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Manual Therapy xxx (2012) 1e6

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Manual Therapy
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Original article

Can innominate motion be used to identify persons with ankylosing spondylitis?


A pilot study
Melanie D. Bussey a, *, Stephan Milosavljevic b
a
b

School of Physical Education, University of Otago, 56 Union Street West, Dunedin, Otago 9013, New Zealand
Centre for Physiotherapy Research, School of Physiotherapy, University of Otago, Dunedin, New Zealand

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 17 January 2012
Received in revised form
23 July 2012
Accepted 30 July 2012

Innominate movements during hip abduction and external rotation have recently been described in
healthy individuals. In the present study the aim was to determine whether these hip movement tests
could discriminate altered movement patterns in people with specic pelvic girdle pain (PGP) disorder.
This pilot study is the rst step in determining the usefulness of prone hip abduction and external
rotation in the differential diagnosis of PGP disorders. A cross-sectional comparison between a convenient sample of 6 individuals who had been referred for exercise and advice following diagnosis of
ankylosing spondylitis (AS) via a Medical/Rheumatological pathway and 18 healthy age and gender
matched controls. Transverse and sagittal plane innominate motion was measured using a palpation and
digitizing technique with a magnetic tracking device. Data analysis involved applying best-t equations
to the data and visual inspection of the produced graphs as well as conditional logistical regression for
each test position to determine our ability to predict group association. Graphical comparisons
demonstrate a distinction between the patients with AS and the healthy controls. Further, for all three
hip conditions the innominate angle was a signicant predictor of group association (p 0.002 for AB,
p 0.005 for AB ER and p 0.007 for ER).
2012 Elsevier Ltd. All rights reserved.

Keywords:
Sacroiliac joint
Ankylosing spondylitis
Kinematics
Pelvis

1. Introduction
The human pelvis provides a biomechanical bridge between the
spinal column and the lower limbs, acting as an intermediary in the
load transfer mechanism from the trunk to the legs, and vice versa.
During weight-bearing activities, control of the joints of the pelvic
ring is required for transference of loads between the spine and
lower limbs (Walheim et al., 1984; Jacob and Kissling, 1995). The
ability to effectively transfer load through the pelvis depends upon
an efcient load transfer mechanism which includes (a) optimal
function through the bones, joints and ligaments, (b) optimal
function of muscles and non-contractile connective tissue, and (c)
and well organised sensory-motor control mechanisms
(Hungerford et al., 2003). Disturbance in this load transfer mechanism has been identied as a risk factor for pelvic girdle pain and
injury (McGill, 1987; Damen et al., 2001). Pelvic girdle pain (PGP)
disorders are sub divided into specic, i.e. those with a clearly
identied pathoanatomical basis: such as inammatory pain
disorders of the sacroiliac joint (e.g., sacroilitis or ankylosing
spondylitis) and non-specic: those disorders with no identied
* Corresponding author. Tel.: 64 3 479 8981; fax: 64 3 479 8390.
E-mail address: melanie.bussey@otago.ac.nz (M.D. Bussey).

pathoanatomical basis (OSullivan and Beales, 2007). Much is still


unknown about non-specic PGP disorders, although clearer
patterns are emerging regarding motor control strategies of the
load transfer mechanism (Beales et al., 2009; Beales et al., 2010).
Previous studies investigating sacroiliac joint (SIJ) motion have
demonstrated very limited ranges of motion and hence are
considered by many to have little importance in the study of PGP.
However, research by Damen et al. (2001) has shown a strong link
between asymmetric laxity of the SIJ and moderate to severe levels
of symptoms in participants with peripartum PGP. Further, Damen
et al. (2001) suggest that the active straight leg raise (ASLR) test can
detect asymmetric stiffness of the SIJ even in participants with
minimal pain symptoms. These ndings suggest a link between
altered motor control of the load transfer mechanism (as assessed
by the ASLR) and asymmetric pelvic mobility. Thus, whilst range of
motion at the SIJs may be of little biomechanical consequence with
respect to PGP, the pattern of mobility may be important.
Ankylosing spondylitis is a condition largely affecting the SIJs,
leading to inammation, erosion and eventual fusion of the joint
with resultant disturbance to SIJ mobility (Akgul and Ozgocmen,
2011). Recently, Garrido-Castro et al. (2012) have shown that
participants with AS have signicantly lower spinal mobility when
compared to healthy controls and that limitations in mobility

