control and jump roosters were injected with tetracycline (20 mg/kg im) on days 21 and 28 of the protocol and were weighed on days 0 and 28. Roosters were killed with an overdose of pentobarbital sodium 72 h after the last tetracycline injection. All procedures were approved and closely monitored by the Animal Care Committee of the University of Calgary.
Determination of the mechanical environment.
Triple rosette strain gauges (FRA-1-11-1L, Tokyo Sokki Kenkyujo, Japan)
were attached to the medial, anterior, and lateral aspects of left
middiaphyseal TMTs in roosters of the strain- gauge group (13). At 24 h
after surgery, roosters were recorded during treadmill walking (0.51 m/s) and during drop jumps. Although habitual activities of roosters
are not limited to walking (mostly standing or lying, occasionally very
small jumps), slow walking provides an estimate of peak strain events
encountered during caged housing. Strain-gauge output was amplified
(model 2310, Measurements Group, Raleigh, NC) and sampled at 300 Hz for
10 s. This period covered the loading and unloading phase of several consecutive gait cycles or jumps (Fig. 1).
Before and after recording, gauge attachment and function were
confirmed separately for each gauge by subjecting the bone to a wave
ramp of bending and torsion. After recording, strain-gauge roosters
were euthanized, and strain-gauge positions as well as angular
orientations were determined from microradiographs.
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Histomorphometry. Left TMTs from control and drop jump roosters were used for histomorphometric analyses. TMT length was measured from the most distal phalange to the center of the proximal plateau (±30 µm). With a slow-speed diamond-wafer saw (Isomet Low-Speed Saw, Buehler, Lake Bluff, IL), a transverse section (300 µm) was cut at 45% of total TMT length measured from the proximal end. This site coincided with the plane at which the strain gauges were attached in roosters of the strain-gauge group and was considered as the functional middiaphysis. All sections were fixed in 70% ethanol and subsequently hand ground to 120 µm by using a 1,500-grit paper (wet). Sections were mounted on an epifluorescent microscope (×12.5). A 30° equal-angle star grid was etched into a plastic cover-slip and superimposed such that the center of the star grid coincided with the centroid of the section. Angular alignment was achieved by positioning the 0-180° line of the grid parallel to the anterior cortex (see Fig. 3, inset).
The percentage of single (sLS) and double labeled (dLS) surface with respect to bone surface (BS) was determined in each sector at both surfaces. Mineralizing surface (MS) was defined as (dLS + sLS/2)/BS (30). For the quantification of bone indexes, a video camera was used to capture the central portion of each sector (0.28 mm2) at both surfaces (24 images per section; see Fig. 2 for a sample image). Between week 17 and week 21 of age, bone accretion at the periosteal surface of the growing rooster TMT was facilitated by primary osteonal modeling and by lamellar bone formation leading to incongruent label surfaces (Fig. 2). Consequently, mineral apposition rate (MAR) at the periosteal surface was quantified as the ratio of bone area enclosed by the double label to its mean surface length (with time between the double labels as referent). Labels were traced with minimal operator-based bias by using custom software (19) that automatically identified the line of highest pixel intensities within the fluorochrome labels. In addition to calculating MAR on the basis of the calcein or tetracycline double label, MAR was also determined for the 4-wk time period between the second calcein label (start of jump protocol) and second tetracycline label (completion of protocol). At endocortical surfaces, bone apposition was lamellar in nature, and MAR was calculated by averaging the directly measured interlabel distances at 10 evenly distributed points (VIDAS, Kontron Elektronik, Munich, Germany). Bone formation rate (BFR) with BS as referent (BFR/BS) was calculated for each sector surface by multiplying MAR with dLS/BS. Changes in intracortical remodeling activity were not assessed due to the short study duration.Statistics. Body mass and histomorphometric measures were compared between the two groups with Student's t-tests. Paired t-tests were used to detect changes in body mass within groups, in BFR/BS between the two label periods, and in the mechanical milieu between treadmill walking and drop jumping. Differences in endocortical MAR between controls and jumpers were assessed via nonparametric Mann-Whitney U-tests. Simple linear correlation related the distributions of mechanical parameters induced by the two activities at both cortices (endocortical, periosteal) to each other as well as to the sites of morphological changes. Coefficients of determination (r2) were produced by using the mean values from each of the 12 sectors. Significance for all tests was P < 0.05. All data were expressed as means ± SE. The statistical software package SPSS 8.0 for Windows (SPSS, Chicago, IL) was used for data analysis.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Body mass and tibial lengths. Both jumpers and controls gained body mass during the protocol (P < 0.003), but body masses were not different between groups, either before (1,640 ± 40 vs. 1,670 ± 50 g) or after (1,830 ± 60 vs. 1,800 ± 50 g) exercise intervention. Drop jumping did not affect TMT longitudinal growth. Postmortem TMT length in jumpers was 94.8 ± 1.1 mm compared with 94.8 ± 0.9 mm in controls.
