J Appl Physiol
91: 395–407, 2001.
Respiratory abdominal muscle recruitment and chest
wall motion in myotonic muscular dystrophy
VIVIANE UGALDE,1 SANDRA WALSH,1 R. TED ABRESCH,1
H. WILLIAM BONEKAT,2 AND EILEEN BRESLIN3
1
Department of Physical Medicine and Rehabilitation, 2Division of Pulmonary and
Critical Care Medicine, Department of Internal Medicine, and 3Center for Nursing
Research, University of California Davis Medical Center, Sacramento, California 95817
Received 14 August 2000; accepted in final form 20 February 2001
dynamic electromyogram; transversus abdominis; inspiratory resistance breathing; end-expiratory lung volume
a common source of morbidity and mortality in myotonic muscular dystrophy
(MMD) (7, 32). Respiratory muscle weakness, altered
central ventilatory control, and impaired ventilatory
mechanics lead to global alveolar hypoventilation, microatelectasis, and reductions in compliance (5, 17, 53).
The presence of inspiratory respiratory muscle weakness in MMD is well established, with reductions in
transdiaphragmatic pressure (43), pleural pressure
(15), compound muscle action potential amplitude of
the diaphragm (53), and maximal inspiratory pressure
(MIP) (7, 31, 32, 43, 53). However, the first indication of
pulmonary dysfunction in the MMD population is the
decline in maximal expiratory pressure (MEP) (7, 32,
43). Whereas traditionally inspiratory muscle weakPULMONARY COMPLICATIONS ARE
Address for reprint requests and other correspondence: V. Ugalde,
Dept. of Physical Medicine and Rehabilitation, 4860 Y St., Suite
3850, Sacramento, CA 95817 (E-mail: [email protected]).
http://www.jap.org
ness has been the primary cause of respiratory failure,
expiratory muscle dysfunction has recently been implicated in respiratory failure (26). Despite early declines
in expiratory muscle strength, there has been little
study of expiratory muscle action and corresponding
abdominal wall mechanics in MMD.
Until recently, knowledge of abdominal respiratory
muscle activation during respiration and their function
in normal subjects has been limited. Abdominal muscles were thought to contract as a unit for expiratory
accessory muscle action (24). Recent studies have
shown that transversus abdominis (TA) and the internal oblique (IO) muscles are selectively active in normal subjects during stimulated ventilation or exercise
(1, 2, 16, 47, 48). Expiratory recruitment of abdominal
muscles theoretically enhances inspiration by causing
passive abdominal recoil during initial inspiration,
which aids descent of the diaphragm (19, 36). An objective, indirect measure of stored potential energy for
inspiration is the reduction in end-expiratory lung volume (EELV) as seen during exercise and with pursedlip breathing (28, 44, 47).
In addition to expiratory activity, the TA and IO are
also recruited during inspiration in normal subjects
during stimulated ventilation trials (1, 2, 48). Inspiratory abdominal activity may act as a counterforce to
diaphragm descent optimizing the length-tension relationship in the area of apposition (18). Others postulate
that the inspiratory abdominal activity may act as fine
tuning of abdominal pressure and compliance and diaphragmatic descent (2) or as a braking mechanism to
prevent excessive diaphragmatic descent with hyperinflation (24, 48).
Abdominal muscles are also known postural stabilizers in the erect position and are key for trunk motion
(13, 14, 21, 29, 45). The abdominal muscle activity
during stabilization is affected by respiration (29), and
during respiration in the supine position abdominal
muscle activity is minimal (1, 2).
Abdominal muscle activation and the mechanical
response of chest wall motion in MMD subjects are less
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8750-7587/01 $5.00 Copyright © 2001 the American Physiological Society
395
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Ugalde, Viviane, Sandra Walsh, R. Ted Abresch, H.
