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Effects of yoga on bone metabolism in postmenopausal women.

INTRODUCTION

Hypokinesia, irregular feed habits, poor calcium intake, lack of vitamin D and hormonal deficiency have been suggested as main factors contributing to bone mineral density (BMD) decrease in postmenopausal women (4,5,16). Conversely, physical exercise has been suggested for preserving, maintaining or increasing bone mass. Several studies have demonstrated the mechanisms by which physical exercise can affect the bone health in post-menopausal women (1,3,7,18,26). For instance, resistance training, walking, jogging, cycling, water exercises, vertical jumps and gym exercises have been studied in relation to bone physiology. However, it is not clear which physical exercise mode is the most effective to preserve bone mass (27).

Among the phenotypes that characterize bone mass loss, BMD has been reported as a good predictor for fractures risk (15). In fact, low BMD characterizes osteoporosis, an age-related disorder that represents a burden to public health costs (10). Bone densitometry is a static measurement of specific skeletal sites and it does not necessarily reflect the whole body bone metabolism (19). In that sense, bone biochemical markers have been suggested to provide a more dynamic measure of total body skeletal metabolism (15,17) and appear to be more sensitive to determine the bone response to a given intervention (14). Osteocalcin (OC) is a noncollagenous protein produced by osteoblastic cells during bone formation (8) while carboxy-terminal collagen crosslinks (CTX) is a marker of bone resorption (14). Both have been widely used to assess bone turnover (8,14,26).

It has been suggested that physical exercise has a pizoelectric effect on bone mass induced by dynamic way. Lanyon and Rubin (12) demonstrated that static tension is inefficient when compared to dynamic tension. On the other hand, Swezey (25), using a static, isometric and progressive training with a semi-inflated ball in post-menopausal women, observed a significant increase in bone alkaline phosphatase, a bone marker of bone formation. These data suggest that a static stimulus can activate progenitor cells of bone, stimulating bone formation and inhibiting bone resorption.

Yoga is a physical activity consisting of isometric movements that includes breathing exercise and meditation. It has been reported that this type of exercise is effective in improving function and reducing low back pain (22). Moreover, one study demonstrated that a yoga-based program was valuable in relieving some symptoms and signs of carpal tunnel syndrome (6). However, to date no study has attempted to examine the effects of Yoga practice on bone-related phenotypes such as BMD or biochemical markers. Since it has been previously reported that serum estradiol is an important determinant of skeletal remodeling in elderly women (4), it would also be interesting to examine the effects of Yoga on this hormone. Therefore, the purpose of this study was to verify the effects of a six-month Yoga program on biochemical markers (BBM) of bone formation (osteocalcin) and resorption (CTX), and estradiol hormone in postmenopausal women.

METHODS

Subjects

A total of 48 postmenopausal women (mean age of 63.9 [+ or -] 5.6 years) participated in the present study. Volunteers were recruited from a social work program developed by the University which offers physical activities, nutritional assessment and medical assistance to the neighborhood elderly population. Volunteers were physically independent according to the Spirduso's (24) classification. Exclusion criteria were as follows: recent fractures, osteoarthritis, previously diagnosed osteoporosis, uncontrolled hypertension, smoking and morbid obesity (i.e., body mass index [greater than or equal to] 40kg/[m.sup.2]), In addition, all subjects had not engaged in regular exercise for six months prior the study. Volunteers were instructed to not engage in any other training session and to keep their habitual daily activities throughout the study. After written informed consent was obtained from each participant, the sample was randomly assigned to one of two groups: Yoga Group (YG, n = 24) and Control Group (CG, n = 24). The study was conducted in accordance to the Declaration of Helsinki and all procedures were approved by the University Human Subjects Ethics Committee.

Procedures

Bone densitometry and Body Composition

Body weight was measured to the nearest 0.1 Kg using a calibrated physician's beam scale (model 31, Filizola, Sao Paulo, Brazil) with women dressed in light T-shirt and shorts. Height was determined without shoes to the nearest 0.1 cm using a stadiometer (model 31, Filizola, Sao Paulo, Brazil), after a voluntary deep inspiration. Body mass index (BMI) was calculated as body weight divided by height squared (Kg/[m.sup.2]). Measurements total body (TB), lumbar spine (L2-L4), femoral neck (FN), Ward's triangle (WT), trochanter (TR), total hip (Th) and forearm BMD (grams per square centimetres g/[cm.sup.2]) were performed using Dual Energy X-ray Absorptiometry (DEXA) in a Lunar DPX-IQ equipment (Lunar Corporation, Madison, WI). The DEXA scanner was calibrated daily against an aluminium spine phantom provided by the manufacturer and procedures were conducted by the same trained technician. The percent coefficients of variation for FN, WT, and L2-L4 BMD measurements were 2.4%, 2.2%, and 1.3%, respectively.