Mechanical milieu at the periosteal surface.
Drop jumps induced a highly nonuniform strain environment in the
middiaphyseal TMT. Maximal compressive strains (
2,070 ± 360 µ
) were engendered in the anteromedial cortex, and maximal tensile
strains (1,210 ± 250 µ) occurred in the posterior
cortex. These values were 30% (P < 0.04) and 40% (P < 0.03) greater than maximal strains recorded during slow treadmill
walking (Table 1). The distributions of
longitudinal normal strain across the middiaphysis were similar between
drop jumping and walking; the locations of the largest and smallest
magnitudes coincided for both activities (r2 = 0.94). When analyzed sector specifically, changes in absolute strain
magnitude ranged from 13% in sector 12 to +74% in
sector 10 (Fig. 3).
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/s) were 740% greater (P < 0.006) than those
produced by walking (Table 1). At the periosteal surface, the
distribution of peak strain rates was strongly associated with the
distribution of peak strain magnitude (r2 = 0.90).
Peak strain rates during walking were relatively uniform in
distribution and increased in a highly nonuniform fashion during drop
jumping (Fig. 4). The smallest increases
were observed at the lateral cortex (265% in sector 6),
whereas the anteromedial (905% in sector 3) and posterior
cortices (1,090% in sector 10) experienced the largest
increases. Consequently, strain rate distributions engendered by
walking and drop jumping were only moderately correlated (r2 = 0.64).
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/mm) were ~45% greater (P < 0.02) than
during walking (Table 1). Both peak circumferential and peak radial strain gradients were nonuniformly distributed during walking. Drop
jumping significantly increased these values only in those sectors
exhibiting large gradients. The largest circumferential strain
gradients were located at the medial (sectors 11-1) and lateral cortices (sectors 6-7), whereas the largest radial
gradients occurred at the anterior (sectors 2-4) and
posterior cortices (sectors 8-10).
Mechanical milieu at the endocortical surface. Maximal strain magnitudes and strain rates produced during drop jumping and walking were smaller at the endocortical surface than at the periosteal surface, whereas maximal circumferential strain gradients were similar at both surfaces. Specifically, values for maximal compressive strains produced at the endocortical surface during drop jumping were 28% lower than periosteal values (22% for walking); these differences were 31% (33% for walking) for tensile strains, 28% (17% for walking) for strain rates, and 1% (2% for walking) for circumferential strain gradients.
Despite lower peak magnitudes at the endocortical surface, the distributions of all mechanical parameters were strongly correlated between the two surfaces during drop jumping and walking; correlation values (r2) for middiaphyseal distributions during drop jumping (walking) were 0.93 (0.94) for peak strain magnitudes, 0.95 (0.77) for strain rates, and 0.95 (0.93) for circumferential strain gradients.Histomorphometry at the periosteal surface.