William Bonekat, and Eileen Breslin. Respiratory abdominal muscle recruitment and chest wall motion in myotonic muscular dystrophy. J Appl Physiol 91: 395–407,
2001.—Abdominal muscles are selectively active in normal
subjects during stress and may increase the potential energy
for inspiration by reducing the end-expiratory lung volume
(EELV). We hypothesized that a similar process would occur
in subjects with myotonic muscular dystrophy (MMD), but
would be less effective, because of to their weakness and
altered chest wall mechanics. Fine-wire electromyography
(EMG) of the transversus abdominis (TA), internal oblique
(IO), external oblique, and rectus abdominis was recorded in
10 MMD and 10 control subjects. EMG activity, respiratory
inductive plethysmography, and gastric pressure were recorded during static pressure measurement and at increasing levels of inspiratory resistance breathing. EELV was
reduced and chest wall motion was synchronous only in
controls. Although the TA and IO were selectively recruited
in both groups, EMG activity of the MMD group was twice
that of controls at the same inspiratory pressure. In MMD
subjects with mildly reduced forced vital capacity, significant
differences can be seen in abdominal muscle recruitment,
wall motion, work of breathing, and ventilatory parameters.
396
ABDOMINAL MUSCLE RECRUITMENT IN MMD
METHODS
Subjects
Ten ambulatory MMD subjects from a university-based
neuromuscular disease clinic and ten normal controls voluntarily agreed to participate in this clinical investigation. The
diagnosis of MMD was based on criteria described by Harper
(27). The Human Subjects Review Board at our institution
approved the study, and all participants signed a written
consent form. All subjects were living at home, either independently or with assistive devices, were ambulatory at a
limited household level, had no clinically significant comorbid medical or pulmonary problems, and were not taking any
medications.
Subject Preparation
Measurements of pulmonary function (3), MIP, and MEP
(8) were obtained and experimental trials of breathing
against increasing inspiratory resistance were carried out by
each subject. Parameters measured during these trials were
fine-wire electromyography (EMG) of four abdominal muscles [TA, IO, external oblique (EO), and rectus abdominis
(RA) muscles], gastric pressure, respiratory inductive plethysmography, mouth pressure, oxygen saturation, and Borg
scale measurements of dyspnea, work of breathing, and fatigue.
Gastric Pressure
A Jaeger latex balloon catheter (Med Point Technologies,
Stonyridge, OH) was inserted transnasally into the stomach,
attached to a TSD104 pressure transducer (BioPac Systems,
Goleta, CA) that was connected to a DA100 amplifier (BioPac
Systems). Subjects were placed in the supine position with
approximately a 15° angle at the waist for the remainder of
the study. This position was chosen for two reasons. First,
this position eliminated the postural support EMG activity
that may occur in a sitting or standing position. Second, this
position was more comfortable for the MMD subjects than a
complete supine position. Confirmation of positive-pressure
changes in gastric pressure during inspiration with tidal
breathing verified tube placement.
Abdominal Muscle EMG
Two Teflon-coated (8-␮m) fine-wire electrodes were inserted with ultrasound guidance (Acoustic Imaging Ultrasound 5200B, 7.5-MHz transducer) into each of the four
abdominal muscles using a modification of a previously published technique (1, 6, 14, 29, 44, 47, 48). The analog EMG
signals were filtered to a bandwidth of 100 Hz to 4 kHz,
differentially amplified, digitized, and recorded simultaneously (BIOPAC Systems EMG100 amplifiers, MP100 module, and Acknowledge Software version 3.0). EMG visual and
acoustic signal quality was evaluated during isometric resistance with trunk flexion, trunk flexion with rotation, and
bilateral leg lifts. These maneuvers were also used to obtain
maximal recruitment of each of the four abdominal muscles.
At the conclusion of each study, maintenance of electrode
position was verified by administering a twitch stimulus to
each abdominal muscle (STM100A and STMISO, BIOPAC
Systems, Goleta, CA). Ultrasound visualization of the twitch
contraction within each muscle validated the maintenance of
wire electrode position throughout the study.
