The involvement of musculoskeletal system and its influence on postural stability in children and young adults with cystic fibrosis
Kenis-Coskun et al. Italian Journal of Pediatrics
The involvement of musculoskeletal system and its influence on postural stability in children and young adults with cystic fibrosis
Ozge Kenis-Coskun 0
Evrim Karadag-Saygi 2
Yeliz Bahar-Ozdemir 2
Yasemin Gokdemir 1
Bulent Karadag 1
Onder Kayhan 2
0 Semsi Denizer Cad Dr Lutfi Kirdar Kartal Research and Training Hospital, Physical Medicine and Rehabilitation Department Istanbul , 34890 Istanbul , Turkey
1 Marmara University Medical Faculty Pediatric Pulmonology Department Istanbul , Istanbul , Turkey
2 Marmara University Medical Faculty Physical Medicine and Rehabilitation Department Istanbul , Istanbul , Turkey
Background: Cystic fibrosis (CF) affects the musculoskeletal system via a multifactorial pathway that includes vitamin D deficiency and involvement of respiratory muscles such as intercostals due to recurrent upper and lower respiratory tract infections. Eventual result is the deterioration of musculoskeletal health and posture in CF patients. Postural stability is directly affected by posture and can be compromised in every musculoskeletal problem. The aim of this study is to evaluate musculoskeletal system and postural stability in patients with CF. Methods: Patients with CF over six years of age and age and sex-matched control groups were included in the study. Cobb angle and thoracic kyphosis angles were measured on the spine radiographs. Both patients and control group were examined with pediatric gait, arms, legs and spine scale (pGALS). They also were evaluated with a NeuroCom Balance Master for their postural stability. Results: Fifty-one patients with CF and 94 healthy controls participated in the study. In results of the pGALS examination, CF group had significantly more pathological findings than the control group in lower extremity appearance and movement (p = 0.006 and p = 0.01) and spine appearance and movement (p = 0.001 and p = 0.022) domains. The tandem walking speed was significantly higher in controls with a mean of 24.45 ± 7.79 while it was 20.47 ± 6.95 in the CF group (p = 0.03). Various limits of stability parameters also showed significant differences. Medium correlations were found between musculoskeletal examination and postural stability parameters. Conclusion: In patients with CF, a systematic but simple musculoskeletal examination can detect pathologies, which are more frequent than the normal population. These pathologies show a medium correlation with the involvement of postural stability.
Cystic fibrosis; Posture; Postural stability; Musculoskeletal system; Spine
Cystic fibrosis (CF) is the most common autosomal
recessive disorder among individuals of European ancestry.
The life expectancy for CF has dramatically increased in
the recent decade with advancements in medical care
]. This increase in life expectancy has broadened the
span of morbidities in CF and started involving other
systems like musculoskeletal system.
The musculoskeletal involvement of CF is indirect,
usually seen with deformities of the spine as the disease
progresses. There is an increased incidence of scoliosis in
patients with CF. It has been shown in a previous study
that, among 316 CF patients the prevalence of scoliosis
was 15.6%, which is 20 times higher than the prevelance
of the area the research has been conducted [
]. The exact
cause is not clear; it is thought to be a result of the
combination of vitamin D deficiency, use of inhaled
corticosteroids and the strain on postural muscles as the
disease progresses [
]. Thoracic kyphosis also increases
due to decreased bone mineralization. These changes can
lead to musculoskeletal pain, such as persistant back pain,
especially in patients in adulthood. Chronic pain is yet
another added burden to this patient group, and may
exacerbate low mood and decrease motivation, therefore must be
prevented if possible . Various studies defined the spine
involvement in CF [
], but the number of studies
examining the entire musculoskeletal system is limited [
Postural stability is the ability to keep the center of
mass within the base of support in standing still and
during movement which is the combined effort of
sensory, motor and biomechanical systems [
pathologies involving any of these systems end up
disrupting the postural stability. There are two studies
investigating this relationship in fourteen adult patients
with CF [
]. The exact functional implications of
this spine involvement are not defined clearly, and the
data showing the involvement of postural stability and
its relationship to musculoskeletal health is scarce.
