Bone and Mineral, 20 (1993) 125-132 125

1993 Elsevier Scientific Publishers Ireland Ltd. All rights reserved. 0169-6009/93/$06.00
BAM 00531
Hi gh i nt ensi t y act i vi t i es i n y o ung wome n: site
speci f i c bo ne mas s ef f ect s a mo n g f emal e fi gure
skat ers
Charles W. Slemenda and C. Conrad Johnston
I ndiana University School of Medicine, Department of Medicine, 702 Barnhill Drive, Indianapolis, IN 46202
( USA )
(Received 10 March 1992)
(Accepted 8 September 1992)
Summary
We compared young female figure skaters, aged 10-23, with non-athletic control subjects to ascertain
whether there were differences in skeletal densities at various sites. We also compared other characteristics
of body size, including height, weight and percent body fat. Although the skaters were thinner and
significantly more likely to have oligo- or amenorrhea, they had similar skeletal densities at upper body
sites (spine, arms, ribs) and significantly greater densities in the pelvis and legs. These differences were
not evident until the mid-teens, however, suggesting that there is little l i kel i hood o f selection bias as the
cause of the observed differences.
Key words: Bone density; Intense physical activity; Amenorrhea
Introduction
Patterns of physical activity in the developed countries of the world have changed
markedly over the past 20- 30 years. Although there is considerable evidence that
the fitness levels of children have, on average, declined and that children have
become fatter [l ], there are subgroups of the population participating in extremely
intense activities at levels not before contemplated. Among women, participation in
competitive distance running, multiple-sport events (biathlons, triathlons), gym-
nastics, swimming and skating have all increased in recent years. The long-term
skeletal consequences of these temporal changes in activity patterns are not entirely
understood. Whereas, we have shown that moderate activity in children is associated
with increased skeletal mass [2l and others have reported that retrospectively ascer-
Correspondence to: Charles W. Slemenda, Dr.P.H., Indiana University Department of Medicine, 702
Bamhill Drive, Indianapolis, IN 46202, USA.
126
tained childhood activity is associated with greater bone mass in young women [3],
there are also clear risks associated with intense activities in young women when
these activities are associated with menstrual disturbances [4]. This contrast in the
effects of exercise on bone demonstrate the need to answer a number of questions
before a rational approach to exercise recommendations can be made. How much
activity is appropriate and beneficial? What types of activity yield the greatest
benefits? And which skeletal sites are most affected by specific activities? We have
attempted to address aspects of these questions with the study described below,
which compares groups with starkly contrasting activity patterns - - fairly sedentary
young women and regional and international caliber female ice skaters.
Met hods
Populations
All of the young women in these studies were between 10 and 23 years old and cauca-
sian. The sedentary group (n = 22) was recruited for a study of calcium absorption
and were aged 10-23 when measured (Table 1). Although some did participate in
casual athletics, none was involved in intense physical training.
The ice skaters (n = 22) were recruited through the Indiana World Skating
Academy, which conducts evaluation camps and training programs for all levels of
competitive skaters, including international caliber competitors. The skaters involv-
ed in this study were both regional and national/international level skaters, aged
11-23 and divided about equally in the three separate skating disciplines: ice
dancers, pairs skaters and individual competitors. The international caliber skaters
trained 25-40 h per week on average, nearly all of this time being spent in weight-
bearing activities on the ice. (Dance training was the only other activity to contribute
Tabl e 1
t-Tests comparing skaters to non-athletic comparison group
Vari abl e Skat er s Cont r ol s P- val ue
Age (years) 17.7 3.2 16.0 3.4 0.11
Age (first menses) 13.7 2.1 12.6 1.1 0.06
Hei ght (in) 62. 4 2.8 63.0 2.8 0.37
Wei ght (lbs) 111 16 117 21 0.22
Body fat (%) 18.7 5.4 24.3 6.0 0. 0004
Ol i gomenor r hei c a (%) 20 0
Amenor r hei c a (%) 20 0 0.01
Nor mal a (%) 60 100
Ar ms BMD 0.81 0.09 0.78 0.09 0.12
Ri bs BMD 0. 70 0. 06 0.67 0.08 0.08
Spi ne BMD 1.07 0.15 1.01 0. 14 0.08
Tr u n k BMD 0. 94 0.09 0.87 0. 10 0.005
Legs BMD 1.21 0. 14 1.10 0.15 0.005
Pelvis BMD 1.21 0. 14 1.06 0.13 0.0001
Tot al body BMD 1.13 0.11 1.07 0.11 0.02
aExcl udes pr epuber t al (n = 2 skat er s, n = 4 cont rol s).
127
more than 2 h per week for any skater). The top-level regional competitors were
slightly younger than the elite skaters, but generally aspired to compete at higher
levels. Their average training time was about half of the elite level skaters, but did
not differ qualitatively (i.e. virtually all training was skating).