Specificity of muscle recruitment. With the close approximation of the lateral abdominal wall muscles to each other,
there is a concern that cross-contamination of the EMG
signal could be a source of error. The use of fine-wire electrodes and appropriate filtering limit this error (1, 42, 50). In
addition, we were able to observe independent activity of the
muscles during respiration with no contamination of the
waveforms from adjacent muscles. At the end of each study,
ultrasound visualization of a twitch stimulus within each
muscle confirmed that the wires had remained in the correct
muscle for the duration of the experiment.
Respiratory Volume
Volume was determined using respiratory inductive plethysmography (Respitrace System, Ambulatory Monitoring,
Ardsley, NY) with data collection through a DA100 amplifier
(BioPac Systems). The rib cage inductor band was placed
around the rib cage with the superior border of the band at
the level of the axilla, and the abdominal band was placed
below the lower border of the costal margin and above the
iliac crest. Bands were then calibrated as previously described (47).
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well understood. Selective TA and IO activity was seen
during pursed-lip breathing in MMD subjects in a
supine position with corresponding mechanical responses of increased gastric pressure and decreased
abdominal volume (47). In a group of MMD subjects,
abdominal paradox and chaotic breathing patterns
were associated with decreased tidal volume and increased respiratory rate. With progressive increases in
carbon dioxide rebreathing, the same group of MMD
subjects demonstrated lower minute ventilation and
lower tidal volume. With the reduced ventilatory responses, transient occlusion mouth pressure measurements were normal. Serisier et al. (43) hypothesized
that the reduction in respiratory muscle strength in
MMD subjects leads to disordered pulmonary mechanics, which result in greater inspiratory pressure
needed to produce the same ventilation.
To date there have been no studies performed in the
MMD population describing abdominal muscle recruitment patterns and corresponding mechanical changes
in chest wall motion during exercise. Therefore, we
conducted a controlled, observational study to determine the abdominal muscle recruitment during static
maximal pressure measurements and during the exercise produced by inspiratory resistance breathing
(IRB) and the subsequent effect of this recruitment on
ventilation and chest wall mechanics. We also wished
to study whether these changes resulted in an inspiratory biomechanical advantage, e.g., a reduction in
EELV. We hypothesized the following. 1) In MMD
subjects, the TA and IO would demonstrate selective
activation of the abdominal muscles during static pressure measurements and during IRB. 2) MMD subjects
would recruit the abdominal muscles at lower levels of
inspiratory resistance than controls. 3) Mechanical responses of increased gastric pressure and the relative
reduction in abdominal volume would correspond with
phasic expiratory EMG activity of the abdominal muscles. 4) Corresponding to the expiratory activation of
the abdominal muscles, a reduction in EELV would be
seen. 5) MMD subjects would exhibit asynchronous
breathing patterns when challenged with IRB in the
supine position.
ABDOMINAL MUSCLE RECRUITMENT IN MMD
Inspiratory Pressure
Subjects breathed through a Hans Rudolph non-rebreathing valve (Kansas City, MO) that was attached to a mouthpiece and connected to a resistance device (40). Inspiratory
pressure was measured using a TSD140 pressure transducer
(BioPac Systems) attached to the Hans Rudolph valve and to
a DA100 amplifier (BioPac Systems). A nose clip was used to
occlude the nostrils.
