ORIGINAL
ARTICLE
E n d o c r i n e
C a r e
Vitamin D Status and Muscle Function
in Post-Menarchal Adolescent Girls
Kate A. Ward, Geeta Das, Jacqueline L. Berry, Stephen A. Roberts, Rainer Rawer,
Judith E. Adams, and Zulf Mughal
Imaging Science and Biomedical Engineering (K.A.W., J.E.A.), and Health Methodology Research Group (S.A.R.),
University of Manchester, Manchester M13 9PT, United Kingdom; Central Manchester Primary Care Trust (G.D.),
Longsight Health Centre, Longsight, Manchester M13 0RR, United Kingdom; Vitamin D Research Group (J.L.B.),
Medicine, University of Manchester, Manchester Royal Infirmary, Manchester M13 9WL, United Kingdom; Novotec
Medical GmbH (R.R.), D-75172 Pforzheim, Germany; and Department of Paediatric Medicine (Z.M.), Saint Mary’s
Hospital for Women & Children, Central Manchester & Manchester Children’s Hospitals National Health Service Trust,
Manchester M13 0JH, United Kingdom
Context: There has been a resurgence of vitamin D deficiency among infants, toddlers, and adolescents in the United Kingdom. Myopathy is an important clinical symptom of vitamin D deficiency,
yet it has not been widely studied.
Objective: Our objective was to investigate the relationship of baseline serum 25 hydroxyvitamin
D 关25(OH)D兴 concentration and PTH with muscle power and force.
Design: This was a cross-sectional study.
Setting: The study was community based in a secondary school.
Participants: A total of 99 post-menarchal 12- to 14-yr-old females was included in the study.
Main Outcome Measures: Jumping mechanography to measure muscle power, velocity, jump
height, and Esslinger Fitness Index from a two-legged counter movement jump and force from
multiple one-legged hops was performed. Body height, weight, and serum concentrations of
25(OH)D, PTH, and calcium were measured.
Results: Median serum 25(OH)D concentration was 21.3 nmol/liter (range 2.5– 88.5) and PTH 3.7
pmol/liter (range 0.47–26.2). After correction for weight using a quadratic function, there was a
positive relationship between 25(OH)D and jump velocity (P ⫽ 0.002), jump height (P ⫽ 0.005),
power (P ⫽ 0.003), Esslinger Fitness Index (P ⫽ 0.003), and force (P ⫽ 0.05). There was a negative
effect of PTH upon jump velocity (P ⫽ 0.04).
Conclusion: From these data we conclude that vitamin D was significantly associated with muscle
power and force in adolescent girls. (J Clin Endocrinol Metab 94: 559 –563, 2009)
T
here has been a resurgence of vitamin D deficiency among
infants, toddlers, and adolescents in the United Kingdom
(1– 6). Extremely low levels of 25 hydroxyvitamin D 关25(OH)D兴
(measurable parameter of an individual’s vitamin D status) in
adolescents cause nonspecific limb pain, lower limb and pelvic
deformities, tetany, and convulsions (4). In addition to these
symptoms, vitamin D deficiency can cause myopathy (4, 7),
which tends to be more marked in proximal muscles (8). Myopathy associated with vitamin D deficiency has been less well
studied (9). In children, myopathy can lead to nonparticipation
in physical education or organized sports. Muscles play a crucial
role in bone development and maintenance of their integrity (10,
ISSN Print 0021-972X ISSN Online 1945-7197
Printed in U.S.A.
Copyright © 2009 by The Endocrine Society
doi: 10.1210/jc.2008-1284 Received June 12, 2008. Accepted November 13, 2008.
First Published Online November 25, 2008
Abbreviations: BMI, Body mass index; Ca, calcium; EFI, Esslinger Fitness Index; 25(OH)D, 25
hydroxyvitamin D; JM, jumping mechanography; LJ, leg jump; P, phosphate; RCT, randomized controlled trial.
For editorial see page 418
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559
560
Ward et al.
Vitamin D and Muscle Function
11). Thus, chronic vitamin D deficiency might influence skeletal
development and mineralization though promotion of gastrointestinal absorption of calcium (Ca) and phosphorous, and ensuring optimal muscle action on the skeleton.
Jumping mechanography (JM) is designed to measure muscle
force and power by deriving measurements from an individual’s
ground reaction forces (12); the method has only recently been
introduced as a tool to assess muscle function, and has been
validated in children, athletes, and the frail elderly (13–15). The
proximal muscles required to jump (quadriceps, gastrocnemius,
soleus) are those most often affected in subjects with vitamin D
deficiency (8), and, therefore, JM provides a way of assessing
this. Compared with the more common functional techniques
used to assess proximal muscle function such as chair rising and
timed up and go, JM had the smallest short-term error, is least
influenced by learning effect, and had the largest interindividual
variation (14, 15). Using a dynamic measure such as JM might be
more functionally relevant than static measures such as isometric
or dynamic isokinetic tests (15).
