ARTICLE IN PRESS

Manual Therapy 13 (2008) 404–410

www.elsevier.com/math

Original article

Ultrasound imaging of the lateral abdominal wall muscles in

individuals with lumbopelvic pain and signs of
concurrent hypocapnia
Jackie L. Whittaker
Whittaker Physiotherapy Consulting, 101 12761-16th Ave. Surrey British Columbia, Canada V4A 1N2
Received 9 October 2005; received in revised form 9 February 2007; accepted 11 March 2007

Abstract

The purpose of this study was to compare the change in thickness of transversus abdominis (TrA) and internal oblique (IO)
muscles, during resting supine respiration, in individuals with lumbopelvic pain (LP) to those who in addition to LP, demonstrate
signs of concurrent hypocapnia (LP&HYPO). B-mode ultrasound images were obtained at the height of inspiration, and at the end
of expiration, over three subsequent breaths during a single session. The average percent change in thickness of TrA during resting
respiration in the LP&HYPO group (20.877.6%) was found to be statistically greater (Po0.001) than that of the LP only group
(1.375.8%), while the difference between the groups for the percent change in thickness of IO (LP&HYPO 9.278.1%, LP
2.077.2%) did not differ (P ¼ 0.073). These findings suggest that respiratory modulation of TrA thickness, as measured by
ultrasound imaging, greater than 20%, detected in a resting supine position, may be associated with an episode of hypocapnia, and if
present warrants further investigation.
r 2007 Elsevier Ltd. All rights reserved.

Keywords: Hypocapnia; Internal oblique; Lumbopelvic pain; Transversus abdominis; Ultrasound imaging

1. Introduction respiratory and postural drives, allowing for simulta-

There is mounting evidence indicating that low back
pain is associated with disorders of breathing and
continence (Pool-Goudzwaard et al., 2005; Smith
et al., 2006). One possible explanation for this correla-
tion is the multifaceted roles and interactions of the
transversus abdominis (TrA) muscle. Previous studies
have demonstrated that this muscle contributes to
respiration, postural control of the lumbopelvic region,
and influences the continence mechanism (DeTroyer
et al., 1990; Hodges and Richardson, 1997; Hodges and
Gandevia, 2000; Sapsford et al., 2001; Richardson et al.,
2002; Sapsford and Kelly, 2004). Furthermore, that the
activity of this muscle is a summation of both
Tel.: +604 535 5268; fax: +604 535 5269.
E-mail address: jwphysio@telus.net.
neous execution of these tasks (Hodges and Gandevia,
2000; Hodges et al., 2001; Saunders et al., 2004).
In regard to respiration TrA is an accessory muscle.
Under normal circumstances little to no increase in
EMG activity or, architectural change (as viewed with
ultrasound imaging) of this muscle is seen with resting
respiration (Strohl et al., 1981; Detroyer et al., 1990;
Ninane et al., 1992; Goldman et al., 1997). However, if
respiration is challenged (either through increased
chemical drive or elastic loading), or voluntarily
promoted, TrA is the first abdominal muscle recruited
to assist with expiration (DeTroyer et al., 1990; Ninane
et al., 1992; Abe et al., 1996; Misuri et al., 1997).
Further, there is preliminary evidence supporting the
speculation that if aberrant chemical, mechanical or
behavioral factors exist, prolonged untimely expiratory
activity of TrA may disrupt its functional integration