Data Collection
Data Analysis
Abdominal muscle EMG. The digitized EMG data were
rectified, and the area under the EMG curve per unit time
(AUC/second) was calculated separately for inspiration and
expiration for each muscle. This AUC/second was used as a
measure of muscle activity, such that the entire burst of the
EMG signal was analyzed (42, 50). For each muscle, the
AUC/second of EMG activity was normalized as a percentage
of the activity (AUC/second) recorded during a maximal voluntary contraction (14, 42, 47). Because of our simultaneous
sampling of 13 different channels of data for this study, the
rate at which data was sampled was limited by the maximum
throughput of the hardware. Therefore, the EMG signals
were acquired at either 200 or 500 Hz. Because these sampling rates are below the Nyquist frequency for fine-wire
EMG, we were unable to determine the frequency of the EMG
signal. However, these sampling rates do allow a statistical
Table 1. Borg scale
0
0.5
1
2
3
4
5
6
7
8
9
10
Nothing at all
Very, very slight
Very slight
Slight
Moderate
Somewhat severe
Severe
Very severe
Very, very severe
Maximal
evaluation of the AUC/second of the EMG signal. The validity
of the AUC/second as a measure of EMG activity at the lower
sampling rates was confirmed in a separate experiment.
EMG activity of the brachioradialis was recorded during 10
repetitions of flexion and extension with a fixed weight and
fixed distance using sampling rates of 10,000, 2,500, 500, and
200 Hz. ANOVA analysis of AUC/second yielded no statistically significant differences between the mean AUC/second
determined at the four sampling rates.
Respiratory volume. Total volume was determined using a
sum waveform that was the sum of the abdominal waveform
and the rib cage waveform (28, 47). End-expiratory rib cage
volume, end-expiratory abdominal volume, and EELV were
determined using these waveforms. Illustrations of recordings from a control subject and a subject with MMD during
tidal breathing and IRB at 60% MIP are shown in Figs. 1 and
2. The volume at the minimum point of the sum waveform at
end expiration during tidal breathing represents functional
residual capacity and will be called the end-tidal point. The
volume at this end-tidal point has also been called EELV (28)
(Fig. 3). The difference between EELV during tidal breathing
and the EELV during IRB was calculated. Inspiratory rib
cage volume and inspiratory abdominal volume were determined. Inspiratory and expiratory durations were determined from the time between peak and trough points on the
sum waveform.
Statistics
Two-way repeated-measures ANOVA was used to determine the overall effect of the IRB and to determine the effect
of the disease (MMD vs. control). Dunnett’s multiple-comparisons procedure was used after the ANOVA to compare each
activity level with 0% resistance. Data from each series of
breaths were averaged to get a mean value for each IRB level.
To determine whether variances were homogeneous, a Hartley’s F test was performed. If the variances were not homogeneous, appropriate transforms (either log or arc sine
square root) were performed. Pearson correlation coefficients
were used to determine the correlation between the EMG
activity of the TA and the gastric pressure. Statistical significance for all tests was accepted at P ⬍ 0.05.
RESULTS
Pulmonary Function
The MMD subjects demonstrated none to mild restrictive lung disease on the basis of FVC testing (Table 2) (30). All of the MMD subjects demonstrated
reduced MIP and MEP, with values comparable to
those previously published for MMD populations (7,
32). A plot of vital capacity vs. MIP demonstrates a
relationship in normal subjects but no relationship in
the MMD group (Fig. 4).
Abdominal Muscle Recruitment
During MEP, both MMD and control subjects recruited the TA and IO at 60–80% of the EMG activity
during a maximal contraction (Fig. 5). This activity
was significantly greater than the activity of the EO
and RA, which were recruited at 10–30% of their
maximal EMG activity. There was no significant difference in the pattern of recruitment or the percentage
of maximal EMG activity between the MMD group and
control group during MEP.
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When subject preparation was completed, each subject
breathed 10 breaths at each level of inspiratory resistance
(IRB) beginning with no resistance. Weights equal to 20, 40,
or 60% of the individual’s MIP (20% MIP, 40% MIP, and 60%
MIP, respectively) were added progressively to achieve the
desired inspiratory resistance. Once the desired pressure
was achieved, data were collected for 10 breaths. Each breath
was monitored to ensure that the correct pressure was maintained. During the IRB, the EMG of the abdominal muscles,
the gastric pressure, inspiratory pressure, and respiratory
inductive plethysmography measures of abdominal and rib
cage volumes were recorded simultaneously. A rest period of
⬃2 min was allowed between each level of resistance. At the
end of each IRB trial, oxygen saturation (Nelcor 2000) was
recorded and each subject rated the intensity of dyspnea,
fatigue, and respiratory effort by pointing to the appropriate
value on the modified Borg scale (Table 1) (33, 35). To assess
the perception of dyspnea, subjects were asked, “How short of
breath are you now?” To assess the perception of respiratory
effort, subjects were asked, “How hard are you working to
breathe?” To assess the perception of fatigue, subjects were
asked, “How tired are you now?”