Bone mass measurements
Total body bone mineral density (TBBMD) was assessed using dual-energy x-ray
absorptiometry (DXA) on a Lunar Instruments DPX-L (Lunar Corporation,
Madison, WI). This scan also yields values for soft tissue, including total grams of
fat and lean tissue, percent body fat (%BF) and percent lean tissue (%LT). The preci-
sion error of TBBMD (repeated scans of individuals separated by about 1 week) is
of the order of 1%; precision errors for total grams of fat or lean tissue are somewhat
higher (2-4%).
Each scan was analyzed and densities calculated for head, arms, legs, pelvis, trunk,
ribs and spine. Reliable reference data do not exist for head or ribs. In addition, head
densities can be affected by the presence of orthodontic appliances (which several
participants had) and therefore these two regions are not discussed further.
Other measurements
All subjects were questioned regarding the onset (age at first period) and frequen-
cy of menses (cycles in the last year) and the use of birth control medications (now,
ever, duration of use).
Information regarding training patterns was also collected from each athlete,
using questionnaires specifically designed to focus on the primary activities of
skaters. Additional questions regarding dance, weight-training and other activities
were included for all subjects. In addition to the scans, anthropometric data were
collected on the skaters. Subscapular skinfold thickness, calf circumference and
biacromial width were measured on each subject, using standard methods [5]. These
sites were selected based on our published work demonstrating independent and
significant associations between each of these measurements and skeletal densities
at multiple sites [6].
Calcium intake was assessed using a 14-item food frequency questionnaire which
we have tested in several populations and shown to be reproducible and which is
moderately correlated with 3-day diet diaries [7]. Mean calcium intake was 976
mg/day, but it did not correlate with BMD at any site (-0.12 < r < 0.02) and is
not further discussed.
Analysis
Between-group comparisons in BMD were made using unpaired t-tests. Because
of differences in age and body weight, adjusted differences in BMD were calculated
from general linear models which included age, weight and whether or not a person
was a skater.
Results
Table 1 compares the skaters to the non-athletic group. The skaters were older
(2 years) yet lighter, although not significantly so. There was a highly significant dif-
ference in the frequency of oligo- and amenorrhea between the groups, with 40% of
128
Table 2
Regression models predicting skeletal densities at selected sites, using age, weight
and skating status as predictors
Skeletal site Predictor Coefficient SE P-value
Arms Age +0.032 0.023 0.16
Age x Age -0.0007 0.0007 0.32
Weight +0.0023 0.0004 0.0001
Skating +0.0020 0.0174 0.91
Spine
Legs
Pelvis
Age +0.0768 0.0365 0.04
Age x Age -0.0018 0.0011 0.10
Weight +0.0031 0.0006 0.0001
Skating -0.0001 0.0279 0.91
Age +0.089 0.037 0.02
Age x Age -0.0024 0.0011 0.03
Weight +0.0035 0.0006 0.0001
Skating +0.059 0.027 0.04
Age +0.081 0.036 0.03
Age x Age -0.0022 0.0011 0.05
Weight +0.0032 0.0006 0.0001
Skating +0.121 0.028 0.0001
the skaters having some disturbance in normal menstrual patterns (P < 0.001) and
the skaters experienced menarche on average 1 year later than the non-skaters. BMD
was higher among the skaters with differences ranging between 3.8% (arms,
P = 0.12) and 14.1% (pelvis, P = 0.001), with generally greater differences in the
lower part of the skeleton.
Regression models were then constructed to address the question of whether there
were significant differences in BMD after correction for the above-noted differences
in age and weight (see Table 2). No significant effects of skating were observed for
upper body sites. However, there remained a significant effect of skating on lower
body densities (leg and pelvis). Adjustments for differences in percent body fat, age
at menarche or time since menarche, did not alter these results. Table 3 shows the
Table 3
BMDs, adjusted for weight and age, in skaters and non-athletic comparison group
Skeletal site Skaters Cont rol s P-value
Arms BMD 0.79 0.79 n.s.
Spine BMD 1.03 1.04 n.s.
Legs BMD 1.19 1.14 0.04
Pelvis BMD 1.20 1.08 0.0001
129
1 . 6
1.4'
1.2
1 . 0
0 . 8 -
0 . 6 -
NON-ATHLETES, PELVIS
A SKATERS, PELVIS
0
o o
o o
o+
o+
0
0
@
1.5-
1. 4-
1. 3-
1.2
ci
m
1. 1-
tu
-J
1.0 -~
0 . 9 =
0.8 -
0.7 -
1 1 1 1 1 1 1 1 1 8 1 1 2 1
10 11 12 13 14 15 16 17 1 19 20 1
AGE
B NON-ATHLETES, LEGS
SKATERS, LEGS
@
@ o
o
o
o o
: ; o
@ 0
: 0 0
0 o .

~ o
I I
22 23
I I I I I I I I I I I I I !
10 11 12 13 14 15 16 17 18 19 20 21 22 23
AGE
Fig. i Values of (A) pelvis and (B) leg BMD by age for skaters (dotted line, open circles, O) and
non-skaters (solid line, closed circles, O). The fitted lines are the regression of BMD on age and age 2,
determined separately for the skaters and non-athletic controls.
