Authors:

Katharina Kerschan-Schindl, MD
Eva Uher, MD
Stefan Grampp, MD
Alexandra Kaider, MSC
Abdel-Halim Ghanem, MD
Veronika Fialka-Moser, MD, PhD
Elisabeth Preisinger, MD

Osteoporosis

Research Article

Affiliations:
From the Departments of Physical
Medicine and Rehabilitation (KK-S,
EU, A-HG, VF-M, EP), Radiology
(SG), and Medical Computer Sciences
(AK), University of Vienna, Vienna,
Austria.

Reprints:
All correspondence and requests for
reprints should be addressed to
Katharina Kerschan-Schindl, MD,
Department of Physical Medicine and
Rehabilitation, University of Vienna,
1090 Vienna, Waehringer Guertel 1820, Austria.
0894-9115/01/8005-0351/0
American Journal of Physical
Medicine & Rehabilitation
Copyright 2001 by Lippincott
Williams & Wilkins

A Neuromuscular Test Battery for

Osteoporotic Women
A Pilot Study
ABSTRACT
Kerschan-Schindl K, Uher E, Grampp S, Kaider A, Ghanem A-H, Fialka-Moser V,
Preisinger E: A neuromuscular test battery for osteoporotic women: a pilot study.
Am J Phys Med Rehabil 2001;80:351357.
Objective: To examine the efficacy of a short neuromuscular test battery in
elderly women suffering from osteoporosis in accordance with the World Health
Organization criteria, with and without a history of fractures.
Reduced bone mass and a high likelihood of falling increase the risk of osteoporotic fractures. There is a need for neuromuscular tests to identify individuals at risk for falls and fractures.
Design: The women were assessed twice. Forty-two women, with a mean
age of 70.0 5.1 (SD) yr, completed the first assessment. The number of
postmenopausal fractures and the womens history with regard to agility and
falls were assessed. The women performed neuromuscular tests (one-leg
stance, tandem walk, and body sway); bone mineral density of the spine and
femoral neck were measured. For the follow-up assessment, 13.2 1.3 mo
later, 39 women were studied. The same outcome measurements were obtained at both evaluations.
Results: During the observation period, five women fell once and one woman
fell twice; there were only two vertebral fractures and no nonvertebral fracture.
Neuromuscular performance did not change during this observation period. The
median changes in bone mineral density between the two assessments were
clinically not relevant. A comparison between patients suffering from established
osteoporosis and osteoporotic patients without a history of postmenopausal fractures showed that both groups of patients did not differ with respect to age,
neuromuscular performance, bone mineral density, and fear of falling.
Conclusion: This neuromuscular test battery is a feasible and practical tool
because it is brief and economical to perform. However, its efficacy as a
predictor of fractures must be tested in additional studies with a long-term
follow-up and a larger group of subjects.
Key Words: Osteoporosis, Neuromuscular Performance, Bone Mineral
Density, Fractures

May 2001

Neuromuscular Test Battery for Osteoporosis

351

one mineral density (BMD), body

sway, and muscle strength are independent and powerful synergistic
predictors of the incidence of fracture.1 As reported on hip fractures by
Hayes and colleagues,2 falling, the
impact of force to bone, and bone
capacity play important roles in the
etiology of fractures. The risk of falling is also multifactorial. Documentation3 revealed that postural stability declines with age and that poor
postural stability has been associated
with frequent falling.4 An estimated
one-third of elderly people fall each
year.5
A fall in an elderly person can
lead to injury and loss of independence. One year after hip fracture,
40% of these patients are still unable
to walk independently, 60% require
assistance in one essential activity of
daily living, and 80% are unable to
perform at least one instrumental activity of living.6 However, falls may
not only break bones but also damage
self-confidence.5 The psychological
after-effects of a fall are also important; perhaps even more significant
than the acute injury, an intense fear
of falling limits a patients mobility
and independence. Tinetti et al.7 evaluated patient history including an assessment of this fear of falling. This
documentation comprised questions
concerning previous falls, their
causes and consequences, as well as
fear-related restrictions of daily life
and the subjects agility.
Thus far, most studies on the
subjects risk of falling profile evaluated the risk factors in a complex
manner; balance and gait, other diseases, regular medications, a potential history of previous falls, and race
were included in the analyses. With
the exception of bone densitometry,
there are no practical measures or
tests to predict additional nonvertebral fractures. Therefore, we performed this study to examine the efficacy of a new neuromuscular test