1356-689X/$ e see front matter 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.math.2012.07.010

Please cite this article in press as: Bussey MD, Milosavljevic S, Can innominate motion be used to identify persons with ankylosing spondylitis? A
pilot study, Manual Therapy (2012), http://dx.doi.org/10.1016/j.math.2012.07.010

M.D. Bussey, S. Milosavljevic / Manual Therapy xxx (2012) 1e6

increase with severity of symptoms of the disease (as measured by


the Bath Ankylosing Spondylitis Metrology Index). The authors have
chosen to investigate innominate kinematic parameters in a pilot
group of serologically diagnosed subjects with this musculoskeletal
systemic disorder. It was postulated that due to the inammation
and potential fusion of the SIJ, the AS participants will have altered
SIJ stiffness leading to a decrease in innominate mobility and
potentially altered mobility patterns as compared to healthy
controls. The primary aim of this study was to use a valid and reliable
innominate kinematic evaluation procedure (Bussey et al., 2009a,
2009b; Adhia et al., 2012) to determine whether participants with
a specic systemic PGP disorder, ankylosing spondylitis have
abnormal patterns of innominate mobility. The secondary aim of this
study was to determine if the outcome measures of the innominate
testing could be used to correctly identify persons with ankylosing
spondylitis from a group of healthy controls.
2. Methods
2.1. Design
A comparative study between healthy individuals and individuals diagnosed with ankylosing spondylitis using a randomized
block design of three hip positions, external rotation (ER), hip
abduction (AB) and the combination (ER AB). Participants were
allocated to three random-order blocks ([ER, AB, ER AB]; [AB,
ER AB, ER]; [ER AB, ER, AB]) for testing. Within each of these hip
positions, participants lower limbs were rotated up to six 10
increments. There were two outcome measures of innominate
motion in the transverse and sagittal planes. Details of each of these
measures (hip position, rotation, and pelvic angles) follow.
2.2. Participants
Ethical approval was granted by the University of Otago Human
Ethics Committee. Twenty four consenting participants aged
between 23 and 55 were recruited. There were 6 participants with
ankylosing spondylitis (AS) with a mean age of 36.3 yrs (SD 10.0;
BMI of 24.4 kg/m2 SD 2.3) and 18 healthy age and sex matched
controls with a mean age 35.0 yrs (SD 9.3; BMI of 23.5 kg/m2 SD
2.7). The AS participants were a convenient sample of current and
previous physiotherapy patients referred for exercise and advice
following diagnosis of ankylosing spondylitis via a Medical/Rheumatological pathway. Time since diagnosis was quite variable
between AS participants ranging between 2 and 10 years. All AS
participants were HLA B27 positive and had described the presence
of bilateral SIJ symptoms on presentation. Healthy controls were
dened as participants who were free of back, hip or pelvis pain/
injury following direct questioning. Exclusion criteria for both
groups included pregnant or breast feeding women; diagnosed
acute disc herniation/prolapse / radiculopathy; spinal surgery;
recent lower limb injury or surgery; known congenital anomalies of
the hip, pelvis or spine; known systemic neuropathy or other
inammatory arthropathy; the presence of malignancy; or the
presence of other known musculoskeletal red ags. All participants completed the Roland Morris Disability Questionnaire
(RMDQ) and a pain prole questionnaire on the day of testing
(Roland and Morris, 1983). The AS group also described their
present pain level using a visual pain scale (Huskisson, 1974). Five of
the six AS participants were taking medication at the time of the
study and were instructed to take this as normal on the day of
testing. On the day of testing all AS participants rated their daily
function as very good and also described their pain as mild to
moderate compared to the most severe pain they had experienced
due to their condition.