1356-689X/$ - see front matter r 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.math.2007.03.008
 ARTICLE IN PRESS
J.L. Whittaker / Manual Therapy 13 (2008) 404–410
and lead to compromises of postural control (Hodges
et al., 2001), and possibly continence.
As the responsibilities of TrA are diverse its dysfunc-
tion can manifest in a variety of ways (low back or
pelvic pain, urinary incontinence, breathing disorder),
or perhaps more realistically as a multi-factorial
presentation (Smith et al., 2006). The challenge becomes
determining where to concentrate the initial focus of
treatment. A pragmatic approach would advocate
addressing the physiological priority, namely respira-
tion, as it is likely that if it is deregulated it will
perpetuate altered motor control in the region, and
possibly diminish response to traditional treatment
approaches aimed at restoring postural control or
continence. At present few objective tools exist that
provide clinicians with an insight into the possible
presence of breathing disorders in the typical lumbo-
pelvic pain (LP) patient population. However, as access
to ultrasound imaging (USI) in the clinical setting is
increasing an added option may now exist.
The literature defines hypocapnia as a reduction or
deficiency in the arterial partial pressure of carbon
dioxide resulting from emotional (anxiety, fear), beha-
vioral (forced speech, habitual sighing, yawning),
physical, chemical (increased levels of sodium lactate,
caffeine, etc.) and/or environmental stressors that led to
over breathing, or ventilation in excess of metabolic
need (Gardner, 1996). The exaggerated respiratory
response results in the elimination of carbon dioxide in
volumes greater than it is being produced by the body
and ultimately its deficiency. Hypocapnia is associated
with respiratory alkalosis and a wide variety of
symptoms, including neuronal excitability (paresthesia,
increased resting muscle activity); changes in regional
blood flow, dizziness, fatigue and chest pain (Gardner,
1996). The incidence of hypocapnia has been estimated
to be as high as 6–10% of general practice patients
(Vansteenkiste et al., 1991). However, as most indivi-
duals are not seen during an attack, and the clinical
presentation can be quite variable, symptoms are rarely
recognized and the risk of misdiagnosis is high
(Vansteenkiste et al., 1991; Gardner, 1996).
The purpose of this study was to investigate the
hypothesis that a change in thickness of TrA and,
internal oblique (IO) muscles, associated with resting
supine respiration, in a specific sub-group of individuals
with LP who demonstrated signs of a concurrent
hypocapnic episode would be greater than in a group
of individuals with signs of LP only. Accordingly, that
the resting visual modulation (supplemental video
available at www.elsevierhealth/journals/math/.com) of
these muscles, as detected with USI, is associated with
the hypocapnic episode, and hence its presence may
suggest the need for further investigation or, manage-
ment that diverges from the conventional approaches
to LP.
405
2. Methods
2.1. Subjects
Twenty-four subjects were recruited from the general
case load of a private physiotherapy practice following
an in clinic advertisement that provided information
about the study and requirements for participation.
Inclusion criteria were as follows: LP (inclusive of a
distribution consistent with sacroiliac joint involvement
as described by Fortin et al., 1994), willingness to
participate in either of the two groups with informed
consent, and fulfillment of the diagnostic criteria:
positive active straight leg raise (ASLR) test (Mens
et al., 2001; O’Sullivan et al., 2002; Stuge et al., 2004),
and consistent anterior rotation of the innominate with
one leg stance (Hungerford et al., 2004). The pain
distribution and diagnostic tests had to be positive on
one side, which was referred to as the dysfunctional side.
The first 12 subjects that fulfilled the inclusion criteria
for LP constituted the LP only group, while the first 12,
whom in addition to the diagnostic criteria for LP,
presented with concurrent hypocapnia (resting end tidal
carbon dioxide ofo35 mmHg; Lum, 1978), as deter-
mined by capnography, comprised the concurrent
dysfunction group (LP&HYPO).
Subjects were excluded if they presented with cardi-
opulmonary, neurological or other serious disease, if
they were pregnant or, in the first 6 months post partum,
as well as, if they had a history of, or were currently
undergoing, treatment for a psychological disorder. All
subjects gave written informed consent to participate in
the study.
2.2. Procedure for demographic and self-report measures
Subjects completed a standard data collection form
which provided general demographic details (age, sex),
information related to the distribution and duration of
their symptoms, as well as medical history. Height and
weight were measured and then the Quebec back pain
disability scale, a self-report functional measure (Kopec
et al., 1995), was administered.
2.3. Procedure for capnography
Although the gold standard for determining physio-
logical carbon dioxide (CO2) levels is arterial blood gas
analysis, the use of capnography to monitor real-time
CO2 levels is accepted common practice (Gardner, 1996;
Meuret et al., 2001; Roth, 2005) as the end-tidal partial
pressure of CO2 in exhaled air have been found to be
similar to arterial levels (Hoffmann et al., 1990; Barton
and Wang, 1994). A portable, capnometry device
(sCapnoTrainer, (Better Physiology Ltd. Boulder CO,
USA) was used to assess the end tidal carbon dioxide
 ARTICLE IN PRESS
406 J.L. Whittaker / Manual Therapy 13 (2008) 404–410