Bone Biochemistry

Biochemical markers of bone formation (osteocalcin, OC) and resorption (carboxy-terminal collagen crosslinks, CTX) were measured in serum by an eletrochemioluminescence immunoassay preformed on an automated analyzer (Elecsys 2010, Roche Diagnostics[R]' Mannheim, Germany). Estradiol hormone was evaluated by the same aforementioned methodology. Blood samples were collected from each participant and subsequently analyzed at baseline and after the six month intervention period. Intra and inter-assay coefficients of variation were respectively 3.84% and 6% for CTX, 2.21% and 3% for OC, and 9.2% and 4.4% for estradiol.

Yoga Program

Yoga was performed three times per week over a six month period. Each session lasted one hour and was divided into three parts; 1) five minutes of breathing exercises on the floor in a seated position and with crossed legs; 2) forty five minutes of Yoga postures (20 seconds in each posture); 3) five minutes of meditation followed by five minutes of relaxing on the floor in supine position. Participants who did not complete at least 80% of the sessions were excluded from analyses.

Statistical Analysis

Descriptive statistics was performed for all variables, which are expressed as the mean [+ or -] standard deviation. Independent-samples t test was used to examine baseline differences among groups for age, height, BMI, percent body fat, lean mass and fat mass. The effects of yoga on dependent variables (i.e, BMD, BBM and estradiol) were analyzed using a mixed factorial aNovA (time x group) where the within-subjects factors were the pre and post values and the between fixed factor was group (YG and CG). Statistical significance was set at an alpha level of p<0.05 and analyses were performed using the SPSS 14.0 software (Chicago, IL, USA).

RESULTS

The descriptive characteristics of both groups are presented in Table 1. Thirty volunteers began the Yoga program with twenty four satisfactorily completing the protocol, resulting in an adherence rate of 80%. Reasons for noncompliance included lack of interest and address alteration. No significant differences were observed between groups for age, height, body weight, BMI, percent body fat, lean mass, BMI or fat mass. No baseline significant differences were noted for any of the examined BMD sites. It was observed that the CG presented a significant pre to post intervention decrease in lumbar spine and total hip BMD while the YG exhibited a significant decrease only in lumbar spine BMD. As shown in Table 2, no pre- to post- significant difference was observed for the remaining BMD sites for both groups. No injuries were observed throughout the study.

No significant differences

were observed for OC, CTX or estradiol between groups at baseline (Table 3). However, ANOVA revealed that OC was significantly increased in YG while it was significantly decreased in CG, when comparing pre to post measurements. Moreover, a significant time x group interaction was noted and the post values were found to be significantly higher in the YG when compared to the CG. In relation to CTX values, both groups presented significant pre to post decreases, however, the percent change was considerably different between YG and CG (8.29% vs. 46.36%, respectively) and a significant time x group interaction was observed. No significant intra nor inter group difference was observed for the estradiol hormone and no significant time x group interaction.

DISCUSSION

Contrary to our expectations, lumbar spine and total hip BMD were significantly reduced after the study protocol for the CG and lumbar spine BMD significantly decreased in the YG. The Yoga exercises performed in the present investigation emphasized the specific bone locations that could

cause tension in the bone insertion, thus expected to induce a piezoelectric effect and subsequent stimulation of the bone progenitor cells. However, the examined intervention failed to elicit lumbar spine BMD preservation. These results may suggest that yoga training is an ineffective stimulus for restraining bone loss, but there are other factors that should be considered as follows.

Yoga exercises do not demand sudden movements and are performed at a slow and progressive rate. Some studies have demonstrated that static stimulus for bone tissue is inefficient to cause osteogenesis (12,20). However, it must be pointed out that these studies were performed in animals and the static stimulus performed for relatively long duration. In that sense, it has been suggested that human exercise programs aimed at maintaining bone mass are more effective if the stimulus is broken into smaller bouts separated by recovery periods (20). In addition, it was previously demonstrated that extension or isometric exercises might be more appropriated for patients with postmenopausal osteoporosis, since a higher number of vertebral compression fractures occurred in those who complied a flexion exercise program (23).