352

Kerschan-Schindl et al.

battery in osteoporotic women with

and without a history of fractures.

neighborhood (daily, at least three

times a week, or less than three times
a week).8

METHODS

Neuromuscular Tests

Subjects

One-Leg Stance. Static balance is

tested by standing on one leg with
the subjects eyes open. Testing is
repeated three times for each leg, alternating from left to right. The test
is timed andmodified according to
Suni and colleagues9 stopped if30
sec are exceeded. In all three tests, we
obtained the mean value for each leg
for statistical analysis.

All subjects were Caucasian

women, who had been postmenopausal for several years and were patients in the outpatient clinic of the
Department of Physical Medicine and
Rehabilitation, University of Vienna.
They had established osteoporosis or
osteoporosis without a history of
postmenopausal fracture according
to the World Health Organization criteria. The purpose of this study was
explained to the subjects. Informed
consent was obtained from all participants. The study protocol conformed
with the Declaration of Helsinki.

First Assessment
History. During the first assessment,
the subjects were asked about the
number of postmenopausal nonvertebral fractures. Agility and history, according to Tinetti et al.,7 were recorded. The women were asked
whether they usually spent at least 4
hr a day or 4 hr a day on their feet,
how often they fell on the floor, how
often they had nearly fallen during
the previous 2 yr, whether the falls
had occurred as a result of dizziness
or stumbling, and whether the falls
had caused any serious injuries (fracture, contusion/hematoma, or none).
A fall was defined as falling all the
way down to the floor or ground, or
falling and hitting the floor, ground,
or an object like a chair or a stair. A
near fall was one in which the subject caught herself before hitting the
floor, ground, or object. The women
were also asked whether they were
afraid of falling (yes, no) and whether
they allowed this fear to restrict their
activities of daily life (yes, no). The
level of mobility was assessed in
terms of a modified life-space diameter which groups subjects according
to how frequently they leave their

Tandem Walk. The tandem walk

along a line, 2 m long and 5 cm wide,
involves dynamic balance.10 In addition to timing, the number of errors
the subjects made were counted; an
error was defined as stepping off the
line, touching, or grabbing the examiner or an object, or taking steps with
the heel and toe visibly separated.
Body Sway. The coordinated stability
task, according to Lord et al.,11 measures the subjects ability to adjust
balance in a steady, coordinated fashion and simultaneously placing the
subject near or at the limits of his or
her equilibrium. A 40-cm rod extending anteriorly is attached to the subjects waist by a belt; a pen is affixed
at the end of this rod. The subject
stands in front of a table of adjustable
height; on top of this table is a piece
of paper, showing a convoluted
1.5-cm wide track. The subject is
asked to direct the pen at the end of
the rod through this track and adjust
his or her balance by bending or rotating the body without moving the
feet. Leaving the track is interpreted
as an error and the total error score is
calculated. All subjects were administered the test twice; the best result
was used for the assessment.
To ensure the best possible performance in neuromuscular tests,
subjects were always instructed to repeat the trial if they were disturbed
by external noise.

Am. J. Phys. Med. Rehabil.

Vol. 80, No. 5

X-Ray, Densitometry. Biplanar roentgenograms of the spine were used to

diagnose vertebral deformities caused
by fractures. Radiographic examinations of the thoracic and lumbar spine
were performed in all women. Depending on the amount of height loss, grading was performed as follows: Compression fractures were classified as
mild, moderate, or severe.12 Actual
BMD of the lumbar spine and the femoral neck was measured and the t score
was calculated for the lumbar spine
and femoral neck by dual energy x-ray
(QDR 4500, Hologic, Waltham, MA).

Treatment
According to the results of the
BMD measurements obtained during
the first assessment, bone-specific
medication was started or adjusted.
All women could voluntarily enroll in
a course for home exercise,13, 14
which included a warm-up period,
stretching exercises, and exercises for
improving posture and coordination.