397
398
ABDOMINAL MUSCLE RECRUITMENT IN MMD
Fig. 1. Sample waveform recordings of
control subject showing tidal breathing
(0%) and breathing against inspiratory
resistance (60% of maximal inspiratory
resistance). IRB, inspiratory resistance
breathing; Trans, transversus; Vol,
volume; Insp, inspiration.
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Fig. 2. Sample waveform recordings of
myotonic muscular dystrophy (MMD)
subject showing tidal breathing (0%)
and breathing against inspiratory resistance (60% of maximal inspiratory
resistance).
ABDOMINAL MUSCLE RECRUITMENT IN MMD
399
Fig. 4. Relationship between maximal inspiratory pressure (MIP)
and forced vital capacity (FVC) in control and MMD subjects. Values
are means ⫾ SE. Solid line, best-fit regression for the controls (r2 ⫽
0.26); dotted line, best-fit regression for the MMD subjects (r2 ⫽ 0.56).
During MIP, all of the abdominal muscles in the
control group were recruited at 20–30% of their maximal EMG activity. There was no difference in the level
of recruitment among the four abdominal muscles (Fig.
5). In the MMD group, the TA and IO recruited at
55–65% of their maximal EMG activity, which was
significantly greater than the activity of the EO and
RA (20 and 15% of their maximal EMG activity, respectively). In addition, the TA and IO muscles in the MMD
group demonstrated significantly more EMG activity
during MIP than the TA and IO muscle of the control
group.
During tidal breathing, there was no significant
EMG activity in either MMD or control subjects. The
EMG activity of the abdominal muscles during IRB
(Fig. 6) was much lower (2 and 12% of maximal EMG)
Table 2. Pulmonary function data of subjects
Number and sex
Age, yr
FVC, l
FVC, %predicted
FEV1, l
FEV1, %predicted
FEV1/FVC
FEV1/FVC, %predicted
MIP, cmH2O
MEP, cmH2O
Control
MMD
5 Males and 5
females
36.8 ⫾ 12.4
4.8 ⫾ 1.1
104.6 ⫾ 9.4
3.9 ⫾ 0.9
106.9 ⫾ 10.3
0.81 ⫾ 0.08
102.6 ⫾ 8.7
⬎100.8 ⫾ 35.8*
⬎126.1 ⫾ 29.2†
9 Males and 1
female
42.7 ⫾ 8.3
3.8 ⫾ 0.0.6‡
80.6 ⫾ 13.7‡
3.2 ⫾ 0.5
85.6 ⫾ 15.8‡
0.84 ⫾ 0.03
107 ⫾ 9.0
50.9 ⫾ 27.8‡
63.3 ⫾ 20.5‡
Values are means ⫾ SD. MMD, myotonic muscular dystrophy;
FVC, forced vital capacity; FEV1, forced expiratory volume in 1 s.
MIP, maximal inspiratory pressure; MEP, maximal expiratory pressure. * 2 Controls exceeded maximum for our equipment (150). † 5
Controls exceeded maximum for our equipment (150). ‡ P ⬍ 0.05,
MMD different from control.