Using a standardized question and physical exam, we
hypothesized that the detected number of
musculoskeletal pathologies in patients with CF are higher than
typically developing children. Also, we hypothesized that
the musculoskeletal involvement affects the postural
stability parameters in patients with CF.
This study was conducted between February 2014–
December 2014 in Marmara University Physical
Medicine and Rehabilitation Clinic. The inclusion criteria
were the presence of a diagnosis of CF according to the
criteria depicted in Cystic Fibrosis Foundation 2008
consensus report [
] and being above six years of age.
Exclusion criteria were a history of an acute exacerbation and/
or internalization in an intensive care unit within the last
three weeks, history of a lung or liver transplant;
concomitant neurological, cardiovascular, metabolic, rheumatic or
vestibular diseases; physical disabilities impairing
locomotion; orthopedic problems and a history of
musculoskeletal system operations.
Among the cohort of 312 patients that are currently
followed by the clinic 78 were above the age of six. All
the patients were reached on the telephone and were
informed of the research eleven patients were excluded
due to their recent history of acute exarcebation, and
one patient was excluded due to a recent tibia fracture.
Fifty-one patients accepted to join the study. (Fig. 1)
This study was carried out in accordance with the
recommendations of Marmara Universtiy Ethical
Committee with written informed consent from the parents for
the patients under the age of 16 and the subjects above
16 years of age. All subjects gave written informed
consent in accordance with the Declaration of Helsinki. The
protocol was approved by the Marmara Universtiy
Age (years), height (metres), weight (kilograms), and
body mass index (BMI) (kg/m2) Z-scored were recorded
for the CF group. All the participants in the CF group
underwent spirometry and their FEV1, FVC, FEV1/FVC,
and PEF scores were recorded. All the measurements
and postural stability evaluations were done on the same
day. Patients were grouped according to their FEV1
levels as mild (above 70%), moderate (between 70 and
40%) and severe (below 40%) [
]. Patients with
25-OHvitamin-D levels below 30 ng/ml were labeled as vitamin
D deficient [
After the analyses of CF group have been finished, age
and sex matched controls without a history of
musculoskeletal and pulmonary pathologies who are referred to
us mainly by the nearby district schools for a routine
musculoskeletal examination were selected. The control
group was not derived from a pool but rather every
subject and their parents were asked to volunteer on a
personal basis and the controls that have accepted are
included in the study. Subjects in the control group
underwent heigh and weight measurements, pGALS
examination and postural stability assessment. They did
not undergo pulmonary function tests, blood tests or
received radiographs due to ethical considerations.
The participants were evaluated with pediatric Gait,
Arms, Legs and Spine (pGALS) system. pGALS
examination system was developed based on GALS in 2006. It
is a fast and efficient way of musculoskeletal
examination in school-age children [
]. The physician
performing pGALS (EKS) was educated about the system. It
includes three scanning questions and 17 maneuvers to
examine the upper extremity, lower extremity, spine and
temporomandibular joint. Pathologies were reported
according to movement and appearance [
The spine radiographs were taken for the CF group and
were evaluated with Surgimap® (Nemaris Inc. New York,
USA) system. Two blinded researchers (YBO and OKC)
measured the Cobb and kyphosis angles twice [
Thoracic kyphosis angle was measured between the angles of
the upper border of T4 and the lower border of T12
]. Scoliosis was defined as a Cobb angle of more
than 10 degrees [
]. Increased thoracic kyphosis were
defined as a kyphosis angle above 40 degrees [
Postural stability evaluations
The evaluations done with NeuroCom Balance Master®
(Natus Medical, San Carlos, California, USA) are as follows:
a) Modified (mCTSIB): Participants were required to
stand on a firm surface with eyes open and closed
for 30 s respectively. The same process was repeated
on a foam surface. The sway velocity (degrees/s) in
center of gravity (COG) was measured. Every
measurement was done three times, and the mean of
these measurements was used.