Follow-Up
Approximately 1 yr later, the
women were called in for a follow-up
visit to obtain history.7 During the
first assessment, elderly women
found it very difficult to answer the
question regarding how often they
had experienced a near fall during
the last 2 yr; hence, this question was
eliminated during the second assessment. In addition to taking patient
history, in accordance with the
method of Tinetti and associates,7 we
assessed neuromuscular performance, the number of nonvertebral
fractures during the observation period, an x-ray of the spine, and BMD
of the lumbar spine and femoral neck
(dual energy x-ray). The follow-up xrays were evaluated using the same
procedure as during the initial assessment. An experienced radiologist
reviewed the old and the new x-rays.
The variables registered at baseline
and follow-up are shown in Table 1.
May 2001

RESULTS
TABLE 1
Variables
History of falling
Number of fractures
Neuromuscular function
One-leg stance
Tandem walk
Body sway
X-ray of the spine
Bone mineral density
Hip
Lumbar spine

Statistics
Normally distributed continuous
variables are described as mean
SD. The median values (quartiles) are
given to describe nonnormally distributed variables. The BMD differences between the first and second
assessments were calculated for all
patients who completed both measurements (n 36 subjects for the
hip; n 33 subjects for the lumbar
spine), and the median changes
(quartiles) are given for illustration.
For statistical analyses, the right and
left one-leg stances were summarized
by calculating the mean of the two
performances.
The changes in both BMD measurements and the results of neuromuscular tests between the first and
second assessments were analyzed
using Wilcoxons signed-rank test.
The Wilcoxons rank-sum test was
used to compare age, BMD measurements, and the results of neuromuscular tests obtained during the second assessment between the two
groups of patients with and without a
history of fractures. The 2 test was
used to compare the fear of falling
between the two groups of patients
with and without a history of
fractures.
P 0.05 was considered statistically significant. Statistical analysis
was done using the SAS software
(SAS System for Windows, version
6.12, 1996, SAS Institute, Cary, NC).

Forty-two women completed the

first assessment. Thirty-nine women
were followed-up during the second
assessment. Among the three women
who were lost to follow-up, one could
not be contacted, one had developed
cancer, and one refused to undergo
evaluation. The mean interval between these two assessments was
13.2 1.3 (SD) mo.
The participants characteristics
during the first and second assessments are shown in Table 2. The
menopausal age of the women was
48.5 4.5 (SD) yr. The most frequently taken bone-specific medication consisted of hormones, calcium
supplementation, and bisphosphonates. Twenty-three (54.8%) women
had a history of at least one nonvertebral fracture; we recorded one nonvertebral fracture (n 13 women),
two nonvertebral fractures (n 4
women), three nonvertebral fractures
(n 4 women), and five nonvertebral
fractures (n 2 women). The predominant sites of fracture were the
distal radius (33%); ankle (14%); hip
(9%); humerus, tibia, ribs, and toes
(7% each). Sixteen (38.1%) women
had suffered at least one vertebral
fracture. Seven of these women had
one vertebral fracture, four women
had two vertebral fractures, four
women had three vertebral fractures,
and one woman had four vertebral
fractures. During the follow-up period, there were no nonvertebral fractures; however, two vertebral fractures occurred. Both women who
experienced a renewed vertebral fracture had suffered previous vertebral
fractures. All vertebral fractures were
graded as mild or moderate intensity.
In accordance with the BMD measurements at the time of the first
assessment, 19 women were administered routine bone-specific medication or at least had their previous
medication adjusted. The median
BMD change from the first to the
second assessment was 10.5 [4; 34]

Neuromuscular Test Battery for Osteoporosis

353

TABLE 2
Participants characteristics
1st Assessment (n 42)

1nd Assessment (n 39)

69.9 5.1
16

70.9 5.2
27

Age, yr
Persons taking bonespecific medication
BMDhip (g/cm2)b
BMDhip (t score)b
BMDspine (g/cm2)b
BMDspine (t score)b

614
2.8
769
2.5

[559; 636]
[3.4; 2.6]
[705; 849]
[3.1; 1.8]

614
2.9
777
2.5

[576; 665]
[3.2; 2.3]
[721; 859]
[3.0; 1.7]

BMD, bone mineral density.

a
Mean SD.
b
Median [quartiles].