Patterns of Rib Cage and Abdominal Motion
During tidal breathing, control subjects exhibited
synchronous motion (Fig. 1) with relatively equal contributions of the abdomen and rib cage to inspiratory
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Fig. 3. Illustration with sample waveforms to demonstrate volume
definitions with various breathing maneuvers. *, Line representing
the end-tidal point. EELV, end-expiratory lung volume.
than the EMG activity during MIP and MEP (15 and
80%) testing in both MMD and control groups. As the
inspiratory resistance challenge increased, the recruitment of the abdominal muscles increased. However,
even at 60% MIP, the recruitment of the TA, the most
active of the abdominal muscles, was only ⬃10% of the
EMG activity generated during a maximal contraction
in both groups.
The EMG activity of the four abdominal muscles of
the two groups during IRB is summarized during inspiration (Fig. 6, A and C) and expiration (Fig. 6, B and
D). When compared with tidal breathing, the MMD
group and control group had significant phasic recruitment of the TA and IO during inspiration and expiration. Neither the control group nor the MMD group
demonstrated significant recruitment of the RA. Both
the control group and the MMD group significantly
recruited the EO at 60% MIP during inspiration only.
Because the MIP of the MMD group was approximately one-half of the MIP of the control group, the
abdominal muscle recruitment by the MMD group occurred during IRB at a significantly lower absolute
pressure (cmH2O) than the pressure at which the abdominal muscle recruitment of the control group occurred (P ⫽ 0.034) (Fig. 7).
Qualitative analysis of the timing of the TA and IO
muscle activity demonstrated a variety of patterns, as
shown in Tables 3 and 4. There was no general pattern
of recruitment activity in either the MMD or control
group during either inspiration or expiration. Phasic
activity occurred in several patterns: phasic activity
throughout inspiration and expiration in both the TA
and IO, only end-inspiratory activity, or isolated initial
expiratory activity. Both groups demonstrated these
variations. Interestingly, there was never a pattern of
isolated end expiratory activity in either group that
would theoretically correspond with reduction in
EELV.
400
ABDOMINAL MUSCLE RECRUITMENT IN MMD
Fig. 5. Electromyogram (EMG) activity of the abdominal muscles as percentage of maximal contraction during MEP (A) and MIP (B) determinations.
Values are means ⫾ SE. TA, transversus abdominis;
IO, internal oblique: EO, external oblique; RA, rectus abdominis. *Significant difference between control and MMD groups, P ⬍ 0.05.
Fig. 6. EMG activity of the abdominal
muscles. A: control group during inspiration. B: control group during expiration. C: MMD group during inspiration. D: MMD group during expiration.
*Significant difference between each
level of IRB and tidal breathing for
each muscle, P ⬍ 0.05. Values are
means ⫾ SE.
its tidal volume. During expiration, the abdominal wall
had an outward motion (increasing volume), whereas
the rib cage was moving inward (decreasing volume).
There was a significantly greater reduction in EELV
of the control group with increased IRB than in the
MMD subjects. There was a slight reduction in EELV
in the MMD group (Fig. 8) at 20% IRB but none at 40%
or 60% IRB.
Gastric Pressure
There was no effect of IRB on end-inspiratory gastric
pressure in either group. During expiration, gastric
pressure decreased to its nadir at end expiration.
There was no increase in gastric pressure with abdominal EMG activity using group analysis. However, the
EMG levels were low and data were variable, with
some individuals demonstrating increased gastric
pressure. Because of the variability in expiratory gastric pressure, no correlation was found between gastric
pressure, abdominal EMG activity, and abdominal motion in either group. With MIP and MEP determinations, where the EMG activity was high, we did observe
significantly increased gastric pressure. During MIP,
the gastric pressure of both the MMD and control
groups was correlated to the EMG activity of the TA
(MMD r ⫽ 0.73, control r ⫽ 0.92). This was not true
during MEP, where the EMG activity of the TA corre-
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tidal volume. The tidal volume increased from 851 ml
at 0% IRB to 1,383 ml at 20% IRB and did not significantly change with further increases in IRB levels in
the control group (Table 5). With increasing levels of
IRB, the inspiratory rib cage and abdominal motion
was always outward. However, at 60% MIP, the inspiratory abdominal motion was less outward (reduced
volume) than at lower resistance, which is consistent
with mild asynchrony. As a result, the contribution of
abdomen to the total volume went from 32% at 20%
MIP to 17% at 60% MIP. During expiration in the
control group, both the rib cage and abdomen decreased in volume and their motion was inward.
