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Mechanical Loading and Deloading on Human Bones. I. Vuori, A. Heinonen, ... training on bone mineral density (BMD, g/cm -2) and bone mineral content (EBMC ... weight, nutrition, and genetic influence could be minimized. Me~ods. Des~n. The study was a ...... to be expected, as BMD at that time was still near the base-.
Calcif Tissue Int (1994) 55:59-67

Calcified Tissue International

9 1994Spfinger-VeflagNew YorkInc.

Effects of Unilateral Strength Training and Detraining on Bone Mineral Density and Content in Young Women: A Study of Mechanical Loading and Deloading on Human Bones I. Vuori, A. Heinonen, H. Siev~inen, P. Kannus, M. Pasanen, P. Oja The UKK Institute for Health Promotion Research, P.O. Box 30, SF-35501 Tampere, Finland Received: 29 June 1993 / Accepted: 8 February 1994

Abstract. This s t u d y a s s e s s e d the effect of unilateral strength training at 80% one repetition maximum and of detraining on bone mineral density (BMD, g/cm -2) and bone mineral content (EBMC, g) in young women. Twelve female physiotherapy students trained their left limb by leg press an average of four times per week for 1 year followed by 3 months of detraining. Twelve students served as controls. Repeated bone measurements were performed by dual energy X-ray absorptiometry of the lumbar spine, femoral neck, distal femur, patella, proximal tibia, and calcaneus. The training increased the muscle strength of the trained limb, and the BMD of the same limb showed a nonsignificant but systematic increase in distal femur, patella, and proximal tibia, and in EBMC of the five measured limb sites (considered an index of the total osteogenic effectiveness of the training). Simultaneously, the muscle strength increased in the untrained limb as an evidence of cross-training effect. A corresponding small but systematic increase was also seen in BMD of this limb as well as in EBMC. After the cessation of training, leg extension strength was retained but BMD and EBMC of the trained and untrained limbs declined towards baseline values in 3 months. The BMD and EBMC values in the control group showed an increasing tendency during the follow-up but the changes were less than 1%. The differences of the changes in BMD and EBMC between the left and right limb in the control group, as well as between the same limb in the training and control groups were nonsignificant. The findings of this study indicate that unidirectional strength training, intensive enough to induce substantial strength gain, is not an effective stimulus to increase BMD and BMC in young, physically active women. The unilateral training model turned out to be feasible in these subjects, producing a definite cross-training effect in muscle strength and a trend of similar effect in BMD. Further development of the unilateral training model, and studies to test if training produces adaptation in nonloaded bones (i.e., a crosstraining effect), are also warranted. Key words: Bone mineral density - - Bone mineral content - - Unilateral strength training - - Females - - Dual-energy X-ray absorptiometry.

Correspondence to: I. Vuori

The adaptive response of bone to both the peak magnitude load and frequency of the load applied has been extensively studied. High peak magnitude load rather than repetitive loading of lower loads governs the structural adaptive response of bone [1-4]. This concept is consistent with the results of cross-sectional human studies showing that weight lifters have higher bone mineral density (BMD) than endurance athletes [5-9]. However, few studies have prospectively examined the effects of strength training on bone. Peterson et al. [10], Pruitt et al. [11], Notelovitz et al. [12], and Snow-Harter et al. [13] reported a trend towards greater BMD in young and middle-aged women after weight training. Studies on tennis players [14-16] and a study on rowers [17] suggest that the effects of loading on bone are site specific, that is, they are primarily detectable in the loaded skeletal sites. The long-term unilateral activity of regular tennis playing was associated with greater BMD in the playing arm than in the contralateral arm of tennis players [14-16, 18], the side-to-side difference being greatest in the humerus and smallest in the ulna [18]. However, the influence of unilateral training on bone has not been systematically evaluated with a prospective study design. The purpose of this study was, therefore, to determine the effects of a 12-month, unilateral, high-resistance strength training (80% of 1 repetition maximum, 1-RM) and 3 month detraining on BMD of lumbar spine (L2-L4) , femoral neck, distal femur, patella, proximal tibia, and calcaneus, and on bone mineral content (BMC) of the five lower limb sites in young women. Unilateral training was thought to be a valuable model to study the effects of mechanical loading on human bones, because through side-to-side comparison the effects of confounding factors such as age, gender, height, weight, nutrition, and genetic influence could be minimized.

