Yoga and Bone Density
58
Journal of Exercise Physiologyonline
(JEPonline)
Volume 13 Number 4 August 2010
Managing Editor
Tommy Boone, PhD, MPH
Editor-in-Chief
Jon K. Linderman, PhD
Review Board
Todd Astorino, PhD
Julien Baker, PhD
Tommy Boone, PhD
Eric Goulet, PhD
Robert Gotshall, PhD
Alexander Hutchison, PhD
M. Knight-Maloney, PhD
Len Kravitz, PhD
James Laskin, PhD
Derek Marks, PhD
Cristine Mermier, PhD
Chantal Vella, PhD
Ben Zhou, PhD
Official
Research Journal of
the American Society of
Exercise Physiologists
(ASEP)
ISSN 1097-975
Systems Physiology – Musculoskeletal
Effects of Yoga on Bone Metabolism in Postmenopausal Women
LÍDIA BEZERRA1, MARTIM BOTTARO2, VICTOR MACHADO REIS3,4
LÍDIA ABDHALA5, RICARDO M LIMA2, SANDRA SOARES5, ADRIANA
FURTADO1, RICARDO OLIVEIRA2
1College
of Physical Education, Catholic University of Brasilia, Brazil,
of Physical Education, University of Brasilia, Brazil, 3University
of Trás-os-Montes and Alto Douro, Vila Real, Portugal, 4Research
Centre for Sport, Health, and Human Development, Portugal, 5SABIN
laboratory, Brazil
2College
ABSTRACT
Bezerra L, Bottaro M, Reis, VM, Abdhala L, Lima R, Soares S,
Furtado A, Oliveira, R. Effects of Yoga on Bone Metabolism in
Postmenopausal Women. JEPonline 2010;13(4):58-65. The purpose of
this study was to verify, in elderly women, the effects of Yoga on bone
biochemical markers (BBM) of formation (osteocalcin) and absorption
(carboxy-terminal collagen crosslinks, CTX), and estradiol hormone.
Forty eight post-menopausal women (63,9 ± 5,6 years old) were divided
into two groups: Yoga Group (YG, n = 24) and Control Group (CG, n =
24). The YG performed yoga three times per week (one hour each
session) for six months, while the CG was instructed to do not alter their
habitual daily routine. Bone mineral density (BMD), BBM and estradiol
hormone were analyzed before and after Yoga program by standard
procedures. A mixed factorial ANOVA was performed to verify intra and
inter group differences. A significant decrease in spinal lumbar and total
hip BMD for the CG was observed while only spinal lumbar BMD
decreased in the YG. Osteocalcin values increased in YG and
decreased in CG, while CTX values decreased in both groups. No
significant differences were observed for the estradiol hormone. It was
concluded that the yoga intervention failed to induce significant
improvements in post-menopausal women BMD, however, it was
capable of enhancing biochemical marker of bone formation as
measured by serum osteocalcin, thus suggesting an increased bone
turnover.
Key Words: Bone Static Stimulus; Bone Mineral Density; Bone
Biochemical Markers; Estradiol
Yoga and Bone Density
59
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 ± 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 ≥ 40kg/m2), 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
Yoga and Bone Density
60
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, São 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, São Paulo, Brazil), after
a voluntary deep inspiration. Body mass index (BMI) was calculated as body weight divided by height
squared (Kg/m2). 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/cm2) 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® , 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 ± 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
Yoga and Bone Density
61
sites. It was observed that the
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.
CG presented a significant pre to post intervention decrease in lumbar
Table 1. Descriptive data of subjects
Variable
Age (years)
Yoga Group (n = 24)
(mean  SD)
63.988  5.7
Control Group (n = 24)
(mean  SD)
65.3  3.9
Height (cm)
150.3  6.4
152.4  4.3
63.9  12.0
66.8  15.3
28.4  5.4
28.6  5.7
% Fat
41.6  7.2
40.9  8.9
Fat Mass (kg)
26.7  8.1
27.85  11.5
Lean Mass (kg)
36.4  5.7
37.6  4.6
Corporal Mass (kg)
Body mass index
(kg/m2)
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
Table 2. Comparison of BMD Between the Groups at Baseline (Pre) and After 6
month follow-up (Post).