(ETCO2) level of all subjects. A single nasal canula was
inserted and secured into place with surgical tape.
Subjects were seated comfortably and instructed to
refrain from talking, laughing, chewing or breathing
through their mouth during the data collection period.
Expired air was collected every 30 s for 5 min during
which subjects were distracted from their respiration by
a standardized slide presentation. The CO2 zero level of
the capnograph was calibrated prior to each measure-
ment session by attaching a syringe filled with CO2
absorbent which created a CO2 deficient environment.
The ability of the instrument to accurately analyze CO2
content in the sampled air was calibrated with a solution
of 5% CO2 prior to the collection of the first subject’s
data. The capnography data was captured, stored and
then exported to Windows Excel for further analysis by
the CapnoTrainer software which was run on a laptop
computer running Windows XP. Two respiratory
parameters, the average ETCO2 level and breaths
per minute (bpm), for the middle 4 min period were
recorded.
2.4. Procedure for ultrasound imaging
Thickness of the middle fibers of TrA and IO was
measured with USI. An USI system (Falco, Biosound
Esaote Inc, Indianapolis IL, USA) was used in
conjunction with a 5.0 MHz (40 mm footprint) transdu-
cer to generate brightness (B)—mode images from the
anterolateral aspect of the abdominal wall, on the
dysfunctional side, with subjects in a supine crook lying
position. The transducer was placed in a transverse
orientation on the anterolateral aspect of the abdomen
halfway between the iliac crest and inferior border of the
rib cage (Fig. 1). The angle was manipulated until a clear
image of the lateral abdominal muscles, (TrA, IO and
external oblique) (Fig. 2a,b) was identified. The medial
to lateral placement of the transducer was adjusted such

Fig. 1. Ultrasound transducer placement for imaging the lateral abdominal wall muscles, reproduced with permission by Elsevier, Whittaker (2007).

A B
MEDIAL
SC SC
EO EO
IO IO
TrA
TrA

LATERAL

Fig. 2. Ultrasound imaging (B-mode) of the lateral abdominal wall. (A) Transverse image of the right anterolateral abdominal wall. (B) Labeled
outline. SC—subcutaneous tissue, EO—external oblique, IO—internal oblique, TrA—transversus abdominis muscles.
 ARTICLE IN PRESS
J.L. Whittaker / Manual Therapy 13 (2008) 404–410 407

scores), and respiratory (ETCO2 and bpm) parameters

of the two groups were calculated and then indepen-
dently compared using separate t-tests.
The thickness values for TrA and IO were averaged
over the three breaths and then expressed as a percent
change relative to the thickness of the muscles at the
height of inspiration. This percent change in thickness
for each of the muscle was then independently compared
between the subject groups using two t-tests. When a
significant difference existed in percent change of muscle
thickness between the groups, a Pearson-product
moment correlation coefficient was calculated to assess
the relationship between ETCO2 level and percent
change of muscle thickness.