Me~ods Des~n The study was a controlled trial including an exercising experimental group and a nonexercising control group. The training protocol consisted of 1 year of unilateral strength training of the left limb followed by a 3 month detraining period. The unilateral training was interrupted for June and July in the middle of the program because of the summer season. In order to follow the dynamics of the effects of training and detraining, we did strength and bone measurements on the exercise group in January (beginning of training), May, Au-

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60 Table 1. Anthropometric characteristics of the subjects a

Age, years Height, cm Weight, kg BMI, kg/m 2b Fat %c

Training group (n = 12)

Control group (n = 12)

21.0 167 58 20.8 23.4

22.0 167 61 22.1 24.8

(2.5) (5) (6) (2.4) (4.0)

(3.0) (8) (11) (3.3) (6.0)

a Means (SD)

b BMI = body mass index c Body fat was measured by a bioimpedance analyzer (BIA 106, RJL Systems Inc., Michigan, USA)

gust, and December (end of training), and March of the following year (end of detraining). For the controls, the measuring protocol was the same, except that there were no measurements in May.

Subjects A total of 32 healthy female physiotherapy students between the ages 19 and 27 years participated in the study. Seventeen volunteered to be included in the unilateral training group, and the other 15 served as nonexercising controls. The physical characteristics of the 12 subjects in both groups who completed the study are given in Table 1. The control subjects were slightly older and heavier but the age, height, weight, body mass index (BMI), and percentage of body fat did not differ significantly between the groups. The anthropometric characteristics did not change in either group during the study. Information on physical activity over the previous 3 years and menstrual history was obtained with a questionnaire. Previous and current calcium intake was estimated from approximate daily consumption of milk and cheese [ 19], obtained with a questionnaire. All subjects were fully informed of the study procedure and design as well as of any known health risks, and gave their informed consent. The study was approved by the ethical committee of our institute.

Maximal Isometric Strength Test Maximal isometric extension strength was measured separately for the right and left limb using a leg press dynamometer. The subjects sat on the dynamometer chair in an upright position with a 90 ~ knee and 90 ~ ankle flexion angle. The subjects pressed maximally against strain ganges (measurement range: 0-25 kN; Tamtron, Tampere, Finland) located under their feet. The signal representing the peak force was amplified and recorded by a voltmeter. Before the test, the subjects did three submaximal contractions for practice. The isometric strength was then recorded for three maximal efforts, and the highest value was used as the test score. The reproducibility of the strength measurements was determined before the study by testing 15 sedentary middle-aged women three times within 2 weeks. The day-to-day precision of the strength measurement expressed as a coefficient of variation was 5.4% [20].

Bone Mineral Measurements BMD (g/cm z) and BMC (g) were measured from five skeletal sites of both lower limbs, along with a BMD measurement from the lumbar spine (L2-L4) using a Norland XR-26 dual energy X-ray absorptiometric (DXA) scanner (Norland Inc, Forth Atkinson, WI, USA). The sites measured in the lower limb were the femoral neck, distal femur, patella, proximal tibia, and calcaneus (Fig. 1). For the measurements of the lumbar spine and femoral neck, the subject was positioned in a standard way as suggested by the manufacturer. For the knee measurement, the subject lay on her side with the lower limb of the same side fixed at a 60~ knee angle by two support blocks

at the anterior and posterior sides of the knee. The calcaneus was measured using the same subject positioning. Further details of the measurement procedures are given elsewhere [21]. In addition, the BMC values measured at the five limb sites were summed up (Y~BMC) for both limbs. The change in Y,BMC was considered an index of the total osteogenic effectiveness of the training. The in vivo day-to-day precision (coefficient of variation) of the BMD measurement in our laboratory was 1.7% for lumbar spine, 1.3% for femoral neck, 1.2% for distal femur, 1.0% for patella, 0.7% for proximal tibia, and 1.3% for calcaneus [21]. The scanner was calibrated daily according to manufacturer's instructions. According to daily measurements of a lumbar spine phantom, there was no significant machine drift during the study. The short-term precision of the BMD and BMC measurements was 0,5% and 0.6%, respectively, according to 30 consecutive measurements done with the phantom on the same day.