2.3. Procedure
Kinematic data were collected with a magnetic tracking device
(Polhemus Liberty, 40 Hercules Drive, P.O. Box 560, Colchester, VT
05446), consisting of a transmitter, four receivers, a digitizer and
a systems electronics unit. Measurement error of the system in the
x, y and z coordinates of each of the 4 pelvic points was 0.02 mm
(SD 0.84 mm) on the x-axis, 0.07 mm (SD 0.82 mm) on the y-axis
and 0.03 (SD 0.99 mm) on the z-axis. The global average value of
imprecision in the measurement of a point for intra-observer reliability was 0.80 mm (SD 1.47 mm). A global coordinate system was
established by mounting the transmitter to a rigid wooden support.
The receivers were mounted to thermoplastic frames and secured
rmly to the thighs and over the S1 and L3 spinous process with
double-sided tape and Velcro support straps (legs only) (Bussey
et al., 2009a, 2009b, Fig. 1). An anatomically relevant reference
system for identifying the hip joint centre was dened with
a predicative method based on each subjects pelvic and lower limb
anthropometrics (Bush and Gutowski, 2003).
A hip rotation frame (as described in Bussey et al., 2009a) was
used to standardize the rotational increments applied to the femurs
in three anatomical hip positions: external rotation (ER), abduction
(AB), and a combination of external rotation and abduction called
ER AB, which is reminiscent of the Patrick Fabers test. A
maximum of six incremental rotations (10 each) for both ER and
AB were available, but not necessarily used, for each participant.
A palpation and digitizing technique known to accurately and
reliably measure innominate motion (Bussey et al., 2004; Bussey
et al., 2009a; Adhia et al., 2012) was used to calculate motion of
the innominate bones in reference to their initial static positions.
The global system, mounted to the standardizing frame, was
transformed to a local reference system, which was attached to the
skin over the 3rd lumbar spinous process of each participant. The
motion of the innominate in the sagittal and transverse planes of

Fig. 1. Participant set-up in standardizing frame for a participant in the neutral position. Receivers attached to the pelvis and legs are embedded to the local anatomical
reference system through digitised coordinates of the ASIS and PSIS of the pelvis and
the greater trochanter, medial and lateral epicondyles of the femur.

Please cite this article in press as: Bussey MD, Milosavljevic S, Can innominate motion be used to identify persons with ankylosing spondylitis? A
pilot study, Manual Therapy (2012), http://dx.doi.org/10.1016/j.math.2012.07.010

M.D. Bussey, S. Milosavljevic / Manual Therapy xxx (2012) 1e6

the local reference system was calculated as angular displacement


between the reference position and each subsequent 10 hip
rotation (of ER, AB and ER AB) (Bussey et al., 2009a, 2009b).
Sagittal plane motion was calculated as a composite angle between

innominates rotating about the sagittal-horizontal axis of the pelvis


(described in Bussey et al., 2009a, 2009b). Transverse plane motion
was calculated as absolute displacement of left and right bones
individually about the vertical axis.

Fig. 2. Trend graphs depicting the innominate motion trend of each healthy control (thin black lines) and AS (thick coloured lines) participant. (A) Transverse plane motion during
the AB condition; (B) Sagittal plane motion during the AB condition; (C) Transverse plane motion during the ER condition; (D) Sagittal plane motion during the ER condition; (E)
Transverse plane motion during the AB ER condition; (F) Sagittal plane motion during the AB ER condition.

Please cite this article in press as: Bussey MD, Milosavljevic S, Can innominate motion be used to identify persons with ankylosing spondylitis? A
pilot study, Manual Therapy (2012), http://dx.doi.org/10.1016/j.math.2012.07.010

M.D. Bussey, S. Milosavljevic / Manual Therapy xxx (2012) 1e6

Table 1
Mean (and standard deviation) maximal innominate and passive hip angles measured in each hip position.
Angles

Hip condition
External rotation (ER)

Innominate

Transverse (degrees)
Sagittal (degrees)

Hip
a

Passive (degrees)

C
AS
C
AS
C
AS

4.37
2.13
5.72
2.37
52.5
28.9

(1.67)a
(1.27)
(3.13)a
(1.38)
(5.1)a
(9.4)

Combination (ER AB)

Abduction (AB)
4.76
2.32
6.66
2.68
54.5
36.2

(2.00)a
(1.88)
(3.65)a
(2.13)
(3.5)
(7.5)

5.28
1.70
5.27
2.78
75.4
46.4

(1.89)a
(1.41)
(3.05)a
(2.10)
(11.2) 55.9 (3.8)a
(16.1) 38.8 (8.5)

indicates signicantly different (p < 0.02).