Fig. 3. Ultrasound image indicating the measurement site (vertical line 3. Results
reference ‘‘X’’) for thickness of transversus abdominis (TrA) and
internal oblique (IO) muscles located 5 cm from the most medial extent There was no statistical difference found with respect to
of TrA. age, height, weight, sex distribution, Quebec back pain
scale scores or, duration of symptoms between the groups
that the midline border of TrA was approximately two (Table 1). As expected, there was a statistically significant
centimeters from the edge of the image, and then the difference in ETCO2 levels between the groups (Po0.001)
depth control manipulated such that the muscle layers with the average value for the LP only group being
filled approximately 40–50% of the ultrasound display 38.372.7 mmHg and for the concurrent dysfunction
(Whittaker, 2007). Once the ideal image was generated, group (LP &HYPO) 32.372.0 mmHg. Further, there
diligent care was taken to ensure that the cranial/caudal was no statistically significant difference (P ¼ 0.347)
and medial/lateral position of the probe, as well as its identified in the frequency of breaths between the groups,
angle with respect to vertical, remained consistent (LP ¼ 1673 bpm, LP&HYPO ¼ 1573 bpm).
throughout data collection. The average percent change in thickness of the TrA
Still images were captured, at the height of inspiration muscle during respiration in the LP group was
and at the end of expiration over three consecutive 1.375.8%, while in the concurrent dysfunction group
breaths. All images were captured, stored and measured (LP&HYPO) the average value was 20.877.6%. This
using an ultrasound image and analysis system consist- difference was found to be statistically significant
ing of an analogue frame grabber, computer software (Po0.001; Fig. 4). The relationship between ETCO2
(ePax manufactured by EasyPax, Toronto, Canada) and level and percent change in TrA muscle thickness was
a Pentium-based PC running Windows XP. All images calculated (r ¼ 0.685; P ¼ 0.0002) and a moderate
were captured and measured by one investigator who degree of relationship was detected. The average change
was blinded from the subject’s respiratory status. in thickness of IO in the LP group was 2.077.2%, while
The thickness of TrA and IO was measured along a in the concurrent dysfunction group (LP&HYPO) it was
vertical reference line located 5 cm from the most medial 9.278.1%. Although there was a trend towards a
extent of TrA (Fig. 3). The muscle boundaries were greater change in thickness in the concurrent dysfunc-
defined as the edges of the hypoechoic region (the tion group the difference between the groups was not
heterogeneous boundary where the pixels transition found to be statistically significant (P ¼ 0.073), and
from dark to light) (Ferreira et al., 2004). Prior to any
calculations, the intra-rater reliability of the investigator Table 1
was determined by measuring the thickness of TrA on Demographic and self report measures
the first of the six stored images for each of the 24
subjects on two separate blinded occasions, one week LP LP&HYPO P-value
apart. The intraclass correlation (ICC) was calculated Age (years) 41.4710 44.5710 0.564
and found to be 0.98 which indicated high repeatability. Height (cm) 168710 163710 0.381
Weight (kg) 64.7710 62.378 0.589
2.5. Data analysis Gender (% female) 75 100
Duration of symptoms (months) 63.3751 56.6775 0.905
Quebec back pain disability scale 10.377 16.4715 0.243
The average demographic (height, weight, duration of
symptoms), disability, (Quebec back pain disability scale Except for gender, data are presented as mean7standard deviation.
 ARTICLE IN PRESS
408 J.L. Whittaker / Manual Therapy 13 (2008) 404–410