Training Program The training sessions consisted of unilateral (left limb) strength training using a leg press (Leg Press Frapp, Fysiotec Iuc, Outokumpu, Finland). This type of training provides high mechanical loading in the knee region [22, 23]. The subjects in the training group were asked to train their left limb five times a week for 12 months. The right limb was placed on a board in a relaxed position and it glided passively on the board during the loading of the left limb. In the middle of the program, the unilateral strength training was interrupted for 2 months due to summer vacations. During the first 2 weeks, the subjects in the training group accustomed themselves to the training. The initial load was 50% of 1-RM (i.e., performance with maximum weight that one can do once in good form). The initial training consisted of two to three sets of 10 repetitions in each set. After 2 weeks of training, the load was increased to 80% of 1-RM and the session contained five sets and 10 repetitions. Thereafter, the training was kept progressive by testing the 1-RM of each subject every week. The exercise load relative to 1-RM was adjusted accordingly. The initial 1-RM was 92 (35) (-+SD) kg and the 80% 1-RM training load 72 (27) kg. The training was individually monitored by an instructor once a week. Program compliance and other physical activities were controlled by a diary.

Statistical Analysis Changes in BMD, Y.BMC, and muscular strength at the end of the training are expressed as percentages of the baseline values. To estimate the intergroup differences of these changes, an analysis of covariance (ANCOVA) was used separately for both limbs (left versus left leg and r i ~ t versus right leg of the training and control group, respectively). The intragroup differences between the changes in the left and right limbs were also estimated using ANCOVA. The baseline values were used as covariates in these analyses.

Results

Program Adherence and Compliance A total o f 12 s u b j e c t s in e a c h g r o u p c o m p l e t e d t h e study. Five subjects from the exercise group dropped out for the following r e a s o n s : a n old k n e e p r o b l e m b e c a m e a g g r a v a t e d in o n e s u b j e c t , o n e s u b j e c t h a d a skiing a c c i d e n t in w h i c h h e r a n t e r i o r c r u c i a t e l i g a m e n t w a s r u p t u r e d , o n e m o v e d to ano t h e r c o m m u n i t y , a n d t w o s u b j e c t s lost i n t e r e s t in t h e study. T h r e e o f the 15 c o n t r o l s u b j e c t s m o v e d to a n o t h e r c o m m u nity a n d w e r e t h e r e b y lost f r o m t h e study. R e p o r t e d c o m p l i a n c e , d e f i n e d as t h e p e r c e n t a g e o f t h e c o m p l e t e d t r a i n i n g s e s s i o n s o u t of t h e p r e s c r i b e d s e s s i o n s a w e e k , was o n a v e r a g e 77% (3.9 t i m e s p e r w e e k ) in t h e exercise group. T h e total n u m b e r o f h o u r s s p e n t in all e x e r c i s e

I. Vuori et al.: Effects of Unilateral Strength Training on Bone Mineral Density

~

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v

% Fig. 1. Anatomic sites of the bone mineral measurements. The dimensions given are in millimeters.

and training during the 1-year period was 410 (194) in the training and 171 (86) in the control group. There was no significant association between the number of the total training hours and BMD at any site. The corresponding numbers of total weekly exercise and training sessions were 8 (5) and 4 (3). The amount, type, or intensity of other physical activities did not change in either group during the study period. There were no significant differences in the initial BMD values at any skeletal site between the subjects with different training history.

TRAINING LOADS 80% OF 1-RM kg 140

100

The subjects in both groups reported an average of five exercise sessions (e.g., walking, jogging, swimming, cycling, or aerobics) per week during the last year prior to the inquiry. None of the subjects had engaged in strength or power training. Questionnaire data of menstrual history indicated that none of the subjects was or had been amenorrheic. In the training group, five subjects had normal periods, seven had menstrual irregularities, and three used oral contraceptives. The corresponding numbers among the controls were 4, 8, and 11. The BMD values of the subjects with menstrual disturbances were not different from the mean values of the other subjects. In the training group, the estimated mean daily calcium intake from milk and cheese products was more than 800 mg in one subject, 500-800 mg in five subjects and less than 500 mg in six subjects. The corresponding numbers of subjects in the control group were 3, 9, and 0. The BMD values of the subjects with less than 500 mg daily calcium intake from dairy products did not differ from the corresponding mean values of the training group.