b) Limits of Stability (LOS): This test required participants
to transfer their COG toward eight targets spaced at
45° intervals around the body’s COG. Participants were
asked to keep their bodies in a straight line and use
their ankles as their movement axis to reach the
targets, which are preset according to the participants’
height. Participants were asked to reach each of the 8
targets separately. Target 1 was forward, 2 was
forward-right, 3 was straight right, 4 was backward
right, 5 was straight backward, 6 was backward- left, 7
was straight left and 8 was forward left. Target
placement takes into account the conversion of
the angular motion of leaning to linear movement
of the COG represented on the screen. Directional
control (DC), endpoint excursion (EPE) (percentage
of the distance achieved toward a target on the initial
movement), and movement velocity (MVL) (average
speed of COG movement based on the middle 90% of
the distance, measured in degrees per second) were
measured. The results of these tests were abbreviated
as DC1 meaning directional control forward, and so on.
c) Tandem walk: This test requires the participant to
tandem walk on the bold black line in the middle of
the platforms and wait until the testing ends at the
end of the line in tandem position. Step width (cm),
speed (cm/s) and end sway velocity (degrees/s) were
measured. The mean of three measurements was
d) Sit to Stand (STS): Participants were required to sit
on a wooden box placed on the platform with their
hands on the side and the legs closed. Then they
were asked to stand up on cue and stand for 5 s.
Tests were repeated three times. Weight transfer
time (seconds), weight transfer index (percent of
body weight) and sway velocity (degrees/s) were
measured and the mean of three measurements
With an alpha = .05 and power = 0.80, the projected
sample size has been calculated as approximately 40 subjects
for cystic fibrosis group and 80 subjects for the control
group for a between groups comparison of limits of
stability parameters to detect a 30% difference between groups.
SPSS for Windows 16 was used for statistical analysis.
Descriptive statistical methods like mean, standard
deviation and median have been used. In analyzing ordinal
data, means were compared by Student t test or
MannWhitney-U test according to the distribution of the data.
A level of p < 0.05 has been accepted as significant.
Fifty-one patients with CF and 94 healthy controls
participated in the study. There were no significant differences
in sex and age between groups (p = 0.331 and p = 0.8
respectively). In CF group there were 26 males and 25
females, and there were 52 males and 42 females in control
group. Ages, BMI Z-scores, vitamin D levels, FEV1 and
FVC values, treatment durations of the patient group are
given in Table 1 and the characteristics of the control
group are shown in Table 2.
FEV1 was inversely correlated with age (r = −0.524,
p = 0.001). FEV1 and FVC levels showed no
correlation with Cobb angle and thoracic kyphosis angle.
Cobb angles seem to increase with age (r = 0.326 p = 0.04)
while there were no correlations between age and thoracic
kyphosis angle. Forty-six of the patients (79.3%) had lower
levels of vitamin D. Vitamin D levels had an inverse
correlation with Cobb angle (r = 0.634 p = 0.04). BMI
Zscores did not show any correlation with vitamin D levels
when it is checked as a surrogate measure for nutrition.
Results of pGALS examination
As previously mentioned, pGALS examination consists of
two major parts: Scanning questions and musculoskeletal
examination. According to the results of scanning
questions, there was a significant difference between groups
only in answer to question ‘Do you experience difficulty
going up and down the stairs?’ (Table 3).
There were no differences between the groups in
upper extremity appearance and movement examination.
In all other parameters, CF group had significantly more
pathological findings (Table 4).
Six patients (10%) had pes planus, which was the most
common finding in patients. Other findings in patients
in lower extremities were genu varum (1 patient), genu
valgum (1 patient), genu recruvatum (2 patients) and
increased knee flexion during gait (1 patient).
Concerning the spine and postural examination in CF
patients, scoliosis in 10 patients (17%), increased
thoracic kyphosis in 5 patients (5.1%), winged scapula in 3
patients (5.1%) and asymmetry in trapezius muscles in 6
patients (10.3%) were found. In sub-group analyses,
there were no significant differences between genders
considering the results of examination (p = 0.15).
The musculoskeletal pathologies in the control group
were pes planus in 5 (5.3%), scoliosis in 3 (3%), increased
thoracic kyphosis in 1 (1.02%), winged scapula in 1
(1.02%) and asymmetry in trapezius muscle in 4 (4%) of
the participants. These pathologies also showed no
significant differences among genders (p = 0.14) or did not
show any correlations with age within the CF group.