Therefore, the aim of the current study was to use JM to study
the effects of vitamin D status, as reflected by serum 25(OH)D
concentrations on muscle function. Because vitamin D deficiency
leads to secondary hyperparathyroidism, the effect of serum
PTH on muscle function was also studied. The data used in this
study were collected during the screening phase of a double-blind
randomized controlled trial (RCT) of vitamin D supplementation in a group of girls at risk for vitamin D deficiency. The
specific pretrial hypotheses were that baseline serum 25(OH)D
concentration would be positively, and PTH concentration negatively, related to muscle power and force measured using JM.
Subjects and Methods
Participants
Participants attended an all girls, inner city multiethnic school in
Manchester, United Kingdom, and were being screened for inclusion in
a randomized trial of vitamin D supplementation. The school was chosen
because we had previously found that a high level (⬎70%) of individuals
had low 25(OH)D levels (⬍37.5 nmol/liter) without the presence of
symptoms (3). Inclusion criteria were that the girls were post-menarchal,
free from disabilities that precluded jumping, and that they did not suffer
from chronic childhood conditions.
The school doctor (G.D.) introduced the study to the participants. All
parents of girls, aged 12–14 yr, were then contacted by telephone (G.D.)
to discuss the trial and confirm whether their daughters could participate
in the RCT. Informed consent was gained from all parents and verbal
assent gained from participants themselves. The study received ethical
approval from Covance Clinical Research Unit Independent Ethics Committee and was registered with the European Clinical Trials Database
(EudraCT No. 2005-004729-25).
Anthropometric measurements
Standing height was measured using a microtoise (Chasmors Ltd.,
London, UK). Before jumping, weight was measured using the JM platform during quiet stance.
JM
Peak jumping power, jump height, and velocity were measured using
the Leonardo Mechanography Ground Reaction Force Platform, software version 4.1 (Novotec Medical GmbH, Pforzheim, Germany). Each
J Clin Endocrinol Metab, February 2009, 94(2):559 –563
participant performed three maximum countermovement jumps with
arms moving freely and at least a 60-sec rest between each jump. Each
jump was two footed, and participants were instructed to jump as high
as possible. The jump of greatest height was used for data analysis.
JM measures ground reaction forces (N), and by integrating these,
computes vertical velocity (m/sec) (16); power (kW) is the product of
force and velocity. Jump height (m) can be calculated from velocity (m/
sec) and time taken (sec) for jump. The Esslinger Fitness Index (EFI) is a
comparison of power per kg of body weight to an age and gendermatched reference population (15, 17) and is expressed as a percentage.
In children the reference population consisted of 312 individuals (177
females) from Germany (17). The precision, measured as coefficient of
variation, of muscle power measurement in adults is 3.6% (14) and
children 3.7% (17); peak jumping force 关from two leg jumps (LJs)兴 in
children was 8.9% (17).
Maximum voluntary force (N/kg) is measured from multiple one-LJs.
The participant is instructed to hop as fast and hard as possible, landing
only on the forefoot; data are expressed as force relative to body weight
(force times body weight). In this study one-LJ measurements were taken
on the dominant foot. Participants did three sets of one-LJ and the one
with highest force selected.
25(OH)D and PTH measurements
Nonfasting blood samples (5–7 ml) were taken at the same time as
jumping measurements to determine total 25(OH)D and PTH levels.
Serum was stored at ⫺20 C until measurement. Thawed samples were
whirly mixed, and 1 ml serum was taken for extraction of vitamin D
metabolites. Each sample was made up to 3 ml with 0.9% saline, and 20
␮l 25-hydroxy关26,27-methyl-3H兴cholecalciferol recovery tracer (TRK
655; GE Healthcare UK Ltd., Amersham Bucks, UK) was added to each
tube, mixed, and allowed to equilibrate for 30 min. After equilibration,
3 ml acetonitrile was added, and each tube was whirly mixed for 30 sec
before centrifugation at 2800 rpm, at 4 C for 15 min (Sigma Labs 4K15,
Shrewsbury, Shropshire, UK). One milliliter of distilled water was added
to each sample before application to C18 Sep Pak Cartridges (Waters UK,
Elstree, Herts, UK) preconditioned with 2 ml methanol and 5 ml water.