'

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Previous Physical Activity, Menstruation, and Calcium Intake

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Fig. 2. The change of the average training load (80% 1-RM) across time.

group. The intergroup difference (based on ANCOVA) was significant (P = 0.004). In the untrained right limb, the mean strength increase was 16% in the training group and 1% in the control group (P = 0.002). After the detraining period of 3 months, the mean strength was virtually unchanged in the training group (1% decrease in the left and 1% increase in the right limb). In the control group, muscular strength increased by 3% in both limbs.

BMD and ZBMC Table 2 shows the mean baseline BMD values and the ZBMC for the left and right limbs separately. The dynamics and percentage of change in the BMD and EBMC are presented in Figures 4-6.

Isometric Strength

Intergroup Differences

The 1-RM leg extension strength of the trained leg increased by 24 (26)%, from 92 (35) to 120 (42) kg during the 1-year period. The corresponding figure for the 80% 1-RM training load was 31 (26)%, from 72 (27) to 97 (33) kg. The change of the training load across time is shown in Figure 2. The dynamics and percentage change in the maximal leg extension strength of both groups are presented in Figure 3. In the left (trained) limb, the mean increase in muscular strength was 24% in the training group and 5% in the control

Lumbar Spine (Fig. 4). After the training, the spinal BMD had increased an average of 2.0% in the training group and 1.4% in the control group (P = 0.061). Femoral Neck (Fig. 5A). In the left (trained) limb, the BMD increased an average of 1.1% in the training group and 1.0% in the control group (P = .86). In the right limb, the mean increase was 1.9% in the training group and 0.6% in the control group (P = 0.46).

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I. Vuori et al.: Effects of Unilateral Strength Training on Bone Mineral Density TRAINING GROUP

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Fig. 3. Percentage of change in the maximal isometric strength (mean + SE) in the leg extension text. - I I - left limb; . . . I . . . fight UAR~ limb.

Table 2. Initial values of maximal isometric strength, BMD, and EBMC a Control group (n = 12)

Training group (n = 12)

Muscular strength (kg) BMD (g/cm- 2) L2-L4 Femoral neck Distal femur Patella Proximal tibia Calcaneus EBMC(g) a

Left limb (trained)

Right limb (untrained)

Left limb

Right limb

70.1

71.1

79.1

82.3

(13.4)

0.964 (0.117) 1.272 (0.165) 1.069 (0.155) 1.096 (0.145) 0.648 (0.093) 87.83 (13.52)

(13.4)

0.966 (0.099) 0.966 (0.099) 1.283 (0.183) 1.078 (0.161) 1.090 (1.143) 0.665 (0.110) 88.15 (13.65)

(13.4)

(16.8)

1.086 (0.101) 0.988 (0.128) 1.273 (0.117) 1.079 (0.104) 1.100 (0.126) 0.684 (0.076) 90.64 (10.05)

1.013 (0.134) 1.266 (0.122) 1.066 (0.089) 1.114 (0.107) 0.678 (0.0779) 91.62 (9.72)

a EBMC = sum of the BMC of the five measured leg sites; means (SD)

Distal Femur (Fig. 5B). In the left (trained) limb, the BMD increased an average o f 2.0% in the training group and 0.6% in the control group (P = 0.09). In the right limb, these changes were 1.1% and 0.7% (P = 0.65). Patella (Fig. 5C). In the left (trained) limb, the BMD increased an average of 1.6% in the training group and decreased 0.6% in the control group. This was the only significant (P -- 0.02) intergroup difference. In the right limb, the mean increase was 0.8% in the training group and 0.7% in the control group (P = 0.82). Proximal Tibia (Fig. 5D). In the left (trained) limb, the BMD increased an average of 2.2% in the training group and 0.8% in the control group (P = 0.19).iln the right limb, these changes were 2.2% and 0.1% (P = '0.005). Calcaneus (Fig. 5E). In the left (trained) limb, the BMD increased an average of 2.0% in the training group and 1.5% in the control group (P = 0.80). In the right limb, these values were 2.4% and 2.6% (P = 0.69). EBMC (Fig. 6). In the left (trained) limb, the EBMC increased an average of 2.7% in the training group and 0.4% in the control group (P = 0.10). In the fight limb, the mean change was 2.6% in the training group and 0.9% in the control group (P = 0,17).