TABLE 3
History of falls and fractures

Persons with a history of at least one

fall during the preceding 2 yr/during
the observation period (%)
Persons with fractures caused by falls
Persons with fear of falling (%)
Persons with a feeling of restricting
daily activities because of fear (%)
Persons leaving their neighborhood
daily (%)

1st Assessment
(n 42)

2nd Assessment
(n 39)

20 (48)

6 (15)

6
21 (50)
15 (36)

0
16 (41)
8 (21)

9 (21)

16 (41)

TABLE 4
Neuromuscular tests

One-leg stance right (sec)

One-leg stance left (sec)
Tandem walkerrors
Body swayerrors

1st Assessment
(n 42)

2nd Assessment
(n 39)

20.8 [9.9; 28.0]a

18.3 [10.7; 27.9]
1 [0; 2]
2 [1; 7]

22.2 [10.6; 30.0]

21.6 [9.8; 30.0]
2 [0; 2]
2 [0; 6]

Median [quartiles].

(median [quartiles]) g/cm2 for the hip

and 9 [5; 28] g/cm2 for the lumbar
spine. The difference was statistically
significant for the hip (P 0.0174)
and not statistically significant for
the lumbar spine (P 0.0620). Two
women started the home exercise
program during the first assessment,
whereas 31 women had already
started the exercise course.

354

Kerschan-Schindl et al.

The participants agility and history, according to the method of assessment by Tinetti et al.,7 are summarized in Table 3. Table 3 shows
that just one woman spent 4 hr per
day on her feet. Twenty women had
fallen at least once during the 2 yr
preceding the first assessment. Only
six women had fallen in the period
between the two assessments; five

women had fallen once and one

woman fell twice. Except for one fall,
all of these falls were caused by stumbling. Six falls before the first assessment resulted in a fracture; all other
falls only caused hematomas. One additional fall was not included because
it was the result of a skiing accident;
because similar falls often happen
with younger people as well, this particular fall was not interpreted as a
lack of coordination. The fear of falling was present in 50% of the women
during the first assessment and in 41%
of the women during the second assessment. The number of women who
felt that their daily activities were restricted because of this fear of falling
was reduced from 36% to 21% during
the follow-up period. The number of
persons leaving their neighborhood every day almost doubled.
The results of the neuromuscular tests are summarized in Table 4.
Participants were able to hold the
stance on the left and right legs for
about the same time. The performance in the three different neuromuscular tests did not demonstrate
statistically significant differences between the two assessments.
Table 5 compares persons with
established osteoporosis and patients
without a history of postmenopausal
fractures, including vertebral and
nonvertebral fractures. No statistically significant differences in oneleg stance, errors made during the
tandem walk and body sway were registered between the two groups. Also,
their ages and BMDs did not show
group-specific statistically significant
differences. Although statistically
nonsignificant (P 0.20), 50% of the
women who had a history of fractures
were afraid of falling, whereas 29% of
the women without a history of fractures were afraid of falling .

DISCUSSION
This neuromuscular test battery
is a practical and feasible tool. The

Am. J. Phys. Med. Rehabil.

Vol. 80, No. 5

TABLE 5
Neuromuscular tests at second assessment for persons
with and without a history of fractures

Mean of right and left

one-leg, stance (sec)
Tandem walkerrors
Body swayerrors

Persons with History of

Fractures (n 22)

Persons without History

of Fractures (n 17)

18.8 [6.4; 30.0]

24.8 [17.2; 29.5]

1.5 [0.0; 2.0]

1.0 [0.0; 4.0]

2.0 [0.0; 2.0]

2.0 [2.0; 6.0]

Median [quartiles].