BMD
(gcm2 )

Yoga (n = 24)
BMD.TB
Pre1.075  0.121
L2 – L4
0.984  0.190
Femoral
Neck
Wards
Triangle
Trochanter
0.843  0.172
Post1.072  0.115
0.959 
0.28
Control Group (n = 24)
Pre1.090  0.133
Post
1.084  0.129
0.56
2.55
1.021  0.227
0.836  0.182
0.84
0.870  0.128
0.865  0.132
0.58
0.675  0.177
0.666  0.185
1.39
0.677  0.177
0.669  0.178
1.19
0.738  0.139
0.736  0.134
Total Hip
FA.UD
0.175 *,†
0.989
0.235 *,†

3.14
0.28
0.789  0.160
0.772  0.166
2.16
0.915  0.169
0.910 
0.174†
0.55
0.970  0.161
0.954 
0.164†
1.65
0.288  0.061
0.291  0.058
1.04
0.287 0.055
0.282  0.054
1.75
Values are mean ± SD. Abbreviations: *; significant difference between pre and post-test (p < 0,05), †; significant
difference between groups (p  0,05), BMD; bone mineral density, L2-L4; BMD of lumbar spinal, Trochanter; BMD of
trochanter, FA.UD; BMD bone mineral of forearm ultradistal region.
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 and Bone Density
62
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).
Table 3. Biochemical markers and estradiol hormone pre and post test in both groups.
Variable
Yoga (n = 24)
Control (n = 24)
Pre
Post

Pre
Post

OC (ngml)
15.4  6.2
20.9  9.4*
35.3
16.20  7.0
14.2  6..6*†
-12.5
CTX (ngml)
0.35  0.18
0.32  0.26*
-8.3
0.45  0.13
0..243  0..206*
-46.4
Estradiol (pgml)
30.9  14.7
30.01  10.3
-2.6
28.2  13.7
24.84  8.7
-11.8
Values are mean ± SD. Abbreviations: *; significant difference between pre and post-test (p < 0,05), †; significant
difference between groups (p  0,05), OC; Osteocalcin, CTX; carboxy-terminal collagen crosslinks.
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
Yoga and Bone Density
63
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 Universitário Darcy Ribeiro. College of Physical Education.
Sala 53. Faculdade de Educação Física – Universidade de Brasília. Zipcode: 70910-900
Brasília / DF / Brazil; Phone: +55 – 61 – 8195-0132. rjaco@unb.br
REFERENCES
1.
Bassey E, Rothwell M, and Littlewood J. Pre and postmenopausal women have different bone
mineral density response to the same high-impact exercise. J Bone Miner Res 1998;19:18051813.
2.
Boyce B and Xing L. Regulation of bone remodeling and emerging breakthrough drugs for
osteoporosis and osteolytic bone metastases. Kidney Int 2003;63:2-5.
3.
Cussler E., Lohman T, Going S, Houtkooper L, Metcalfe L, Flint-Wagner H, Harris R, and
Teixeira P Weight lifted in strength training predicts bone change in postmenopausal women.
Med Sci Sports Exerc 2003;35:10-17.
4.
Ettinger B, Pressman A, Skalarin P, and Bauer C. Associations between low levels of serum
estradiol, bone density, and fractures among elderly women: the study of osteoporosis
fractures. J Clin Endocrinol Metabol 1998; 83: 2239-2243.
5.
Frost M. Muscle, bone, and the utah paradigm: a 1999 overview Med Sci Sports Exerc
2000;32:911-917.
6.
Garfinkel MS, Singhal A, Katz WA, Allan DA, Reshetar R, and Schumacher HR. Yoga-Based
Intervention for Carpal Tunnel Syndrome: A Randomized Trial JAMA 1998;280:1601-1603.
7.