130
adjusted BMDs for arms, spine, legs and pelvis. After adjustment for age and weight
(and/or % body fat), leg and pelvis BMD were significantly higher in the skaters
(5.5% and 11%, respectively). Figures la, b show the actual leg and pelvis BMDs for
the skaters and controls by age (fitted line is the age and age-squared regression).
At both sites the skaters appeared little different from the controls until about age
15, at which time the slope for the skaters continues to increase while that for the
controls flattens.
We then examined factors which might influence BMD among the skaters.
Although the skaters with menstrual disturbances had lower densities (about 2%
depending on skeletal site) than normally menstruating skaters (pre-pubertal sub-
jects were excluded), these differences were not significant. We were also not able
to demonstrate differences between skating disciplines (e.g. individual vs. pairs
skaters). However, there was a trend toward lower BMDs among those who trained
more hours each week. Correlations between hours of training and BMD were be-
tween r = -0.40 and r = -0.45, depending on site. After adjustments for age (and
age-squared) there remained a significant negative effect of hours of training on leg
and pelvic densities in the skaters, despite the fact that these were the two sites with
the greatest differences favoring the skaters. Further adjustments for weight, percent
body fat, menstrual frequency and other factors did not substantially diminish this
association.
Discussion
This study was undertaken to address concerns regarding the frequency of menstrual
irregularities among this group of elite athletes and the proven potential of such
disturbances to diminish skeletal integrity [4,8]. These skaters, however, demon-
strated only small (about 2%) negative effects of menstrual irregularities on their
skeletons. Surprisingly, skeletal densities among the skaters were significantly
greater than densities in non-skaters in the lower part of the skeleton and not
significantly different elsewhere. A similar lack of detrimental effects in elite
oarswomen with irregular menses has been observed [9]. The likelihood of selection
bias in observational studies must always be considered, but in this case the dif-
ferences between skaters and controls are not evident among the younger skaters,
but seem rather to develop in later adolescence and young adulthood. This would
suggest that selection for skaters to be drawn from a population with greater skeletal
densities is less likely, since all of these skaters began training at very young ages.
The skaters are smaller and lighter than the non-skaters at all ages.
The potential mechanisms for increasing skeletal densities in ice skaters include
two prominent possibilities. The training of these skaters is intense and dominated
by repetitious practice of each aspect of their programs, including jumps, spins and
other elements. The jumps, which~are now the focus of competitive skating, involve
considerable impact upon the completion of each jump, with dissipation of the
energy from such jumps absorbed mainly in the muscles of the upper legs and hips.
Similarly, the transition into j umps (transferring the energy of stroking into jump-
ing) also requires the use of these same muscle groups and may produce similar
forces on the skeleton. Site specific positive effects on bone mass in elite athletes have
been reported for the forearms of tennis players [10] and parallel negative effects
have been observed in hemiplegia, comparing the affected to the unaffected limbs
[i l l .
131
It is unclear why the apparent skeletal benefits of skating do not emerge until the
mid-teens, since most of the skaters began competing at quite a young age. Although
this is reassuring in terms of the role of selection bias in these data, one could
speculate that the benefits of skating only accrue during the rapid growth process,
perhaps by extending the length of time during which skeletal modelling occurs. If
intense activity affects bone mass by slowing remodeling, then continued activity at
this level may be necessary to maintain the advantages noted. It is also not clear why
there was a tendency toward lower BMDs among those who spent the greatest
amount of time training, although this level of training may be associated with more
subtle disturbances in gonadal function [12], or alterations in other systems which
we could not measure.
The absence of a significant detrimental effect of disturbed menstrual patterns on
bone mass was surprising. The small (about 2%) deficit in those with menstrual
irregularities would not generally be cause for clinical concern and suggests that in-
tense weight-bearing activities may diminish the negative effects of these irregular-
ities on bone mass. However, caution in this regard is required. Few women, other
than professional athletes, have activity levels approaching those observed here.
Additionally, statistical power to detect modest differences in BMD (e.g. 0.05
g/cm 2) varied considerably. Although there was greater than 70% power to detect
differences between amenorrheic skaters and controls, there was only 40-50% power
to detect such differences within the skating group. Moreover, the frequency, intensi-
ty and nature of the activities of these skaters are unique and are certainly not possi-
ble for the vast majority of women. Finally, we have observed very low skeletal
densities in other female athletes whose activity patterns, while extremely intense,
differ in the extent of weight-bearing (e.g. elite triathletes), suggesting that there may
be characteristics unique to skating which yield the apparent substantial benefits to
some skeletal sites. Although these data are reassuring for this group of elite athletes,
persistent menstrual irregularities in those with more moderate exercise habits
should still be considered a cause for concern and clinical attention.
Acknowledgements
We would like to acknowledge the cooperation of the Indiana World Skating
Academy and the United States Figure Skating Association for their assistance in
facilitating the participation of the skaters in this study. This work is supported by
AG 05793 US Public Health Service.
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