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Manual Therapy 16 (2011) 596e601

Contents lists available at ScienceDirect

Manual Therapy
journal homepage: www.elsevier.com/math

Original article

Ultrasound measurement of abdominal muscles activity during abdominal


hollowing and bracing in women with and without stress urinary incontinenceq
Amir Massoud Arab a, *, Mahshid Chehrehrazi b
a
Department of Physical Therapy, University of Social Welfare and Rehabilitation Sciences, Evin, Koodakyar Ave., P.O Box 1985713834, Tehran, Iran
b
Isfahan University of Medical Sciences, Isfahan, Iran

a r t i c l e i n f o a b s t r a c t

Article history: Synergistic co-activation of the abdominal and pelvic floor muscles (PFM) has been reported in the
Received 3 March 2010 literature. Considering that PFM dysfunction is present in women with stress urinary incontinence (SUI),
Received in revised form altered abdominal muscle activation may also occur in incontinent women. The purpose of this study
28 April 2011
was to investigate the abdominal muscle activity during abdominal hollowing and bracing maneuver in
Accepted 6 June 2011
women with and without SUI using ultrasound. Convenience sample of 20 non-pregnant female
participated in the study. Subjects were categorized into two groups: continent females (N ¼ 10) and
Keywords:
females with SUI (N ¼ 10). The percentage of change in thickness of right transverse abdominals (TrA)
Abdominal muscles
Stress urinary incontinence
and internal obliques (IO) was measured during abdominal hollowing and bracing maneuver in both
Ultrasound groups. The result of two-way mixed-design ANOVA revealed no significant health status by maneuver
Hollowing interaction effect for ultrasound measurement of the percentage of change in thickness of TrA (P ¼ 0.66)
Bracing and IO (P ¼ 0.36). The main effect of health status on the percentage of the change in thickness of TrA
(P ¼ 0.52) or IO (P ¼ 0.84) was not statistically significant. In overall, no significant difference was found
in the percentage of changes in thickness of TrA and IO muscles during abdominal hollowing or bracing
maneuver between women with and without SUI.
Ó 2011 Published by Elsevier Ltd.

1. Introduction 2008). It is probable that this contributes to urinary continence.


Investigators attributed the generation of intra-vaginal pressure in
Stress urinary incontinence (SUI) is a common health related continent women to co-activation of PFM and abdominal muscles
problem in women, involving 50% of women with urinary inconti- (Madill and McLean, 2006). Neumann and Gill (2002) showed that
nence (Abrams et al., 2003; DeLancey and Ashton-Miller, 2004). SUI continent women were unable to fully perform PFM contraction
is defined as “the complaint of involuntary leakage on effort or without simultaneous contraction of the transverse abdominals
exertion, or on sneezing or coughing” (Abrams et al., 2003). For (TrA) and the internal obliques (IO).
urinary continence to be maintained, urethral pressure must be A significant difference in abdominal EMG amplitude during
greater than bladder pressure at all times. Under normal circum- maximal voluntary PFM contraction was found between healthy
stances, pelvic floor muscles (PFM) contract to increase the pressure continent women and those with severe SUI (Madill et al., 2009).
of the urethra during the tasks that increase intra-abdominal pres- Some reports have also demonstrated less PFM activity and more
sure. There is substantial evidence indicating PFM dysfunction in abdominal muscle activity during PFM contraction in the inconti-
women with SUI (Bø, 2003; Morin et al., 2004; Amaro et al., 2005). nent women compared with asymptomatic women (Thompson
Synergistic co-activation of the abdominal and PFM has been et al., 2006). It is thought that incontinent women can not perform
reported in the literature with electromyographic (EMG) evidence a correct PFM contraction using a localized muscle strategy and use
of this synergistic relationship (Sapsford et al., 2001; Sapsford and muscle substitution strategies and activate all the muscles of the
Hodges, 2001; Neumann and Gill, 2002; Madill and McLean, 2006, abdomino-pelvic cavity (Thompson et al., 2006). EMG studies have
found delayed abdominal muscle activity during arm movement
(Smith et al., 2007a), greater external oblique activation during
postural tasks (Smith et al., 2007b), and greater abdominal activa-
q This research was reviewed and was approved by the Human Subject
tion during balance tasks (Smith et al., 2008) in women with SUI.
Committee at University of Social Welfare and Rehabilitation Sciences.
* Corresponding author. Tel./fax: þ98 21 22180039. Real-time ultrasound imaging is a reliable and valid technique
E-mail addresses: arabloo_masoud@hotmail.com, amarab@uswr.ac.ir (A.M. Arab). recently used by physical therapists to evaluate muscle structure,