Both double fluorochrome labels covered the entire periosteal surface
in controls and jumpers (dLS/BS = 1). Thus values for MAR at periosteal
surfaces coincided with values for BFR/BS. BFR/BS measured in controls
and jumpers before exercise intervention did not differ in any sector
of the cortex; mean values for the periosteal surface were 4.6 ± 0.2 µm/day (controls) and 4.8 ± 0.2 µm/day (jumpers). After 3 wk of
jump training, BFR/BS was significantly elevated with respect to
control values at the medial (113%, sectors 12-1) and
posterior (39%, sectors 8-10) cortices (Fig.
5). When BFR/BS was calculated taking the
entire span of the 4-wk protocol into account rather than just the last
week, results were qualitatively similar (r2 = 0.83). Consistent with data from the second labeling period, the
largest differences in BFR/BS were detected in sector 1 (+52%), sector 8 (+39%), and sector 12 (+36%).
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Histomorphometry at the endocortical surface.
Unlike periosteal surfaces, which comprised continuous double calcein
and double tetracycline labels in all animals, endocortical surfaces
were only partially labeled (single or double labels) at either label
interval. During the first label interval, the percentage of
mineralizing surface with respect to bone surfaces (MS/BS) was,
averaged across all sectors, 58 ± 11% in controls compared with 55 ± 8% in drop jumpers). Particular
regions of the endocortical surface that consistently lacked
incorporated labels were not observed. There were no significant
differences in MS/BS between controls and jumpers in any sector.
Similarly, no significant differences in MAR and BFR/BS were detected,
either for the entire section or for any specific sector.
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Correlations at the periosteal surface.
At the periosteal surface, none of the mechanical parameters related to
drop jumping was significantly correlated with the absolute differences
in BFR/BS between jumpers and controls. Large differences in BFR/BS at
the medial cortex (sectors 12 and 1) occurred in
regions of large circumferential strain gradients, whereas altered
BFR/BS at the posterior cortex was associated with regions of large
tensile strains (sectors 8-10). Relating the absolute
difference in mechanical parameters produced by drop jumping and
running, rather than the values engendered by drop jumping, to
differences in BFR/BS also did not produce significant correlations
(Table 3). Similarly, using relative rather
than absolute differences in mechanical and histomorphometric
parameters or using absolute BFR/BS in jumpers did not significantly
enhance the correlations.
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Correlations at the endocortical surface.
At the endocortical surface, strain rates produced by drop jumping were
significantly associated with sites of the absolute increases in BFR/BS
(r2 = 0.44, P < 0.02; Fig.
7). Strain magnitude and strain gradients failed to generate significant correlations (Table 2). Correlating the
difference in mechanical milieus between drop jumping and running to
differences in BFR/BS produced a significant correlation only for
strain rate (Table 3). Correlations using relative rather than absolute
differences in BFR/BS did not render significance. Correlating absolute
BFR/BS measured in jumpers to mechanical parameters induced by jumping
led to significance for strain rate (r2 = 0.67) and
strain magnitude (r2 = 0.54).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Superimposing 200 daily drop jumps on normal daily activities led to significantly increased bone formation in the middiaphyseal TMT of immature roosters. Despite the short exercise duration of ~2.5 min/day, increases were substantial and nonuniform in distribution at both endocortical and periosteal surfaces. The mechanical environment induced by drop jumping involved large strain rates and was also highly nonuniformly distributed across the middiaphysis. At the periosteal surface, no single mechanical parameter accounted for differences in BFRs, whereas strain rate was significantly correlated with elevated BFRs at the endocortical surface. The osteogenic relevance of high strain rates was suggested previously with external loading models (24, 28, 40, 42), but ours uniquely related high strain rates to a potent osteogenic response in an exercise model of bone adaptation.
A critical component of this study was the determination of the
mechanical milieu of the TMT. Although we only quantified a few of the
many previously proposed mechanical parameters, strain magnitude and
distribution, strain rate, and strain gradients are among the principal
parameters that have been assessed experimentally. Peak strain
magnitudes and peak strain rates during treadmill walking were similar
to those reported from the TMT in adult roosters (12) and from the
human tibia (5). Few studies have measured bone strains during jumping.