neuromuscular performance of 39
women with osteoporosis according
to the World Health Organization criteria did not change within 13 mo.
Within this follow-up period, only six
women fell and none of these falls
resulted in a fracture. Women with a
history of postmenopausal fractures
did not perform worse in neuromuscular testing than did women without a history of such fractures. Their
BMDs and the prevalence of the fear
of falling were also comparable.
The change in BMD of the hip
was statistically significant but not
clinically relevant. However, intensive and personal care may have accounted for this finding. During the
initial assessment, the womens
bone-specific medication was adjusted to the BMD. Additionally,
women could voluntarily participate
in a home exercise program. Besides
medical regimens, exercise is often
advised to reduce the risk of fracture.
A recent study15 showed that longterm recreational gymnastics improve muscular performance and
body balance, and increase bone mass
and bone size in the tibia.
The incidence of falls rises with
increasing age.16 In our study, all
falls but one were associated with an
environmental factor that may have
contributed to the fall, such as tripping over stairs, snow, or ice. Tinetti
et al.7 reported that a potentially contributing environmental factor was
found in 44% of persons aged at least
75 yr who had fallen. Falls may lead
May 2001

to fractures; however, although no

physical injury occurs, the shock of
falling can generate fear. Frequent
falls can carry a serious psychosocial
impact by inducing the fear of falling.
A great majority of elderly individuals
do not sustain serious physical injuries from falls. Despite this fact, a
high proportion of elderly people report the fear of falling. A study among
persons aged 75 yr showed that
nearly 50% of those who had previously fallen admitted having this
fear.7 In this study, the fear of falling
was admitted by nearly 50% of the
participants during the first assessment and by 41% during the second
assessment.
Elderly victims of falls may lose
confidence in their ability to engage
in routine physical and social activities, resulting in isolation.17 It seems
that the fear of falling, as well as the
restriction of daily activities because
of fear, were slightly reduced during
the follow-up period, whereas the
number of women leaving their
neighborhood every day increased
during the follow-up period. Therefore, it may be assumed that the participants self-confidence increased.
The reason may be that the investigator talked to the participants about
their neuromuscular performance.
Because they performed better than
did the participants of the majority of
previously cited studies, most of
them were told that they did moderately well. This may have increased
their self-confidence, leading to

changes in everyday life and, therefore, to changes in the history collected according to Tinetti and
colleagues.7
The one-leg stance, as performed
in this study, is a part of Suni and
colleagues health-related fitness test
battery for adults.9 In their study, it
was tested in younger persons aged
37 to 57 yr, who were able to hold
their position for a longer period (i.e.,
for 40 sec) than the patients in our
study. Nevitt and co-authors10 investigated the ability of elderly persons
to stand on one leg. They found that
in persons who could stand on one
leg for 2 sec, the risk of two or
more falls during the following year
increased by a factor of 1.6. Standingon-one-leg tests are considered to
have validity in relationship with falls
in the elderly. Gehlsen and Whaley18
found that static balance, as measured by the one-leg stance, is a factor that distinguishes elderly fallers
from the nonfallers. In our study, the
groups performed the one-leg stance
test as well as did Gehlsens and Whaleys subjects without a history of
falling.
Concerning the tandem walk,
Nevitt and co-authors10 reported no
absolute data; however, they established a risk profile for future falls.
Making at least eight errors while
performing the tandem walk is a risk
factor associated with two or more
falls during the next year. It increases
the risk of multiple falls by a factor of
2.2. Except for grip strength, none of
their investigated neuromuscular
tests are associated with the risk of a
single fall. In this study, no woman
made more than eight errors while
performing the tandem walk; only
one woman made eight errors during
the first assessment. She did not fall
during the follow-up period; during
the second assessment, she improved
by making 7 errors. Therefore, our
collective group of patients and subjects fared a lot better than did that of
Nevitt and co-authors. The reason
may be that Nevitt et al. only enrolled