Bone densitometry (DEXA) is a static measurement of specific sites and it does not necessarily reflect the whole body bone metabolism (19). On the other hand, bone turnover markers provide a dynamic measure of total body skeletal metabolism (17,19). Although the Yoga stimulus employed in the present investigation has failed to elicit BMD improvements, it was able to induce significant changes in the measured bone turnover markers. While the CG has presented a significant decrease in osteocalcin (marker of bone formation) concentrations, the YG showed a significant increase in this variable over the study period. Osteocalcin is a bone specific protein produced by osteoblastic cells during bone formation (9) and its measurement has been widely used to asses bone turnover (13). Therefore, our findings indicate increased bone turnover following the Yoga intervention, which over time may lead to BMD preservation or improvement. The mechanisms underlying these observations were not addressed in the present study. It can be conjectured that the Yoga postures had produced bone stimulus such as hydroxyapatite crystals activation, generating electric charges which activated the osteoblastic cells and inhibited the osteoclastic cells (8,17,21). Future studies are important to elucidate such mechanisms and to examine the potential of a longer intervention period in reducing the rate of BMD loss in postmenopausal women.

According to Boyce et al. (2), the bone remodeling process occurs between 120 and 170 days. In our study, a similar period (six months) of Yoga intervention was able to increase osteocalcin and decrease CTX levels. Swezey et al. (25) demonstrated that static and progressive training in humans for a period of six months induced a significant increase in bone alkaline phosphatase and no significant alteration in the marker of resorption. Vincent and Braith (26) examined the effect of six months of low or high resistance training intensities in older individuals, and reported that minor changes occurred in BMD measurements; however, osteocalcin levels were increased by 25% and 39% for the low and high intensities, respectively. To our knowledge, no other study had attempted to examine the effects of yoga on bone-related traits, thus making specific comparisons difficult.

The bone static stimulus caused by Yoga practice could have reached the minimal effective tension threshold and increased osteoblastic cells recruitment by bone adaptation. Pavalko et al. (19) demonstrated that the osteoblastic cells reorganize its cytoskeleton in response to mechanic stimulus changing the cell mechanosensitivity, and accommodating the tension ambient. The Yoga practice could allow this reorganization of the cells mechanosensitivity, increasing the number of osteoblastic of bone matrix.

CONCLUSIONS

The results of the present study indicate that six months of Yoga practice failed to induce significant improvements in post-menopausal women BMD. Conversely, the intervention did increase concentrations of the biochemical marker of bone formation as measured by serum osteocalcin, while it remained unchanged in the control group. These findings suggest that Yoga can increase bone turnover in postmenopausal women, which over a longer period might lead to BMD maintenance. Future studies are required to test this hypothesis.

ACKNOWLEDGEMENTS

We would like to thank CNPq (Proc.478939/2003-5) and Catholic University of Brasilia for the financial support.

Address for correspondence: Campus Universitario Darcy Ribeiro. College of Physical Education. Sala 53. Faculdade de Educacao Fisica - Universidade de Brasilia. Zipcode: 70910-900 Brasilia / DF / Brazil; Phone: +55 - 61 - 8195-0132. rjaco@unb.br

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LIDIA BEZERRA [1], MARTIM BOTTARO [2], VICTOR MACHADO REIS [3,4] LIDIA ABDHALA [5], RICARDO M LIMA [2], SANDRA SOARES [5], ADRIANA FURTADO [1], RICARDO OLIVEIRA [2]

[1] College of Physical Education, Catholic University of Brasilia, Brazil, [2] College of Physical Education, University of Brasilia, Brazil, [3] University of Tras-os-Montes and Alto Douro, Vila Real, Portugal, [4] Research Centre for Sport, Health, and Human Development, Portugal, [5] SABIN laboratory, Brazil
Table 1. Descriptive data of subjects

Variable               Yoga Group (n = 24)     Control Group (n = 24)
                     (mean [direct sum] SD)    (mean [direct sum] SD)

Age (years)          63.988 [direct sum] 5.7    65.3 [direct sum] 3.9
Height (cm)          150.3 [direct sum] 6.4    152.4 [direct sum] 4.3
Corporal Mass (kg)   63.9 [direct sum] 12.0    66.8 [direct sum] 15.3
Body mass index       28.4 [direct sum] 5.4     28.6 [direct sum] 5.7
(kg/[m.sup.2])
% Fat                 41.6 [direct sum] 7.2     40.9 [direct sum] 8.9
Fat Mass (kg)         26.7 [direct sum] 8.1    27.85 [direct sum] 11.5
Lean Mass (kg)        36.4 [direct sum] 5.7     37.6 [direct sum] 4.6

Table 2. Comparison of BMD Between the Groups at Baseline (Pre) and
After 6 month follow-up (Post).