2.4. Data analysis


Data analysis involved applying best-t equations to the data
and visual inspection of the produced spaghetti graphs. Statistical
calculations were performed using statistical software SPSS
(version 18 SPSS Inc., IBM Company Chicago, Illinois 60606).
Independent t-tests were used to assess differences in hip and
innominate angles for each hip condition test between the AS and
Control groups. Statistical analysis consisted of conditional logistic
regression for each test position to determine our ability to predict
group association from test outcome of maximal sagittal and
transverse angles. The alpha level was adjusted for multiple
comparisons using Bonferonni adjustment to 0.017. The conditional
logistic regression measured the probability to predict group
association from sagittal and transverse angles as well as predicted
group association for each individual participant. Receiveroperated characteristics (ROC) curves were inspected to determine cut-off points for each continuously scaled hip condition test
outcome of angle. Cut-off points for maximising the sensitivity and
specicity for each hip condition test were determined using the
Youden Index (Schisterman et al., 2005).
3. Results
Response to the visual analogue pain scale for the AS participants ranged from 10 mm to 46 mm corresponding to mild to
moderate pain levels (Hawker et al., 2011). The RMDQ responses
ranged from 0 to 3 indicating no signicant disability among
participants. In fact all participants apart from three AS, scored 0 on
the RMDQ.
Some control as well as all AS participants were clearly best
described via polynomial equations. Thus, polynomial equations
were t to all the data. Visual inspection of the trend graphs
conrms that the motion patterns of the AS participants are
different from that of the Control participants (Fig. 2AeF). For AB
and AB ER test conditions, the lines representing the AS participants tend to cluster at the bottom of the graph below 2.5 (Fig. 2A
& B, E & F). For the ER test condition (Fig. 2C & D), there are two
notable visual differences. First, is that the AS participants had
fewer total ER rotations than the Control group. Five of the AS
participants had 3 or less rotations while all controls achieved at
least 5 rotations (Fig. 2C & D). The second most notable nding, was
the strong downward polynomial trend of the AS transverse
innominate angles, this differs from the strong mostly upward
polynomial trends of the controls (Fig. 2C & D). Another notable
nding for the AS group is the apparent trade-off occurring
between the transverse and sagittal angles in the AB and ER test
conditions. Viewing the transverse and sagittal graphs side by side,
it is clear that while the motion in the transverse plane declines the
motion in the sagittal plane increases.
Mean maximal angles and standard deviations (SD) for the
innominates and hip are presented in Table 1. As shown in Table 1,

the results of the independent t-tests showed that the AS participants have reduced innominate and hip range of motion compared
to the controls, particularly in the ER position. The results of the
conditional logistic regression showed that the outcome variable of
maximal transverse and sagittal angles were signicant predictors
(p 0.002 for AB, p 0.005 for AB ER and p 0.007 for ER
Table 3) of group association. The beta statistic for all three tests
was negative, showing the negative correlation between angle and
group association. This means that the greater the angle measure
the less likely it is that the participant belongs to the AS group. The
cross tabulation tables produced by the logistic regression are
presented in Table 2.
The ROC curves were produced and analysed for each position
the cut-off criterion, sensitivity, specicity, and area under the
curve (AUC) values are presented in Table 3. The area under the
curve is the best indicator of the accuracy of a test, the values
determined for our tests range from 0.884 to 0.965 showing good to
excellent accuracy (Table 3). The sensitivity and specicity for the
cut-off criterion relate well to the cross-tabulation table produced
by the conditional logistic regression (Table 2 and Table 3). The cut
values range from 2.1 to 3.4 , which gave excellent sensitivity
(>80%) and fair to excellent specicity (75e91%). Since AS is
strongly associated with decreased SIJ motion, larger cut values will
allow more false positives to be identied. Hence tests with larger
cut values have lower specicity.
Motion about the vertical axis (transverse plane) demonstrated
a pattern of innominate motion in the healthy control participants,
which tended to be either reciprocal (50%) or unilateral (50%). In
the reciprocal pattern each innominate rotates in opposing directions about the vertical axis whereas in the unilateral pattern both
innominate bones rotate in the same direction about the vertical
axis, usually in the direction of the applied load. In this scenario if
the left hip was being stressed both innominates would rotate
towards the left and if the right hip was being stressed both
innominates would rotate towards the right. In the AS group 4 out
of 6 participants (67%) displayed a unilateral innominate pattern,
where both innominates rotated in the same direction regardless of