Evaluation of spine radiographs
Measurements of kyphosis and Cobb angles had high
correlation between the two researchers (r = 0.99). Ten
patients had scoliosis (17.2%), eight had increased
thoracic kyphosis (13.7%). No vertebral fractures or other
vertebral defects were detected on radiographs. When
the diagnoses of scoliosis were compared between
pGALS examination and radiograph measurements,
there was a high level of correlation (r = 0.721 p = 0.001).
There were no correlations among FEV1 and scoliosis or
increased thoracic kyphosis. In sub-group analyses, the
presence of scoliosis did not show a significant
difference between males and females (p = 0.14).
Postural stability parameters
In mCTSIB test, there were no significant differences
between groups in sway velocity. Also, there were no
significant differences between groups in parameters obtained in
the walk across and STS test. There was an inverse
correlation between the angle of thoracic kyphosis and weight
transfer index of STS test (CC: −0.698, p = 0.01).
There was a significant decrease in the tandem
walking speed in CF group while there were no differences in
step width and sway velocity. Tandem speed correlated
with FVC (r = 0.6 p = 0.03).
There were no significant differences between reaction
times between the groups but reaction time negatively
correlated with kyphosis angle (r:-0.398, p = 0.016).
According to the results of the LOS tests, CF group
were significantly slower than the control group in going
right and going left back (trials number 3 and 6).
About the EPE values, CF group has traveled
significantly less in going forward and going forward-left (trials
1 and 7). There was a negative correlation between
kyphosis angle and the EPE value of the 6th trial going to
left backward. (r:-0.634, p = 0.04).
When CF and control groups were compared for
directional control, there were significant differences in
trials 1, 2 and 8, which are going forward, forward right
and going back (Table 5).
There were no correlations between the presence of
musculoskeletal abnormalities or the presence and
severity of scoliosis and thoracic kyphosis with other
There was no correlation between the vitamin D levels
and BMI Z-scores of the patients and the postural
stability parameters. In sub-group analyses, there were
no differences between genders in any of the postural
This study shows that there is an increase in
musculoskeletal pathologies in CF patients. There is also a slight
involvement of postural stability in children with CF,
albeit it is not a wide disparity as hypothesized in the
beginning. Moreover, the influence of these
musculoskeletal involvements in postural stability is present but the
correlation is not strong.
In this study, pGALS was chosen as it is a systematic
way of doing musculoskeletal examination in children
]. It was also aimed to scan not only the spine but
also the entirety of the musculoskeletal system to show a
more detailed picture of musculoskeletal pathologies.
Data was limited in the literature with children CF, with
only a couple of studies that has examined the whole of
musculoskeletal system [
]. The suggested reporting
method and the rapid way of applying the examination
make it quite useful but may have overlooked some of
the minor deficits. Even though, there are still significant
differences in CF group and control group. One of the
disadvantages of this method is that it may not be
considered objective enough since it is a musculoskeletal
examination without objective measurement tools or
cut-off values. To decrease this discrepancy, spine
radiographs were obtained and considered as the primary
measurements in diagnosing scoliosis and increased
thoracic kyphosis. There is a high correlation between
the examination and radiographs, which shows that
when in doubt, a physician should not deter from
ordering a spine radiograph. An unexpected side benefit of
using pGALS is that the scanning question ‘Do you
experience difficulty going up and down the stairs?’ can
differentiate normal children from patients with CF. It is
shown in this study that even if there is mild
involvement, exertional activities like taking the stairs are
significantly affected in children with CF when compared
to typically developing children.
This study has also shown a significant increase in the
incidence of scoliosis and thoracic kyphosis in patients
with CF concurrent with some of the previous research
2, 7, 8
]. However, there is not a correlation between the
presence of scoliosis or the increase in thoracic kyphosis
and lung function in this study. A recent review
investigating this relationship between posture and lung
functions in patients with chronic obstructive diseases also
resulted that the extent of alterations and its clinical
impact is variable in these patients. The reason may be the
lack of standard postural evaluations in the literature
]. The other musculoskeletal pathologies have not
been described previously. Most common pathology
defined in this study is pes planus. Possible reasons for pes
planus or other additional musculoskeletal pathologies
are still not clear and beyond the scope of this study.