Intragroup Difference The BMD and ZBMC changes in the left (trained) limb of the trained subjects did not differ significantly from those in the fight limb. Neither did the controls show any intragroup differences.

Detraining After the detraining period of 3 months, the BMD values of the training group almost returned to the baseline level, except in the femoral neck and calcaneus. In addition, the Y.BMC of both limbs decreased steeply.

Discussion

Bone adjusts to mechanical stress affecting it by altering its structure and density [24, 25]. It has been proposed that the load magnitudes (peak forces) are osteogenically more important than the number of repetitions [1-4, 26-28]. It is suggested that the remodeling of bone is related to " e r r o r signal" (the difference in the local strain caused by habitual and specific loading), and therefore the response is likely to be site specific [3]. The capability of bone to respond to mechanical loading is probably determined by a genetically controlled set point which is further modified by previous

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Fig. 4. Percentage of change in the BMD (mean + SE) of the lumbar spine (L2-L4) of the training group (-R-) and the control group (...um.--).

site-specific loading history and several biochemical factors [24, 25, 29]. This study was designed on the basis of the above principles and observations. The aim was to find out the effects of sufficiently long, frequently repeated (five times per week) site-specific mechanical loading on the BMD and BMC, each training session consisting of relatively few highintensity muscular contractions which loaded especially the bones of the knee region [22, 23]. In the leg press training, the principal effective forces are patellofemoral and tibiofemoral compression forces. In addition, tension on the quadriceps tendon and patellar ligament loads the patella [23]. The loading was applied unilaterally in order to test the usefulness of this training model, which offers potential advantages in terms of minimizing the effects of several confounding factors. In order to investigate the effects of detraining, the subjects were followed for 3 months after the cessation of the training. Preliminary observations indicated that the leg press training places high demands on the subjects in terms of exercise frequency and intensity. Therefore, the volunteer subjects were recruited from two classes of physiotherapy students accustomed to exercise and sports training. They tolerated the training well, as indicated by high adherence and low training-induced dropout rate. At the beginning of the study, BMD tended to be greater in the control group than in the training group. Several factors such as intergroup differences in age, weight, use of oral contraceptives, and calcium intake from dairy products could act in this direction. There were no differences in the training history of the groups. The BMD and XBMC changes during the 12-month experimental period were small in both groups. With one exception (left patella of the control group), all values tended to increase. This was probably due to continuing skeletal mat-

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uration of the young, healthy, physically active subjects. The possibility that the observed changes were due to machine drift was excluded by daily phantom measurements. The changes in BMD and EBMC of the trained leg were small and at most sites not significantly different from those of the contralateral sites. However, there was a trend of systematically greater continuing increase of BMD and EBMC in distal femur, patella, and proximal tibia of the trained leg. The lack of significant effect cannot be explained by inadequate training, because the documented compliance for a relatively long period (12 months) was good, and the leg extension strength of the trained leg increased by 24%. Nor can the lack of effects be explained by hormonal imbalance or insufficient calcium intake. In six training subjects, the daily calcium intake from dairy products was less than 500 rag, but their total calcium intake was likely to be greater. The subjects in both groups, and especially in the training group, had engaged frequently in endurance-type activities before the study and continued to do so without changes during the program. However, their BMD values were within the normal limits for their sex and age. This finding is in agreement with previous studies indicating that even longterm regular training in aerobic activities is not associated with substantially increased BMD [6, 7, 9]. In contrast, high BMD values have been measured in strength- and powertrained atheletes [5-9]. Thus, the bones of our subjects should have had sufficient adaptive potential to increase the BMD when exposed to intensive strain stimulus. The possibility that initially less active subjects might have shown greater response to training cannot be excluded. We feel that the main reason for the small effect of the training was the unidirectional characteristics of the loading stimulus. Even when the loading was high and progressive, and the subjects performed the press with about maximum speed, the training consisted of only unidirectional repetitions of knee extensions. This type of training probably did not produce sufficiently multidirectional "error signals" needed for positive bone adaptation. The cross-training effect on muscle strength in this, as in an earlier study [30], suggests that the nontrained limb cannot be considered as training-independent control unit. This notion is strengthened by the observation that the BMD tended to increase more in the bones of the right (nontrained) limbs of the training group than in those of the control group. This difference was even significant in the proximal tibia. Furthermore, the ZBMC change (considered to reflect the total osteogenic effect in the loaded bones) was about equal in the left (trained) and right legs of the training group, 2.7% and 2.6~ respectively. These changes tended to be greater than the corresponding changes in the control group, 0.4% (P = 0.10) and 0.9% (P = 0.17). The tendency for greater intragroup BMD differences in the training group compared with the control group may be due to chance, but neither should a possibility of a cross-training effect be excluded. Systemic effects of exercise on bones, i.e., increased bone density also in the nonloaded bones, have been suggested on the basis of cross-sectional studies [31-33], whereas exercise intervention studies have shown more controversial results [34-36]. The unilateral training model, in which symmetric bones of the same subjects are intensively loaded without inducing differences in weight bearing, has not been used in earlier studies. Further research testing the possibility of inducing transient or permanent cross-training effect on bone, as one type of systemic effect, is warranted. The training model used in this study seems suitable for that purpose. BMD has been shown to decrease after cessation [37] or decrease of training [38] according to the adaptation hypoth-