1356-689X/$ e see front matter Ó 2011 Published by Elsevier Ltd.


doi:10.1016/j.math.2011.06.002
A.M. Arab, M. Chehrehrazi / Manual Therapy 16 (2011) 596e601 597

function and activation patterns. This method allows for real time 2. Material and methods
study of the muscles as they contract. This is especially important
when the activation pattern of deep muscles such as deep 2.1. Subjects
abdominal muscles is investigated (Teyhen et al., 2007; Costa et al.,
2009). Changes in thickness of the TrA and IO muscles are A cross sectional study design was used to compare abdominal
measured as an indicator of muscle activity in ultrasound imaging muscle activity in two groups of women: women with SUI and
(Critchley and Coutts, 2002; Ferreira et al., 2004; Henry and continent women. A total of 20 non-pregnant females participated
Westervelt, 2005; Ainscough-potts et al., 2006; Teyhen et al., in the study. The subject population in this study was a sample of
2007; Costa et al., 2009). The reliability of this method for convenience made up of subjects who were between the ages of 25
measuring changes in TrA muscle thickness has been established and 50 years. An equal number of women (N ¼ 10) were allocated
previously (Costa et al., 2009). Validity studies have compared to each group. The subjects with SUI had been diagnosed by
ultrasound measurements with those obtained using fine wire a urogynaecologist as having symptoms of SUI. The type of urinary
EMG (Hodges et al., 2003; McMeeken et al., 2004). incontinence had also been assessed using a urinary symptoms
McMeeken et al. (2004) found good to high correlation between questionnaire (Ishiko et al., 2000). Inclusion criteria were willing-
the needle EMG recordings of TrA and ultrasound changes in ness to participate, having had urine leakage on coughing,
thickness of the muscle at all activity level. Hodges et al. (2003) sneezing, laughing, lifting and any activity that increases the intra-
compared the thickness changes in the abdominal muscles in abdominal pressure, premenopausal or under hormone replace-
real-time ultrasound and EMG activity. They found that change in ment therapy. Asymptomatic females, matched in age, body mass
thickness and EMG activity of the TrA and IO muscles were linearly index (BMI) and parity, were also evaluated by urogynaecologist
related at low contraction levels. However, these researchers found and found to have no symptoms of urinary incontinence. Exclusion
that the external oblique muscle behaved differently from the TrA criteria were pregnancy and having given birth in previous 12
and IO in that there was no consistent relationship between muscle months, known neurological or respiratory disorders, low back
thickness and EMG activity of external oblique and this muscle did pain in previous six months, prolapse of the pelvic organs greater
not become thicker when it contracted. than the second degree, and major surgery of the abdominal or
These findings support the use of ultrasound imaging as a non- pelvic regions. All the participants signed an informed consent
invasive technique to measure TrA and IO muscle thickness and form approved by the human subjects committee at the university
estimate relative muscle activity. of Social Welfare and Rehabilitation Sciences before participating in
Recent studies have demonstrated a link between low back pain the study. Physical characteristics of the subjects can be seen in
and genito-urinary dysfunction such as SUI (Finkelstein, 2002; Table 1.
Pool-Goudzwaard et al., 2005; Smith et al., 2006). There is
substantial evidence indicating that a primary muscular impair-
2.2. Ultrasound measurement of the abdominal muscle thickness
ment in patients with lumbopelvic pain is dysfunction of deep
abdominal muscles (Hodges, 1999; Richardson et al., 1999; Jull and
A diagnostic ultrasound imaging unit set in B-mode (Ultra-
Richardson, 2000) and major muscular impairment in subjects
sonix-ES500, Canada) with a 7.5 MHz linear head transducer was
with SUI is PFM dysfunction (Bø, 2003; Morin et al., 2004; Amaro
used to measure the changes in thickness of the abdominal
et al., 2005). Considering these findings, altered abdominal
muscles (TrA, IO) during abdominal hollowing and bracing
muscle activation may also occur in women with SUI.
maneuver based on the method explained by others (Critchley and
The abdominal hollowing and bracing maneuvers are
Coutts, 2002; Ferreira et al., 2004; McMeeken et al., 2004; Henry
commonly used to assess and rehabilitate abdominal muscles
and Westervelt, 2005; Ainscough-potts et al., 2006; Teyhen et al.,
(Allison et al., 1998; Richardson et al., 1999; Jull and Richardson,
2007). The measurements were made on the right side of the
2000; Beith et al., 2001). The abdominal hollowing maneuver is
abdominal wall at the end of expiration. The participants were
performed to activate deep abdominal muscles (TrA and IO) and
tested in supine position with one pillow underneath the head and
involves gently drawing the lower abdominal wall in toward the
knee. The lumbar spine was positioned in neutral. The abdominal
spine. The abdominal bracing maneuver is performed with
wall was exposed. The ultrasound transducer was transversely
emphasis on the activation of all the antero-lateral abdominal
located across the abdominal wall over the anterior axillary line
muscles. This is achieved by instructing the subjects to tighten
midway between the 12th rib and the iliac crest to obtain a clear
their abdominal wall and increase the lateral diameter of the
image of the three antero-lateral abdominal muscle layers. Prior to
waist (Allison et al., 1998; Richardson et al., 1999; Jull and
testing, participants were trained by a physiotherapist to perform
Richardson, 2000; Beith et al., 2001). Changes in thickness of
the abdominal maneuvers correctly. A pressure biofeedback device
the TrA and IO muscles during abdominal maneuvers are
was used to standardize each maneuver (Allison et al., 1998;
measured using ultrasound imaging to indicate abdominal muscle
activity (Critchley and Coutts, 2002; Ferreira et al., 2004; Henry
and Westervelt, 2005; Ainscough-potts et al., 2006; Teyhen Table 1
et al., 2007). Descriptive statistics for the subjects and the thickness of the TrA and IO at rest in
To our knowledge, no study has directly evaluated abdominal each group (Mean  SD).