The high strain rates induced by drop jumps were larger than ulnar bone
strains produced by dropping rats from a 30-cm height (0.1 /s) (25),
perhaps reflecting the additional acceleration used for our drop jumps
(14).
The middiaphyseal TMT of White Leghorn roosters has been used
previously to study exercise-related bone adaptation. Protocols involving high-speed running resulted in negative effects in 2- to
12-wk-old (23), 9- to 17-wk-old (15), and 30- to 39-wk-old (21)
roosters, particularly on periosteal bone formation. In contrast, drop
jumping in the present study increased periosteal bone formation,
consistent with the phenomenological observation that high-impact
exercise regimens may be more suitable for stimulating bone growth (2,
6, 7, 9, 27, 39). Comparing the mechanical milieus of drop jumping and
high-speed running revealed that drop jumping involved much larger
maximal strain rates (+256%, P < 0.006), similar
maximal strain magnitudes (+11%, not significant), and a smaller
number of loading cycles (less than 92%) than our previous
running protocols. This suggests that, globally (for the entire TMT
middiaphysis), strain rate was a critical factor for stimulating bone
growth. Whether the smaller number of loading cycles contributed to the
positive effect of drop jumping was unknown. Interestingly, the
osteogenic response occurred despite the extremely stable strain
environment of the middiaphyseal TMT during drop jumping; neither
changes in strain distributions (presumed to be prevalent in many
high-impact activities) nor large strain magnitudes were necessary to
stimulate bone growth. It is possible, though, that changes in either
or both of these mechanical parameters would have further increased the
osteogenic response.
Our analyses focusing on site-specific correlations within a bone section supported the importance of strain rate at the organ level. Peak strain rates induced by jumping were significantly correlated with the specific sites of bone formation at the endocortical surface where the largest differences between sedentary controls and jumpers were observed. Peak circumferential strain gradients that were generated close to the neutral axis could not explain differences in BFRs between jumpers and controls at any surface. That was consistent with data from the growing rat ulna model (25), in which increased bone formation induced by exogenous loading also occurred in regions of high strain rates (strain magnitudes) away from the neutral axis. In contrast, circumferential strain gradients have been correlated with specific sites of periosteal activation (bone formation) in the young adult avian skeleton (10, 13). One major difference between these models lies in the primarily bone-forming surfaces in growing animals and the primarily quiescent surfaces in adult animals. Osteocytes, as well as osteoblasts, bone lining cells, and osteoclasts, can be responsive to mechanical loading (17, 29, 46), and we speculate that the sensitivity of a BS to a specific mechanical parameter can vary with the presence or absence of specific bone cell populations and their level of activity.
One common aspect of strain gradients and strain rate is that both are related to fluid flow in bone, and fluid flow has been implicated in the process by which bone cell populations sense their mechanical environment (17, 29, 41, 44). The specific aspect of fluid flow to which cells are most responsive (e.g., flow volume, flow rate, or flow velocity) has yet to be determined. Very large strain rates may increase flow rate and velocity whereas diminishing flow volume due to limited bone permeability and decreased loading duration. If bone cells are sensitive to mechanisms that emphasize flow rate and velocity (e.g., maximal fluid shear stresses), then the moderately strong relation between peak strain rates and the sites of bone formation at the endocortical surface would be consistent with the premise that the transduction of mechanical stimuli from the tissue to the cellular level was mediated by fluid flow. Consequently, the integration of strain gradients and strain rate into a fluid flow related model could possibly explain the data from a great variety of experimental studies.