After application, cartridges were washed with 3 ml 65% methanol/
water before elution with 3 ml acetonitrile. Samples were dried down
under a stream of nitrogen and transferred to limited volume inserts using
HPLC column solvent. Samples were blown down again, and exactly 250
␮l column solvent was added to each vial then capped.
Separation of metabolites was by straight-phase HPLC (Waters UK)
run overnight using a 5 ␮m, 4.6 ⫻ 255-mm Hewlett-Packard Zorbax-Sil
Column (Hicrom, Reading, Berkshire, UK) eluted with hexanepropan2ol (98:2), and quantified by UV absorbance at 265 nm and
corrected for recovery. Run time for each sample was approximately 16
min, ensuring good separation. Sensitivity was 2 ng/ml and interassay
variation 6%. The assay laboratory is accredited to International Organization for Standardization 9001:2000 and International Organization
for Standardization 13485:2003, and participates successfully in the Vitamin D External Quality Assessment Scheme. Serum intact PTH was measured using the IDS intact PTH ELISA kit(Immunodiagnostic Systems Ltd.,
Boldon, Tyne and Wear, UK) normal adult reference range 0.8 –3.9 pmol/
liter, sensitivity 0.06 pmol/liter, and intraassay and interassay coefficients of
variation 4 and 6%, respectively (manufacturer’s values).
Serum concentrations of Ca adjusted for albumin and inorganic
phosphate (P) were measured using the Roche Modular P unit (Roche
Diagnostics, Ltd., Burgess Hill, West Sussex, UK). Reference ranges for
corrected Ca and P were 2.2–2.6 and 0.7–1.4 mmol/liter, respectively.
Data analysis
Baseline demographical and jumping details for the group are presented in Table 1. Pearson’s correlation coefficients were calculated to
determine the relationship between body habitus, serum 25(OH)D,
and PTH concentrations and jumping variables: muscle power (W),
velocity of jump (m/sec), jump height (m), EFI, and force per kg of
body weight (N/kg).
J Clin Endocrinol Metab, February 2009, 94(2):559 –563
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TABLE 1. Descriptive characteristics of the study population
a
Variable
Mean (SD) (n ⴝ 99)
Age (yr)
Body height (m)a
Weight (kg)
BMI (kg/m2)a
Total 25(OH)D (ng/ml)
PTH (pmol/liter)b
Corrected Ca (mmol/liter)b,c
Phosphorous (mmol/liter)b,c
13.5 (0.58)
1.58 (6.42)
57.2 (11.7)
23.0 (4.79)
11.6 (8.37)
4.87 (4.42)
2.29 (0.08)
1.20 (0.19)
Data missing in 15 of 99 girls (n ⫽ 84).
b
Reference ranges: PTH 0.8 –3.9 pmol/liter, corrected Ca 2.2–2.6 mmol/liter,
and P 0.7–1.4 mmol/liter.
c
Samples were hemolyzed in 16 of 99 girls (n ⫽ 83).
Preliminary exploration of the data indicated that serum 25(OH)D
and PTH concentrations were better represented on a logarithmic scale.
Due to basic physical relationships, the jumping parameters are related
directly to the amount of mass that is being moved in the jump, i.e. the
body weight. Simple normalization (as in, e.g. Refs. 14 and 15) forces a
particular relationship, and a priori it is unlikely that a simple linear
relationship will hold across the whole weight range. Therefore, the data
were adjusted for this effect by adding a weight function to the regression
model, and preliminary analysis indicated that a simple linear function
was indeed inadequate to represent the relationships of the jumping
variables with weight but that a quadratic function was adequate. Analysis of covariance adjusting for weight (as a quadratic function) was used
to determine whether vitamin D status 关log-transformed 25(OH)D or
PTH levels兴 affects muscle function. The effect of vitamin D was expressed as a slope per doubling of the serum 25(OH)D concentration. An
interaction between weight and 25(OH)D was also tested. To address
potential causal relationships, additional exploratory analyses, including body mass index (BMI) and height in the models 关both expressed as
age-specific SD scores relative to national standards (18, 19)兴, were performed but are not presented in detail.
Results
A total of 99 girls aged 12–14 yr participated in the study. Of
those, 68% (n ⫽ 67) were of South Asian origin (Indian Pakistani
and Bangladeshi), 12% were British Black (n ⫽ 12), and 20%
(n ⫽ 20) were white-Caucasian. All girls performed at least one
two-LJ or one set of one-LJ’s satisfactorily to allow their inclu-
561
sion in this study. None of the girls had symptoms associated
with vitamin D deficiency.