muscle activity in women with and without SUI using ultrasound Variables Continent Incontinent P-
measurements. The purpose of this study was to investigate the (n ¼ 10) (n ¼ 10) value
changes in the thickness of the TrA and IO muscles during Age (years) 38.47  5.23 41.66  6.44 0.15
abdominal hollowing and bracing maneuvers using ultrasound in Weight (kg) 67.20  9.36 69.35  10.52 0.56
Height (cm) 160.53  6.78 158.14  4.72 0.78
women with and without SUI. 2
BMI (kg/m ) 25.61  3.50 27.52  4.14 0.67
The hypothesis of this study is as follows: Parity 2.40  0.94 2.84  1.26 0.22
Thickness of the TrA at rest 3.49  0.78 3.72  0.75 0.51
- The percentage of thickness change in TrA and IO muscles (mm)
during abdominal hollowing or bracing maneuvers is signifi- Thickness of the IO at rest (mm) 6.02  0.82 5.89  1.18 0.78

cantly different between women with and without SUI. TrA ¼ Transverse abdominis; IO ¼ Internal oblique.
598 A.M. Arab, M. Chehrehrazi / Manual Therapy 16 (2011) 596e601

Cairns et al., 2000). For this purpose, the pillow pressure was Table 2
placed under the lumbar curve, between first lumbar and second Intra-class correlation coefficient (ICC) values for intra-examiner reliability of the
ultrasound measurements performed in pilot study (N ¼ 10).
sacral vertebrae, and then inflated until 40 mmHg when the
subjects were at rest. The participants were asked to gently drawin Muscle Maneuver ICC (3,1)
the lower abdominal wall toward the spine for abdominal hol- TrA Abdominal Hollowing 0.92
lowing maneuver and to tighten their abdominal wall and increase Abdominal Bracing 0.80
IO Abdominal Hollowing 0.84
the lateral diameter of the waist for abdominal bracing maneuver
Abdominal Bracing 0.84
(Allison et al., 1998; Richardson et al., 1999; Jull and Richardson,
TrA ¼ Transverse abdominis; IO ¼ Internal oblique.
2000; Beith et al., 2001). All contractions were performed while
breathing normally and without visible movement of the lumbar
spine, pelvis, or rib cage. Subjects were not allowed to increase the
design ANOVA, accounting for health status (continent vs. incon-
pressure more than 10 mmHg for both hollowing and bracing
tinent), maneuvers (abdominal hollowing vs. bracing) and inter-
maneuvers (Allison et al., 1998; Cairns et al., 2000). The cursor
action of maneuvers and health status effects, was applied to test
points measured the muscle thickness between the fascial bands
the ultrasound measurement of each abdominal muscle activity
in ultrsonography. The image was frozen on the screen and the
during maneuvers between groups.
muscle thickness was measured in millimeter (mm) by the marker
Statistical significance was set at P ¼ 0.05.
(Fig. 1). The ultrasound transducer was not displaced during the
testing procedure. The participants performed three abdominal
3. Results
muscles contractions and the mean value of three contractions
was measured for the analysis. To assure reliability, all measure-
Descriptive statistics for the subjects and the thickness of the
ments were performed by one examiner. However, using 10
TrA and IO at rest in each group is presented in Table 1. Statistical