Strain rate was correlated with the sites of additional BFRs at the endocortical but not at the periosteal surface, although both surfaces qualitatively experienced similar mechanical milieus. In addition to the higher variability in BFRs (with respect to differences between controls and jumpers) and the different composition of bone cell populations and their levels of activity, the different bone type at the periosteal surface may have also played a role in the disparate results. Similar to bone formation in the rat ulna model (25), growth-related lamellar bone formation occurred at the TMT endocortical surface. The periosteal surface of the rooster TMT comprised a combination of lamellar and haversian bone, possibly giving rise to different bone fluid dynamics (22). Taken together, these data provide further evidence that searching for a single mechanical parameter that can consistently predict the specific sites of bone formation under a variety of physiological conditions may be too simplistic.
The response of growing bone to mechanical stimuli tends to dominate at either the endocortical (4, 23, 45) or periosteal surface (3, 25), likely reflecting differences in age, animal model, and the produced mechanical environment. In our study, relative differences in BFRs were larger at the endocortical than at the periosteal surface although mechanical stimuli were smaller in magnitude at the endocortical surface. This may be related to the greater potential of the endocortical surface to increase formation rates (or to attenuate decreases in formation rates) given that this surface was only partially forming bone and normal MARs were lower. Results from external loading models might argue against this hypothesis because woven bone growth has been observed at periosteal surfaces after a short period of stimulation. Nevertheless, this kind of exuberant bone growth has not been reported from exercise models featuring physiological loads. Alternatively, the differential response at endocortical and periosteal surfaces may have been caused by strain rate-related high intramedullary pressure leading to enhanced fluid flow at the endocortical surface. This hypothesis is supported by preliminary data indicating that fluid pressure at the endocortical surface increases with strain rate (31) and, spatially, decreases exponentially toward the periosteal surface (32).
The tenet that bone detects mechanical stimuli as the difference between a newly imposed mechanical milieu and the habitual mechanical milieu is generally accepted (34, 43). The specific mechanical signal(s) to which bone cells are receptive during habitual loading is, however, unknown. It is also unknown which specific bone cell population modulates biophysical stimuli in the immature skeleton and whether these stimuli supersede the signals responsible for normal growth. Consequently, it is unclear whether absolute values or differences (relative or absolute) in mechanical and histomorphometric parameters should be considered for the correlations. For instance, is it physiologically more appropriate to correlate specific parameters induced by jumping with the total rather than the relative differences in BFR between jumpers and controls? In our study, the mechanical milieu produced by jumping and differences in the mechanical milieu between jumping and walking led to similar correlation coefficients because, generally, the largest differences in a specific mechanical parameter spatially coincided with maximal values generated by jumping. Using relative rather than total differences in BFRs slightly decreased correlation values, whereas correlations increased when absolute BFRs produced by jumping were used. Despite these slight differences in correlative strength, strain rate was the prime mechanical parameter emerging from these analyses.
In summary, high-impact drop jumps created large peak strain rates in the presence of unchanged strain distributions and moderately increased peak strain magnitudes. The comparison between our previous running protocols and the current study indicated that the powerful osteotropic effect of high-impact drop jumping on the middiaphyseal TMT was primarily linked to the large increase in strain rate. Increases in BFRs at the endocortical surface dominated the adaptive response. The moderately strong correlation between the distribution of strain rates and the specific sites of increased BFRs at this surface, consequently, emphasized the sensitivity of growing bone to high strain rates. This information suggested that brief exercise protocols that maximize strain rates while keeping load magnitudes at physiological levels may be osteogenically highly effective.
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ACKNOWLEDGEMENTS |
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We acknowledge Connor Pardy for assistance with the strain measurements.
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FOOTNOTES |
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This study was funded, in part, by the Natural Sciences and Engineering Research Council of Canada and the Alberta Heritage Foundation for Medical Research.
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. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: S. Judex, Program in Biomedical Engineering, Psychology A, 3rd Floor, State Univ. of New York at Stony Brook, Stony Brook, NY 11794-2580 (E-mail: stefan.judex{at}sunysb.edu).
Received 22 November 1999; accepted in final form 11 February 2000.
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TOP
ABSTRACT
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MATERIALS AND METHODS
RESULTS
DISCUSSION
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