Table 2
Two by two contingency tables for each test.
Observed

Predicted
Group
C

AB

AB ER

ER

C
16
AS
2
Overall percentage
C
15
AS
1
Overall percentage
C
15
AS
0
Overall percentage

Percentage correct
AS
2
4
3
5
3
6

88.9
66.7
83.3
83.3
83.3
83.3
83.3
100.0
87.5

Please cite this article in press as: Bussey MD, Milosavljevic S, Can innominate motion be used to identify persons with ankylosing spondylitis? A
pilot study, Manual Therapy (2012), http://dx.doi.org/10.1016/j.math.2012.07.010

M.D. Bussey, S. Milosavljevic / Manual Therapy xxx (2012) 1e6

Table 3
Cut-off criterion sensitivity, specicity and AUC values as calculated for each test independently.
Condition

Criterion

Sensitivity (95% CI)

Specicity (95% CI)

AUC (95% CI)

p-value

AB
AB ER
ER

3.4
2.8
2.1

0.917 (0.615e0.998)
0.917 (0.615e0.998)
0.833 (0.516e0.979)

0.755 (0.578e0.879)
0.806 (0.650e0.918)
0.917 (0.775e0.982)

0.884 (0.759e0.958)
0.891 (0.768e0.963)
0.965 (0.868e0.997)

0.002
0.005
0.007

a signicant at p 0.017.

the leg being stressed at the time, one AS participant displayed


a normal unilateral pattern, moving towards the stressed side, and
in one participant the measured motion was too small to determine
a movement pattern.
4. Discussion
The purpose of the present study was to determine the utility of
a technique developed by Bussey et al. (2009a, 2009b) in detecting
potential abnormal patterns of pelvic joint mobility in participants
with ankylosing spondylitis. Observation of the trend graph readily
discern differences between the AS participants and the control
group. The results of the conditional logistic regression conrm our
ability to predict group association within the participants from our
outcome variables of transverse and sagittal angles for all three
test/hip conditions. The cut values range from 2.1 to 3.4 , which
gave excellent sensitivity (>80%) and fair to excellent specicity
(75e91%). AS is strongly associated with reduced SIJ mobility and
hence larger cut values will allow more false positives to be identied. As a result, the AB condition, which had larger cut value, had
the lowest specicity (75%) and the ER condition, which had the
lowest cut value, had the highest (91%).
The results of the study show that a difference between the two
groups was detectable and so further study will be undertaken to
determine if this technique is sufciently sensitive to use in the
assessment of mobility patterns in clinical populations expected to
have limited movement at the SIJ. In patients with AS, mobility
assessment in the lower lumbar spine and SIJ are standard means of
assessing disease severity- the standard measure being the
Schobers test (Macrae and Wright, 1969; Linden et al., 1984;
Jenkinson et al., 1994). Such measures are incorporated into clinical
scoring systems such as the Bath Ankylosing spondylitis metrology
index (Jenkinson et al., 1994). The assessment of spinal mobility
assists in the identication of sub groups of AS, as well as informing
clinicians as to clinical outcomes of treatments and progression of
the disease (Haywood et al., 2004). Sacroiliac arthropathy is
a strong indicator of the diagnosis of AS (Linden et al., 1984) with
a likelihood ratio of 9.0 (Dougados et al., 1991). Assessment of
mobility of the SIJ by means of palpation (e.g., stork test) is notoriously unreliable (Laslett, 2008), using stress testing and MRI
scanning is the current gold standard for evaluation of inammatory process (Rudwaleit et al., 2009). There are no clinically
accepted validated measures to assess SIJ mobility and or changes
in mobility as the disease progresses (Rudwaleit et al., 2005). This
technique (essentially a modied version of the Patrick Fabers test
(i.e., the ER AB) applied in prone lying) in combination with
palpation and digitising of pelvic landmarks has been shown to be
highly reliable measure trial-to-trial as well as between testers
(Adhia et al., 2012). Combined with the results of the present study
a picture of clinical utility of this technique is emerging. Further
work with AS patients is required but at the moment the use of
a modied Patrick Fabers test (i.e., the ER AB) in combination
with a palpation and digitising technique shows promise as a clinical tool for assessing pelvic joint mobility in AS.
This study is the rst step in gauging the clinical utility of these
hip positions in assessing SIJ pathology. While the ndings are