The rib cage and abdomen of the MMD group were
synchronous during tidal breathing (Fig. 2). During
increasing IRB, the inspiratory motion of the abdominal wall was progressively inward with a resulting
decrease in abdominal volume. It decreased to such an
extent that the contribution of the abdomen to tidal
volume was negative at 40 and 60% IRB. The rib cage
demonstrated outward motion during inspiration with
all levels of IRB (Table 5). In the MMD subjects at 20%
IRB, the rib cage contributed 89% of the total volume
and 11% was contributed by the abdomen. By 60%
MIP, the MMD group exhibited abdominal paradoxical
breathing during inspiration with the contribution of
the rib cage increasing to 124% of its tidal volume,
whereas the abdominal volume decreased to ⫺24% of
401
ABDOMINAL MUSCLE RECRUITMENT IN MMD
Fig. 7. EMG activity of the TA as a function of the mouth pressure
during IRB. Max, maximum.
lated with the gastric pressure (r ⫽ 0.62) for the control
group, but the EMG and gastric pressure had no correlation in the MMD group (r ⫽ ⫺0.01).
The tidal volume of the control group was two to
three times the volume seen in the MMD group at
each level of resistance breathing (Table 5). The tidal
volume of both groups increased significantly from
0% to 20% MIP, but it did not significantly change as
the inspiratory resistance was increased to 40–60%
MIP. As has been previously observed, the use of a
mouthpiece caused a significant increase in the tidal
volume in the control group (445 ⫾ 46 ml with no
mouthpiece to 916 ⫾ 116 ml when a mouthpiece was
used) (4, 23, 49). However, the MMD group had no
change in tidal volume with the insertion of the
DISCUSSION
The purpose of this study was to determine how
respiratory muscular weakness associated with MMD
affects abdominal muscle recruitment, chest wall motion, and pulmonary function. This was done by subjecting MMD and control subjects to static pulmonary
pressure measurements and an exercise stress that
Table 3. EMG activity of the transversus abdominis
0% IRB
60% IRB
Inspiration
Subject No.
Beginning
Middle
Expiration
End
Beginning
Inspiration
Middle
End
Expiration
Beginning
Middle
End
Beginning
Middle
End
⫹
⫺
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Control
1
2
3
4
5
6
7
8
9
10
⫺
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1
2
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4
5
6
7
8
9
10
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MMD
⫺
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⫺
EMG, electromyogram; IRB, inspiratory resistance breathing; ⫺, absence of EMG activity; ⫹, presence of EMG activity.
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Ventilatory Parameters
mouthpiece; tidal volume without a mouthpiece was
343 ⫾ 42 ml and with a mouthpiece the volume was
369 ⫾ 49 ml.
Respiratory rate was significantly greater in the
MMD group than the control group at all levels of IRB.
Increasing the resistance did not significantly alter the
respiratory rate in either the control or MMD groups.
The higher respiratory rate in the MMD group did not
compensate for the reduction in tidal volume, and, as a
result, the minute ventilation of the MMD group was
significantly less than that of the control group at all
levels of resistance. Both groups had a significant increase in minute ventilation with increasing inspiratory resistance. Despite the fact that the minute ventilation of the MMD group was ⬃50% of the control
group, oxygen saturation was not significantly different between the two groups.
Perceptions of breathing. MMD and control groups
demonstrated statistically significant increases in all
three perceptions of breathing, particularly at 40 and
60% MIP. The two groups did not differ in their perception of dyspnea or fatigue, but the MMD group
perceived significantly greater respiratory effort at the
higher IRB levels than the control group (Table 6).