Neuromuscular Test Battery for Osteoporosis

355

persons with a history of at least one

fall in the previous year, which was
not the case in our study.
Although the collective group of
Lord and co-workers11 was of the
same age as ours, our women performed much better in the body sway
than did the subjects in Lords group.
After 1 yr of exercising, including
special activities for balance and coordination, the women in our study
fared better than did the subjects in
the study by Lord et al. Lord and
colleagues did not investigate whether
this dynamic stability test could predict the risk of falling. Subjects in our
study performed very well in neuromuscular tests and they hardly fell
during the follow-up period. A few
participants fell and only one woman
fell twice. Therefore, they probably
were chance fallers and did not belong to a high-risk group such as
multiple fallers.19 This may be the
reason why we were unable to define
a potential risk ratio.
Comparing patients with and
without a history of fractures did not
reveal group-specific differences with
respect to neuromuscular performance or BMD. Copper et al.20 stated
that in patients 75 yr of age, there
was a steep increase in the relative
risk of fracture with reduced bone
mass but above that age the increase
in risk was small, and neuromuscular responses may be more important than bone mass. Probably, our
groups were too small to detect
group-specific differences. The same
may be true for the absence of statistically significant differences in the
fear of falling between the two
groups.
Bone fractures do not only depend on trauma and bone mass because factors other than bone mass
also contribute to the strength of
bone. Bone strength also depends on
a variety of qualitative aspects of bone
structure. These include its architecture, the amount of fatigue damage it
has sustained, and changes in its bulk
material properties.21 Biochemical

356

Kerschan-Schindl et al.

analysis of osteoporotic bone showed

changes in the properties of collagen.22 These aspects of bone quality
were not investigated in our study as
they cannot be measured by simple
bone densitometry. Therefore, it is
assumed that the differences in the
history of fractures, despite the missing differences in neuromuscular
performance and BMD, may be explained by the differences in the quality of bone.
The results of the three neuromuscular tests viewed separately reveal that a subject who performs well
in one test does not necessarily perform well in the other two tests. How
can this be explained? The three tests
measure different types of coordination. In the one-leg stance,9 the base
of support is reduced but the same
muscles serve as stabilizers during
the entire testing period, as the center of gravity is situated directly below the body. Contrary to this test,
dynamic movements perturb the center of gravity. The tandem walk10
challenges the subject to keep the
center of gravity within the area of
the feet and at the same time perform
a longitudinal movement with some
rotatory component. Across the gait
cycle, the muscle activity pattern
shows a phasic behavior. As a subject
performs the test of Lord et al.,11
the subjects feet are not moved
but his or her trunk is moved. Being
near or at the limits of his or her
equilibrium, the center of gravity is
projected outside the area of the
feet. During this test, the stabilizing
muscles are changing every moment
depending on the bodys actual position, and stabilizing is more strenuous when the body is near the limits
of equilibrium. Each of the neuromuscular tests measures a different
kind of coordination. This is important for planning an individual training program aimed at providing maximum protection from falling, with
exercises for specific coordination.
This study has several shortcomings. The sample size was small. As

the collective group was fairly agile

and performed well in the neuromuscular tests, their risk of falling and,
consequently, their risk of fracture
was lower than in previously published studies, such as in the collective study group of Tinetti and colleagues.7 Additionally, the subjects
found it difficult to recall the exact
number of falls during the previous
year. The accuracy of recalling falls in
the elderly is limited; however, it is
better for the preceding 12 mo than
for 3 or 6 mo.23 The investigators
urged the participants to recall incidents of falling as accurately as possible by suggesting various activities
of the participants and locations most
likely to be associated with falls.
Elderly persons require 10 to
15 min to complete this battery of
three neuromuscular tests. Because
all three tests evaluate different aspects of coordination, the entire test
battery should be performed and not
be replaced by just one of the three
tests. The complete test results will
enable the physician to customize the
patients ideal training program.

CONCLUSIONS
This study showed that the neuromuscular test battery is a feasible
and practical tool. Because the test
battery does not take long to complete, it should be possible to perform
the test battery within the daily routine examination. Another advantage
is that no expensive equipment is
required.
The results of this study suggest
that neuromuscular performance
does not change within 1 yr in
healthy elderly osteoporotic women
with no additional painful incidental
fractures during the follow-up period. Women with established osteoporosis did not perform worse in neuromuscular tests than did women
without a history of fractures. The
incidence of falls was too low to conclude whether these neuromuscular
tests are able to predict the risk of

Am. J. Phys. Med. Rehabil.

Vol. 80, No. 5

falling in the next year. Long-term

follow-up and a large sample size will
be required for an in-depth analysis.

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