BMD                                  Yoga (n = 24)
(g~[cm.sup.2])
                           Pre-                       Post-

BMD.TB           1.075 [direct sum] 0.121   1.072 [direct sum] 0.115
L2-L4            0.984 [direct sum] 0.190   0.959 [direct sum] 0.175
                                              *, ([dagger])
Femoral          0.83 [direct sum] 0.172    0.836 [direct sum] 0.182
Neck
Wards            0.675 [direct sum] 0.177   0.666 [direct sum] 0.185
Triangle
Trochanter       0.738 [direct sum] 0.139   0.736 [direct sum] 0.13
Total Hip        0.915 [direct sum] 0.169   0.910 [direct sum] 0.174
                                              ([dagger])
FA.UD            0.288 [direct sum] 0.061   0.291 [direct sum] 0.058

BMD              [??]        Control Group
(g~[cm.sup.2])            (n = 2 [direct sum])

                                 Pre-

BMD.TB           0.28   1.090 [direct sum] 0.133
L2-L4            2.55   1.021 [direct sum] 0.227

Femoral          0.84   0.870 [direct sum] 0.128
Neck
Wards            1.39   0.677 [direct sum] 0.177
Triangle
Trochanter       0.28   0.789 [direct sum] 0.160
Total Hip        0.55   0.970 [direct sum] 0.161

FA.UD            1.04   0.287 [direct sum] 0.055

BMD
(g~[cm.sup.2])
                           Post             [??]

BMD.TB           1.084 [direct sum] 0.129   0.56
L2-L4            0.989 [direct sum] 0.235   3.14
                   *, ([dagger])
Femoral          0.865 [direct sum] 0.132   0.58
Neck
Wards            0.669 [direct sum] 0.178   1.19
Triangle
Trochanter       0.772 [direct sum] 0.166   2.16
Total Hip        0.954 [direct sum] 0.164   1.65
                   ([dagger])
FA.UD            0.282 [direct sum] 0.054   1.75

Values are mean [+ or -] SD. Abbreviations: * ; significant
difference between pre and post-test (p < 0,05), ([dagger]);
significant difference between groups (p 00,05), BMD; bone
mineral density, L2-L4; BMD of lumbar spinal, Trochanter;
BMD of trochanter, FA.UD; BMD bone mineral of forearm
ultradistal region.

Table 3. Biochemical markers and estradiol hormone pre and post test
in both groups.

Variable        Yoga (n=24)

                    Pre                 Post           [??]

OC                 15.4                 20.9           35.3
(ng [??]l)   [direct sum] 6.2    [direct sum] 9.4 *

CTX                0.35                 0.32           -8.3
(ng [??]l)   [direct sum] 0.18   [direct sum] 0.26 *

Estradiol          30.9                 30.01          -2.6
(pg [??]l)   [direct sum] 14.7    [direct sum] 10.3

Variable     Control (n = 24)

                    Pre                  Post            [??]

OC                 16.2           14.2 [direct sum]      -12.5
(ng [??]l)   [direct sum] 7.0      6..6 * ([dagger])

CTX                0.45                 0..243           -46.4
(ng [??]l)   [direct sum] 0.13   [direct sum] 0..206 *

Estradiol          28.2                  24.84           -11.8
(pg [??]l)   [direct sum] 13.7     [direct sum] 8.7

Values are mean [+ or -] SD. Abbreviations: * ; significant
difference between pre and post-test (p < 0,05), ([dagger]);
significant difference between groups (p 00,05), OC; Osteocalcin,
CTX; carboxy-terminal collagen crosslinks.
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Title Annotation:Systems Physiology--Musculoskeletal
Author:Bezerra, Lidia; Bottaro, Martim; Abdhala, Victor Machado Reis Lidia; Lima, Ricardo M.; Soares, Sandr
Publication:Journal of Exercise Physiology Online
Article Type:Report
Date:Aug 1, 2010
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