Table 1 summarizes the demographical details of the study
population; also included are summary statistics of the muscle
function data. Serum concentrations of Ca, P, and alkaline phosphatase were normal. Median serum 25(OH)D concentration
was 21.3 nmol/liter (range 2.5– 88.5), and PTH concentration
was 3.7 pmol/liter (range 0.47–26.2). Serum 25(OH)D concentration was positively, and weight negatively, correlated with all
outcome variables (Table 2). Body height was positively correlated with jumping height and power.
After correction for weight, there was a positive relationship
between 25(OH)D and velocity (P ⫽ 0.002), jump height (P ⫽
0.006), power (P ⫽ 0.004), EFI (P ⫽ 0.003), and force (P ⫽ 0.04)
(Table 3 and Fig. 1). There were no interactions between body
weight and 25(OH)D status.
In general the effects were somewhat smaller for PTH than
seen in 25(OH)D and failed to reach statistical significance in this
sample, although there was a significant negative relationship
between PTH and velocity of jump (P ⫽ 0.04) (Table 3).
The magnitude of these relations with 25(OH)D and PTH
was largely unchanged if we additionally control for BMI and/or
height, suggesting that the mechanism of action is independent of
both growth and obesity.
Discussion
We have used a novel outcome measure of JM to investigate how
skeletal muscle function in the lower limb is affected by vitamin
D and PTH status. Our data demonstrate that in a group of
asymptomatic post-menarchal adolescents, serum 25(OH)D
was positively related to muscle power, force, velocity, and jump
height; PTH had a lesser effect upon muscle parameters. We have
also confirmed the observations that there is an interdependence
of muscle function (force and power) with anthropometric parameters; in our data this was predominantly weight (13, 17).
Therefore, these data suggest that muscle contractility is affected
by the girl’s vitamin D status, those with low-serum 25(OH)D
concentration generated less power, and so jump height and velocity were lower than those with higher concentrations of
TABLE 2. Descriptive statistics and unadjusted Pearson’s correlation coefficient of functional muscle measures, demographical
and biochemical variables
Pearson’s correlation coefficients
Two-LJ
Power (kW)
Jump height (m)
Velocity (m/sec)
EFI (%)
One-LJ
Force (kN/kg)
a
Mean (SD)
Age (yr)
Body height (m)a
Weight (kg)
BMI (kg/m2)a
25(OH)D
(ng/ml)
PTH
(pmol/liter)
2.23 (0.43)
0.34 (0.07)
2.17 (0.23)
89.8 (16.2)
0.06
⫺0.13
⫺0.09
⫺0.17
0.44b
0.26c
0.18
0.19
⫺0.57b
⫺0.32b
⫺0.44b
⫺0.46b
⫺0.33c
⫺0.51b
⫺0.60b
⫺0.60b
0.22c
0.28b
0.31b
0.32b
⫺0.19
⫺0.08
⫺0.10
⫺0.16
2.83 (0.29)
⫺0.74
0.01
⫺0.34b
⫺0.31b
0.25c
⫺0.12
Data missing in 15 of 99 girls (n ⫽ 84).
b
P ⬍ 0.01.
c
P ⬍ 0.05.
562
Ward et al.
Vitamin D and Muscle Function
J Clin Endocrinol Metab, February 2009, 94(2):559 –563
TABLE 3. The effects of 25(OH)D and PTH upon muscle power, force, jump height, EFI and velocity after correction for weight
Parameter
Slope per doubling in 25(OH)D (95% CI)
P value
Slope per doubling in PTH (95% CI)
P value
Power
Velocity (m/sec)
Jump height (m)
EFI
Force (N/kg)
0.10 (0.04, 0.17)
0.066 (0.027, 0.105)
0.016 (0.005, 0.027)
4.15 (1.47, 6.84)
0.054 (0.000, 0.11)
0.003
0.002
0.005
0.003
0.050
⫺0.06 (⫺0.13, 0.01)
⫺0.04 (⫺0.08, ⫺0.002)
⫺0.01 (⫺0.02, 0.001)
⫺2.29 (⫺5.03, 0.46)
⫺0.04 (⫺0.10, 0.01)
0.120
0.040
0.087
0.100
0.12
CI, Confidence interval.
cle function, suggesting that it is more sensitive than the Gowers’
sign; this concurs with previous observations in the elderly (14).
There has been a resurgence of vitamin D deficiency in South
Asian and Middle Eastern girls living in the United Kingdom. Of
our screened population attending this school, 75% have low
25(OH)D levels (⬍15 ng/ml); we had specifically targeted this
asymptomatic population to see whether we could detect a subclinical effect of 25(OH)D on muscle function in these girls. In a
more 25(OH)D replete population, the association may differ;
we tested for a threshold effect (data not shown) in our population, but none was detected.