4. Discussion

Subjects with LP and signs of concurrent hypocapnia

demonstrated greater modulation in the thickness of the
TrA muscle during resting respiration in comparison to
individuals with LP only. Similar differences were not
noted in the IO muscle however this may be a function
of sample size. Although there is previous evidence
which addresses the relationship between disease
(Ninane et al., 1992), postural (Abe et al., 1996;
Goldman et al., 1997), or experimentally increased
respiratory drive (Hodges et al., 2001) and increased
Fig. 4. Percent change in thickness of transversus abdominis (TrA)
TrA activity (as detected with electromyography), as
during respiration for the lumbopelvic dysfunction (LP), and well as evidence suggesting an increase in TrA thickness
concurrent dysfunction (LP&HYPO) groups. A significant difference (measured with USI) associated with voluntary efforts
(Po0.001) was identified between two group. (Detroyer et al., 1990; Misuri et al., 1997), this is the first
reported investigation identified that describes changes
in the thickness of TrA with USI during respiration in
individuals who demonstrate concurrent signs of hypo-
capnia and LP.
Although the visual modulation of TrA thickness
reported in this and two previous studies (Detroyer
et al., 1990; Misuri et al., 1997) may represent some level
of change in muscle activity it is important to under-
stand that the relationship between a change in the two
dimensional shape of a muscle seen with USI, and actual
activity is complex (Hodges et al., 2003; McMeeken
et al., 2004; Hodges, 2005). Various factors including
initial length and width of the muscle, the orientation of
its fibers, as well as other forces competing against the
muscle influence changes in its shape, and must be
Fig. 5. Percent change in internal oblique (IO) during respiration for
considered. For instance as the diaphragm descends
the lumbopelvic dysfunction (LP), and concurrent dysfunction
(LP&HYPO) group although there was a trend towards a greater during inspiration, it pushes the abdominal contents out
increase in thickness in the concurrent dysfunction group it was not into the abdominal wall muscles causing them to
statistically significant (P-value 0.073). relatively lengthen and decrease in thickness. In contrast
during expiration the retraction of the abdominal
contents results in relative shortening and an increase
Table 2
in thickness of these muscles. Consequently although the
Mean, standard deviation and percent change of muscle thickness
values for transversus abdominis (TrA) and internal oblique (IO) modulation in the thickness of TrA may represent actual
muscles during inspiration and expiration muscle activity, it could also reflect an alteration
towards an abdominal respiratory pattern (due perhaps
Muscle Muscle thickness LP (n ¼ 12) LP&HYPO (n ¼ 12)
to an increase in resistance to costal and/or a decrease in
TrA Inspiration (mm) 5.871.6 4.571.1 resistance to abdominal expansion). However, regard-
Expiration (mm) 5.971.6 5.471.3 less of the mechanism(s) responsible for the modulation
% Change* 1.3275.77 20.8177.63 in the thickness of the TrA muscle it appears that this
IO Inspiration (mm) 11.270.45 9.572.2 phenomenon is associated with the presence of a
Expiration (mm) 11.470.47 10.372.4
% Change** 1.9777.33 9.2378.09
concurrent hypocapnia episode in a group of individuals
with LP.
*Po0.001. The detection of increased modulation of TrA
**P40.05. thickness during resting supine respiration in individuals
with LP and signs of concurrent hypocapnia, versus
there was much greater variability demonstrated in the individuals with LP only holds clinical relevance for a
measurements for this muscle (Fig. 5). Descriptive variety of reasons. Firstly, as access to USI is increasing
statistics (mean and standard deviations) of muscle clinicians are privy to previously unavailable informa-
thickness values during inspiration and expiration are tion regarding the behavior of the lateral abdominal
provided in Table 2. wall muscles during respiration. This new information,
 ARTICLE IN PRESS
J.L. Whittaker / Manual Therapy 13 (2008) 404–410
specifically the presence of a modulation in the thickness
of TrA greater than 20% with resting respiration may
assist in the management of individuals with LP by
drawing attention to an elusive sub-group of those that
may require concurrent investigation of their respiratory
health and factors that effect it. Further, USI and the
real-time visual information that it provides may be
useful in the explanation of the condition to the patient
as well as during retraining of the pattern of breathing.
Secondly, the findings of this investigation suggest that
if USI is to be employed as a method of measuring
architectural changes in the lateral abdominal muscles in
individuals with LP or breathing disorders care must be
taken to standardize the point in the respiratory cycle
where measurements are taken in an attempt to ensure
the highest degree of methodological rigor. Finally, the
information gathered in this study may help to improve
the cohesion of cohorts for future study into the efficacy
of interventions aimed at those with LP. In these
investigations where one, several, or combinations of
interventions are being compared against each other it is
critical that there is homogeneity between cohorts and
that concurrent related disorders are controlled for.
Consequently the use of USI as a means to screen for
individuals that are possibly incongruent (i.e. those with
altered physiology resulting from hypocapnia) may have
value, however further investigation is required.
The primary limitation of this study is the use of a one
time measurement to determine the presence of a
breathing disorder such as hypocapnia. As mentioned
previously due to its variable symptomatology hypo-
capnia can be elusive (Vansteenkiste et al., 1991;
Gardner, 1996). Generally it is defined by an ETCO2
value ofo35 mmHg (normal ETCO2 ¼ 35–45 mmHg)
(Lum, 1978). Although hypocapnia can be chronic it is
commonly episodic as individuals over breathe at
specific times, places and under specific circumstances.
Consequently although the individuals in the concurrent
dysfunction (LP&HYPO) group presented with signs
consistent with hypocapnia, further diagnostic work-up
would be required for a conclusive diagnosis.
5. Conclusion
An initial link between hypocapnia and increased
modulation of TrA thickness during resting respiration
has been demonstrated using USI. Further inquiry is
required to determine the validity, sensitivity and
specificity of this tool, as well as the mechanism(s)
behind the visual modulation by comparing it to
indwelling EMG and changes in respiratory patterning.
Perhaps more clinically relevant would be to investigate
the presence of resting respiratory modulation and other
indicators of hypocapnia in other subject groups,
specifically patients who in addition to musculoskeletal
409
dysfunction present with behavioral factors which
predispose them to over breathing and hypocapnia,
such as those with recalcitrant symptoms.
Acknowledgments
The author would like to acknowledge Deydre
Teyhen PhD for her editorial comments, Richard
Bourassa and Ryan Dueck for their statistical assis-
tance, Richard Boothroyd for his technical support, and
Diane Lee for her assistance in the collection of data.
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