volunteers, we assessed within-day intra-tester reliability of the
analysis (independent t-test) revealed no significant difference in
ultrasound measurement. For this purpose, the whole procedure
subjects’ age (p ¼ 0.15), height (p ¼ 0.78), weight (p ¼ 0.56) and BMI
was performed twice in one day. At first the examiner completed
(p ¼ 0.67) among the two groups.
the ultrasound measurements during abdominal maneuvers in
Table 2 presents the ICC for repeat measures of the ultrasound
a subject and then after 30 min repeated the measurement
measurement for TrA and IO taken in the pilot study. All ICC values
randomly in the subjects in the same procedure to reduce the
were greater than 0.80 (Table 2). It indicates high intra-tester
memory effect.
reliability for the measurements. The BlandeAltman plot of
agreement in ultrasound measurement of the TrA during abdom-
2.3. Data analysis inal hollowing between test and retest is shown in Fig. 2. The
BlandeAltman plot demonstrated that 95% of the observations fall
The change in thickness of each abdominal muscle during each between the limits of agreement for test and retest for all ultra-
maneuver was expressed as a percentage of thickness at rest. Kol- sound measurements (TrA and IO during hollowing or bracing). The
mogroveSmirnov test was utilized to assess the normality of limits of agreement are from 1.04 mm to þ2.20 mm.
distribution for tested variables. Normal distribution was observed No significant difference was found in the thickness of the TrA
for variables in both groups. The intra-class correlation coefficient (p ¼ 0.51) and IO (p ¼ 0.78) at rest between women with and
(ICC), two-way mixed effect model, was used to assess intra- without SUI. Fig. 3 depicts the percentage of changes in thickness of
examiner reliability of the measurements. We calculated the ICC abdominal muscle in women with and without SUI during
(3,1) as described by Shrout and Fleiss (1979), because only one abdominal hollowing and bracing maneuver respectively. Detailed
judge evaluated the same population of subjects. The 95% limits of descriptive statistics (Mean  SD) are presented in Table 3. The
agreements method of reliability assessment with a confidence result of two-way mixed-design ANOVA revealed no significant
level of 95% was calculated using a BlandeAltman plot to assess health status by maneuver interaction effect for ultrasound
absolute reliability. Independent t-test was used to compare age,
height, weight and BMI among the two groups. A two-way mixed-
2.5
+1.96 SD
2.20
2.0

1.5
TrA1-hollow - TrA-2 Hollow

1.0

Mean
0.5 0.58

0.0

-0.5

-1.0 -1.96 SD
-1.04

-1.5
-4 -2 0 2 4 6 8 10
AVERAGE of TrA1-hollow and TrA-2 Hollow

Fig. 2. The BlandeAltman plot for ultrasound measurement of the TrA during abdominal
hollowing maneuver. The mean of the test (TrA1-hollow) and retest (TrA2-hollow)
scores is plotted on the X axis and the differences between two scores on the Y axis. The
Fig. 1. Ultrasound measurement of the abdominal muscles thickness. horizontal interrupted lines represent the limits of agreement.
A.M. Arab, M. Chehrehrazi / Manual Therapy 16 (2011) 596e601 599