This study has documented that in assessments of
postural stability, there is involvement in parameters of
tandem walk speed and various parameters of limits of
stability. Both are a part of dynamic stability, which
seems to be affected more prominently in patients with
CF. The direction of the movement that is affected is
not consistent. Rather various parameters in different
directions are affected. The device measuring postural
stability is chosen based on its objectivity and its ability to
detect minor changes in postural stability. It is known
that patients with CF have impaired skeletal muscle
oxidative capacity and this reduced skeletal muscle
oxidative capacity contributes to exercise intolerance in
patients with cystic fibrosis [
]. The involvement of
dynamic stability can also be the result of decreased
muscle oxidative capacity in patients with CF and can
explain the fact that various parameters are involved in
various tests. Therefore, future studies that can correlate
these involvements or show an intervention increasing
muscle oxidative capacity can improve postural stability
would be of value. At this moment however, the exact
clinical meaning of the involvement of postural stability
pattern is obscure. The angle of thoracic kyphosis seems
to be correlated with various postural stability parameters
and influence postural stability in patients with CF. No
other musculoskeletal pathology, neither the Cobb angle
correlated with postural stability.
The extent of the pulmonary involvement of the
patients and does not seem to contribute to the postural
stability parameters. The only correlation found between
lung capacities and postural stability parameters is the
correlation between FVC and tandem walk speed. It is
possible that functional capacity influences the speed of
movement rather than other postural stabilities, but the
exact clinical influence remains obscured in this setting.
The strengths of this study are the inclusion of all the
patients above the age of 6, giving a wider range of
patients, as opposing to the previous studies of similar
nature that investigate mainly adults. Also, this study is
about the full musculoskeletal examination of the
patients with CF, not the spine alone. The use of an
objective measure for postural stability is a plus, but to find
more reliable results; patient pool needs to be expanded.
As a limitation of this study, only 7 of the patients
MVL Movement velocity, EPE end point excursion, DC directional control
involved in this study had a severe involvement (FEV1
level below 40%). The obligation of involving
prepubertal and milder patients, so that postural stability
tasks could be performed, narrowed the patient pool.
This may have caused weaker correlations and has been
an essential drawback of the studies similar to this one
before, which leads to a selection bias and type II error
]. Furthermore, the pediatric pulmonology clinic that
provides the patient pool for our study consists mainly
of younger patients with only approximately 25% above
the age of six. In Turkey, the awareness for cystic
fibrosis has significantly increased in the last decade and it
has been added to the newborn screening program as
recent as 2015. Increased awareness will shift and expand
the patient pool. Genetic analyses for CF have also been
available in Turkey very recently. Patient pool of this
study did not usually had a genetic diagnosis, and a new
one could not be obtained due to lack of funding and
the limitations applied by the ethical committee. It is
becoming more widely available in the future and hopefuly
will help understand the relations of genetics with the
musculoskeletal involvement. Another limitation of this
study is that the association of musculoskeletal
impairments and other clinical pictures that can occur in CF
(i.e. the presence of diabetes) is not investigated. In the
future, another design, which can involve more patients
especially with more severe involvement, and
investigating the relation of a full clinical picture with
musculoskeletal involvement, may answer more questions on
In patients with CF, a simple but systematic
musculoskeletal examination can detect lower extremity and
spine pathologies, which are more frequent than the
normal population. They influence postural stability to a
certain level. However, exact causal relations need
further investigation to be determined.
Ethical approval and consent to participate
This study has been approved by the Ethical Committee of Marmara University.
All the subjects or their parents involved in the study gave their consent and
signed and informed consent form.
This study did not receive any funding from any organization.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from
the corresponding author on reasonable request.
Consent to publish
The patient pool and data of the cystic fibrosis patients were supplied by BK
and YG and they were involved in study desing and patient selection
processes. All clinical evaluations were performed by the same physician
(EKS) with a standardized patient assessment form and perofmed statistical
analyses of the study. OK performed the postural stability analyses provided
blinded assessments of spine radiographs, involved in the writing and editing
of the manuscript. YBO also assessed the spine radiographs and was involved
in the writing and editing of the manuscript. All authors read and approved the
The authors declare that they have no competing interests.
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