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Fig. 5. Percentage of change in the BMD (mean -+ SE) of the lower limb. - I - left limb; 9. . I . . . right limb. (A) Femoral neck, (B) distal femur, (C) patella, (D) proximal tibia, 'MARa2 (E) calcaneus.

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esis. Out observations are concordant with these findings. The BMD seemed to decline most in bones where the greatest decline of loading occurred (distal femur and proximal tibia). These BMDs approached the baseline level in 3 months. A similar pattern was seen in both legs of the trained subjects, and a lesser change and a lesser consistent pattern in the control group. These observations, although not reaching statistical significance in the inter- and intragroup comparisons, support our interpretation of the results: weak site-specific training effect and eventual cross-training effect. The lack of any tendency of decreased BMD following the 2-month training pause in the middle of the program was to be expected, as BMD at that time was still near the baseline, corresponding to the previous habitual loading status of the bones but probably stimulated to increase due to previous intensive training. In contrast to the tendency in BMD, the leg extension strength did not decrease after the cessation of the training. Two factors may contribute to this finding: the subjects continued to be physically active and engaged, e.g., in down-hill skiing, and most probably the maintenance of muscle strength requires less training than its acquisition [39, 40].

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MARa2 Fig. 5. Continued.

Most cross-sectional studies have shown significant correlations between bone density and the strength of the muscles influencing the respective bones [41, 42]. On the basis of the adaptation hypothesis, this is to be expected, especially when both the bone and muscle measurements are made in a relative steady state condition. However, the adaptive changes in bone density and in muscle strength during training and detraining follow different time courses, as shown in this and other studies [37, 43, 44]. Thus, the correlation between BMD and muscle strength, or between their changes, may be low if one or the other parameter is in nonsteady state condition due to training, detraining, or other reasons. In summary, the unilateral strength training program used in this study increased the muscle strength of the trained limb substantially and the BMD of the same limb showed a nonsignificant but systematic increase at several loaded sites. Simultaneously, the muscle strength also increased in the untrained limb indicating a cross-training effect. A corresponding, small but systematic tendency of increase was also seen in the BMD and Y.BMC of the same limb. After training cessation, the BMD of the most loaded sites of the trained limb and of the corresponding sites of the

66

I. Vuori et al.: Effects of Unilateral Strength Training on Bone Mineral Density TRAINING GROUP

CHANGE%

CHANGE%

CONTROL GROUP

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3

.......................................................................................

2

.......................................................................................

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Fig. 6. Percentage of change in the sum of the I 3 - - J A N 91

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untrained limb declined towards baseline values in 3 months. In the control group, the bone changes tended to be smaller and less systematic. The unilateral training m o d e l turned out to be feasible although it did not provide effective training stimulus for the b o n e s o f the young, fit subjects. F u r t h e r d e v e l o p m e n t of the unilateral training m o d e l to study the effects o f e x e r c i s e on bone in a well-controlled fashion, and to test the possibility o f cross-training effect on bone, is warranted.

DEC

AUG

13.

14. 15. 16.

References

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