We used JM to assesses the maximal force developed in seconds;
this type of force is generated through anaerobic metabolism by the
type II fibers that are those responsible for fast anaerobic contraction (26) and those affected by vitamin D deficiency (27). We cannot
directly ascertain how 25(OH)D status affects muscle function in
our population. The mechanism is likely to be multifactorial due to
genomic (protein synthesis) and nongenomic (Ca and P transport)
effects of 25(OH)D’s active metabolite, 1,25 dihydroxy vitamin D,
which interacts with the vitamin D receptor. In a RCT of vitamin D
supplementation, El-Hajj Fuleihan et al. (28) observed an increase
in whole body lean mass (a surrogate measure of muscle mass) in
pre-menarchal girls who received the supplement. Thus, it is plausible that the better muscle function that we have observed is mediated through the effect of vitamin D on muscle mass. Finally, the
effects on muscle might be mediated through hypophosphatemia,
which occurs in vitamin D deficiency due to the secondary hyperparathyroidism (29). However, we did not observe any relationships between serum phosphorous concentrations and the
parameters measured by JM.
The main limitation of the current study is
that the data are cross-sectional, and, therefore, we cannot establish the temporal nature
of any of the relationships described. We cannot exclude any effect of body composition
(BMI or less likely height) from these data, or
whether the effects are due to a direct effect of
25(OH)D, or its metabolites, on muscle.
However, after adjusting for both BMI and
height in the model, the effect sizes differed
very little (data not shown), thus, suggesting
some effect of 25(OH)D on muscle (30, 31).
Finally, we did not measure 1,25 dihydroxy
vitamin D, the biologically active form of vitamin D, but others have reported that
25(OH)D is appropriate for the study of
FIG. 1. The positive relationship between 25(OH)D status and muscle power (left panel; P ⫽ 0.003) and
muscle (8).
force (right panel; P ⫽ 0.05), after adjustment for weight as a quadratic term.
25(OH)D. In this study the majority of girls had an EFI of less
than 100% (median 88%, range 36 –143%).
The majority of girls in our study have force less than 3 N/kg
body weight. Under normal circumstances, the maximum force
generated when jumping is approximately three to 3.5 times an
individual’s body weight (20). Given that the forces generated by
muscles drive bone development, our data suggest that the bones
are not being maximally loaded, which might affect the development of peak bone strength. We recently showed that South
Asians, who should have attained peak bone strength, had less
mineral content and thinner cortices than Europeans; this could,
in part, be due to the lack of optimization of muscle force-generating capacity during childhood (21).
PTH status may also contribute to myopathy associated with
vitamin D deficiency; patients with primary hyperparathyroidism often complain of muscle fatigue and weakness (22), and
show improved muscle strength after surgery (22, 23). Furthermore, an association between high-serum PTH levels and sarcopenia had been reported (24). However, Glerup et al. (8)
showed only small associations between muscle strength and
PTH concentration in individuals with poor vitamin D status. In
our population, PTH seems to have little effect upon muscle
function; there is a negative relationship with velocity of jump,
but no other parameters.
In the current study, none of the girls had symptoms of low
25(OH)D status, yet we have shown the effects of 25(OH)D
upon muscle function. We previously reported that the Gowers’
sign (25), used to detect proximal muscle myopathy in children,
was not related to 25(OH)D status (3). In other words, jumping
appears to be detecting a subclinical effect of 25(OH)D on mus-
J Clin Endocrinol Metab, February 2009, 94(2):559 –563
In conclusion, vitamin D status is significantly associated with
muscle power and force. These data highlight the importance of
vitamin D status on muscle function in adolescent girls. Suboptimal force might have implications for long-term bone development. The long-term implications of these observations require further study.
Acknowledgments
We thank the pupils and staff of Levenshulme High School for Girls for
participating in the study, Hans Schiessl and Harald Schubert (Novotec
Medical GmbH, Pforzheim, Germany) for loaning the jumping mechanography equipment, and, finally, Central Manchester and Manchester
Children’s University Hospitals National Health Service Trust for funding the study.
Address all correspondence and requests for reprints to: Dr. Kate
Ward, Nutrition and Bone Health Research Group, Medical Research
Council Human Nutrition Research, Elsie Widdowson Laboratory, Fulbourn Road, Cambridge CB1 9NL, United Kingdom. E-mail: Kate.
[email protected].
European Clinical Trials Database no.: EudraCT No. 2005004729-25.
Disclosure Statement: The authors have nothing to disclose.
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