encouraging, they must be tempered with the small sample size


and the expectation of reduced mobility in this clinical population.
It was a clear expectation that a healthy normal population would
have both a greater overall range of movement at the SIJ/innominate as well as a greater variability within the range of motion
between participants (Bussey et al., 2009a, 2009b). In this study
innominate motion is measured as the hip is positioned into
extreme ranges of motion as tolerated by the participants, it was
expected that the AS participants would be limited in hip positioning due to pain or discomfort. However, the research found that
the AS participants were limited by physiological restrictions to the
hip range of motion rather than discomfort, as highlighted in
Table 1 the AS participants had signicantly lower passive hip range
of motion compared to the controls. Thus, the source of the reduced
innominate mobility in this population is still in question. At this
point it is not possible to say with certainty that the reduced
innominate mobility originated from increased stiffness at the SIJ or
whether it resulted from the reduced hip mobility imparting
reduced load to the innominate. Further, as highlighted by GarridoCastro et al. (2012) the severity of AS symptoms may impact on the
mobility of the spine, since none of our participants rated their
symptoms as severe at the time of the study, therefore one might
assume the effect may be greater in a population of AS participants
with more severe symptoms. The study ndings in light of these
limitations indicate a larger study on AS is required to investigate
the effect of symptom severity (including amount of SIJ fusion) on
innominate mobility and to determine if kinematic testing of the
innominate has utility for tracking disease progression.
5. Conclusions
The technique of measuring innominate motion during prone
hip ER and ER AB has shown excellent sensitivity (>80%) and fair
to excellent specicity (75e91%) in identifying a known pelvic joint
disorder albeit in a small sample of people with ankylosing spondylitis. More work is needed to determine whether this technique is
a viable option for assessing changes in pelvic mobility in association with progression or are-ups associated with AS. Further work
is also required to determine if this technique is sufciently
sensitive to determine the kinematic difference between nonspecic PGP and in other low back pain populations.
Acknowledgements
The authors would like to acknowledge the School of Physical
Education at the University of Otago for their nancial support and
all the participants for consenting to take part in this project. We
would also like to thank Dr. Simon Stebbings consulting Rheumatologist in the University of Otagos School of Medicine for his
advice and support in the preparation of this manuscript.
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Please cite this article in press as: Bussey MD, Milosavljevic S, Can innominate motion be used to identify persons with ankylosing spondylitis? A
pilot study, Manual Therapy (2012), http://dx.doi.org/10.1016/j.math.2012.07.010

M.D. Bussey, S. Milosavljevic / Manual Therapy xxx (2012) 1e6

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Please cite this article in press as: Bussey MD, Milosavljevic S, Can innominate motion be used to identify persons with ankylosing spondylitis? A
pilot study, Manual Therapy (2012), http://dx.doi.org/10.1016/j.math.2012.07.010

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