pelvic floor on attempting a PFM contraction, EMG activity of the


external oblique muscle was greater than in controls.
It is thought that co-activation of pelvic floor and abdominal
muscles, contributes to the generation of intra-vaginal pressure to
maintain urinary continence in situations of increased intra-
abdominal pressure (Madill and McLean, 2006). Thompson et al.
(2006) believe that incontinent women are unable to perform
a correct PFM contraction using a localized muscle strategy,
therefore, use muscle substitution strategies and activate all of the
abdomino-pelvic cavity muscles. To our knowledge, the present
study is the first to directly assess the abdominal muscles activation
during specific tasks in stress incontinent women compared to
those without SUI using ultrasound measurement. However, what
we measured in this study was a voluntary contraction and not the
automatic recruitment during functional tasks.
The abdominal hollowing with the aim of deep abdominal
muscles activation and abdominal bracing maneuver with emphasis
on the activation of all antero-lateral abdominal wall muscles are
commonly used to activate abdominal muscles (Ferreira et al., 2004;
Henry and Westervelt, 2005; Teyhen et al., 2007).
Considering that performing different abdominal muscle
contractions (hollowing or bracing) increases intra-abdominal pres-
sure in a different way (Richardson et al., 1999; Junginger et al., 2010),
we assessed the abdominal muscle activation during both abdominal
hollowing and bracing maneuvers in women with SUI.
Changes in thickness of the TrA and IO muscles during abdom-
Fig. 3. The percentage of change in thickness of TrA and IO muscles during abdominal
hollowing or bracing maneuver in continent and incontinent women. TAUS ¼ inal maneuvers are measured using ultrasound imaging to indicate
Transabdominal Ultrasound a): During abdominal hollowing TAUS ¼ Transabdominal abdominal muscle activity (Critchley and Coutts, 2002; Ferreira
Ultrasound b): During abdominal bracing. et al., 2004; Henry and Westervelt, 2005; Ainscough-potts et al.,
2006; Teyhen et al., 2007). The reliability of this method in different
measurement of the percentage of change in thickness of TrA positions has been established previously (Costa et al., 2009).
(P ¼ 0.66) and IO (P ¼ 0.36) at a ¼ 0.05. The main effect of health Ultrasound measurement of the change in thickness of TrA and IO
status on the percentage of change in thickness of TrA (P ¼ 0.52) muscle has been shown to have good to high correlation with EMG
and IO (P ¼ 0.84) was not statistically significant. The percentage of amplitude of the muscles at low levels of contraction (Hodges et al.,
changes in thickness of TrA (p ¼ 0.96) and IO (p ¼ 0.53) during 2003) or at all activity levels (McMeeken et al., 2004).
abdominal hollowing was not significantly different in women with The percentage of changes in thickness of TrA during abdominal
SUI compared to those without SUI. No significant difference was hollowing was 51.66% and 52.96 in continent and incontinent
also found in the percentage of thickness change in TrA (p ¼ 0.50) women respectively. In contrast, Teyhen et al. (2009) found that the
and IO (p ¼ 0.48) during abdominal bracing between continent percent change in thickness of the TrA was 20.9% less in subjects
women and those with SUI (Table 3). with lumbopelvic pain compared to the control group. This
controversy may be due to the fact that we excluded the subjects
with current low back pain. Stuge et al. (2006) found no significant
4. Discussion
difference in TrA and IO thickness in women with long lasting
pelvic girdle pain and women who had recovered from PGP. The
Our data showed that the percentage of thickness change in TrA
percentage of changes in TrA muscle thickness was greater than the
and IO muscles during abdominal hollowing and bracing maneuver
IO muscle during both maneuvers for both groups (Table 3). Similar
was not significantly different between women with and without
finding has been reported in subjects with and without lumbo-
SUI. Thompson et al. (2006) studied the muscle activation patterns
pelvic pain (Teyhen et al., 2009).
of the abdomino-pelvic region during PFM contraction and Valsalva
Madill et al. (2009) compared the abdominal EMG amplitude
maneuver in 13 incontinent women compared to 13 healthy
during maximal voluntary PFM contractions between women with
continent women. They found no significant difference in EMG
and without SUI and showed no significant difference in EMG
amplitude of the IO muscles between two groups during Valsalva
amplitudes of the abdominal muscles between two groups.
maneuver. They also showed that in women who depressed the
However, when they categorized the women with SUI to those with
mild or severe symptoms, a significant difference was found in
Table 3 abdominal EMG amplitude between continent women and those
The (Mean  SD) for the percentage of increase in thickness of abdominal muscles with severe SUI. In the present study, we did not classify the
during abdominal hollowing or bracing maneuver in women with and without SUI. incontinent women to those with different severity of SUI
Maneuver Muscle Group P- depending on the severity of the leakage as the number of subjects
With SUI (N ¼ 10) Without SUI (N ¼ 10)
value was too small. We suggest that this study could be repeated on
continent women and subjects with different severity of SUI to
Abdominal TrA 51.66  22.79 52.96  15.2 0.96
Hollowing IO 12.38  14.29 9.18  6.5 0.53 provide more insight regarding the abdominal muscle activity in
Abdominal Bracing TrA 23.15  20.25 31.55  29.02 0.50 women with SUI.
IO 14.06  13.4 18.95  16.55 0.48 Investigators attributed SUI to differences in activation timing of
TrA ¼ Transverse abdominis; IO ¼ Internal oblique; SUI ¼ Stress urinary abdominal muscles and PFM and suggested that in treatment
incontinence. protocols for women with SUI more focus should be placed on
600 A.M. Arab, M. Chehrehrazi / Manual Therapy 16 (2011) 596e601

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