Hayashi R, Okano H, and Hizuma H. The effects of walking at the anaerobic threshold on
vertebral bone loss in post-menopausal women. Calcif Tissue Int 1993;52:411-414.
8.
Hof R and Rabston S. Nitric oxide and bone. Immunology 2001;103:255-261.
Yoga and Bone Density
64
9.
Ivaska KK, Käkönen SM, Gerdhem P, Obrant KJ, Pettersson K, and Väänänen HK. Urinary
Osteocalcin as a Marker of Bone Metabolism. Clin Chem 2005;51:618-628.
10.
Johnell O and Kanis JA. An estimate of the worldwide prevalence, mortality and disability
associated with hip fracture. Osteoporos Int 2004;15:897-902.
11.
Kerr D, Dick I, and Prine R. Exercise Effects on bone mass in postmenopausal women are
site-specific and load-dependent. J Bone Miner Res 1996;11:218-225.
12.
Lanyon L and Rubin C. Static vs dynamic loads as an influence on bone remodeling. J
Biomechanics 1984;12:897-907.
13.
Lello S, Paoletti AM, Migliaccio S, and Melis GB. Bone markers: biochemical and clinical
significance. Aging Clin Exp Res 2004;16:33-6.
14.
Maïmoun L, Simar D, Malatesta D, Caillaud C, Peruchon E, Couret I, Rossi M, and MarianoGoulart D. Response of bone metabolism related hormones to a single session of strenuous
exercise in active elderly subjects. Br J Sports Med 2005;39:497-502.
15.
Marshall D, Johnell O, and Wedel H. Meta-analysis of how well measures of bone mineral
density predict occurrence of osteoporotic fractures. BMJ 1996;312:1254-1259.
16.
Notelovitz M. Overview of bone mineral density in postmenopausal women . J Reprod Med
2002;47:71-81.
17.
Nulend J, Bacabac R, and Mullender M. Mechanobiology of bone tissue . Pathol Biol
2005;53:576-580.
18.
Owroll S, Ferar J, Oviatt K, McClung M, and Huntington K. The relationship of swimming
exercise to bone mass, in men and women. Arch Intern Med 1989;149:2197-2200.
19.
Pavalko F, Chen N, Turner C, Burr D, Atkinson S, Hsieh Y, Qiu J, and Duncan R. Fluid shearinduced mechanical signaling in mc3t3-e1 osteoblasts requires cytoskeleton-integrin
interactions. Am J Physiol 1998;275:1591-1601.
20.
Robling A, Hinant F, and Burr D. Shorter, more frequent mechanical loading sessions enhance
bone mass . Med Sci Sports Exerc 2002;34:196-202.
21.
Rubinacci A, Covini M, and Bisogni C. Bone as an ion exchange system: evidence for a link
between mechanotransduction and metabolic needs. Am J Physiol Endocrinol Metabol
2001;282:851-864
22.
Sherman KG, Cherkin DC, Erro J, Miglioretti DL, Deyo RA. Comparing Yoga, Exercise, and a
Self-Care Book for Chronic Low Back Pain: A Randomized, Controlled Trial. Ann Intern Med
2005;143:849-856.
23.
Sinaki M. and Mikkebsen B. Postmenopausal spinal osteoporosis: flexion vs extension
exercise. Arch Phys Med Rehabil 1984;65:593-596.
Yoga and Bone Density
65
24.
Spirduso, WW. Physical Dimensions of Aging. Champaign, IL: Human Kinetics 1995,329357.
25.
Swezey R, Swezey A and Adams J. Isometric progressive resistive exercise for osteoporosis .
J Rheumatol 2000;27:1260-1264.
26.
Vincent K and Braith R. Resistance exercise and bone turnover in elderly men and women.
Med Sci Sports Exerc 2002;34:17-23.
27.
Vuori I. Dose-response of physical activity and low back pain, osteoarthritis, and osteoporosis.
Med Sci Sports Exerc 2001;33:551-586.
Disclaimer
The opinions expressed in JEPonline are those of the authors and are not attributable to JEPonline.
the editorial staff or ASEP.