402
ABDOMINAL MUSCLE RECRUITMENT IN MMD
Table 4. EMG activity of the internal oblique
0% IRB
60% IRB
Inspiration
Subject No.
Beginning
Middle
Expiration
End
Beginning
Inspiration
Middle
End
Expiration
Beginning
Middle
End
Beginning
Middle
End
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Control
1
2
3
4
5
6
7
8
9
10
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1
2
3
4
5
6
7
8
9
10
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MMD
⫺, Absence of EMG activity; ⫹, presence of EMG activity.
was created by breathing against increasing levels of
inspiratory resistance.
Our MMD subjects demonstrated significant respiratory muscle weakness, as indicated by reduced MIP
and MEP, although they had normal to minimally
reduced FVC. These results are consistent with other
reports of static pressure measurements in MMD populations (7, 9, 10, 53).
Table 5. Ventilation and gastric pressure
Resistance, %MIP
Mouth pressure, cmH2O
Control*†‡
MMD
Tidal volume, ml
Control*†
MMD
Rib volume, ml
Control*†
MMD
Abdominal volume, ml
Control*†
MMD
Respiratory rate, breaths/min
Control*
MMD
Minute ventilation, l/min
Control*†
MMD
Gastric pressure (end inspiratory), cmH2O
Control*
MMD
Oxygen saturation, %
Control
MMD
0
20
40
60
2.9 ⫾ 0.3
2.0 ⫾ 0.3
21.8 ⫾ 3.2
15.1 ⫾ 1.5
42.3 ⫾ 6.6
27.8 ⫾ 3.6
61.0 ⫾ 11.4
33.5 ⫾ 3.6
851 ⫾ 108
369 ⫾ 49
1,383 ⫾ 229
576 ⫾ 117
1,388 ⫾ 203
572 ⫾ 96
1,067 ⫾ 157
540 ⫾ 78
439 ⫾ 96
182 ⫾ 20
927 ⫾ 146
511 ⫾ 99
979 ⫾ 119
646 ⫾ 97
879 ⫾ 126
668 ⫾ 119
412 ⫾ 40
186 ⫾ 39
456 ⫾ 105
64 ⫾ 59
409 ⫾ 108
⫺73 ⫾ 66
189 ⫾ 38
⫺129 ⫾ 90
10.7 ⫾ 1.0
16.1 ⫾ 1.6
10.2 ⫾ 1.4
14.7 ⫾ 1.4
10.8 ⫾ 1.4
15.8 ⫾ 1.7
11.9 ⫾ 1.3
15.1 ⫾ 1.6
9.7 ⫾ 1.4
5.5 ⫾ 0.4
14.4 ⫾ 2.4
7.8 ⫾ 1.3
16.3 ⫾ 3.1
8.4 ⫾ 1.1
15.4 ⫾ 3.3
7.3 ⫾ 1.0
7.6 ⫾ 0.7
10.6 ⫾ 1.2
7.8 ⫾ 1.3
10.8 ⫾ 1.4
8.4 ⫾ 1.2
13.9 ⫾ 2.6
6.9 ⫾ 1.2
16.5 ⫾ 4.6
98.9 ⫾ 0.4
96.7 ⫾ 1.1
99.0 ⫾ 0.9
97.6 ⫾ 0.9
99.5 ⫾ 0.3
97.4 ⫾ 0.9
98.0 ⫾ 0.9
97.6 ⫾ 1.0
Values are means ⫾ SE. Results of 2-way ANOVA: * Disease effect, P ⬍ 0.05. † Inspiratory resistance effect, P ⬍ 0.05. ‡ Disease-resistance
interaction, P ⬍ 0.05.
Downloaded from http://jap.physiology.org/ by 10.220.33.4 on June 18, 2017
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403
ABDOMINAL MUSCLE RECRUITMENT IN MMD
Fig. 8. End-expiratory lung volume at each level of IRB. Values are
means ⫾ SE.
Hypothesis 1: Abdominal Muscles Are Selectively
Activated During Respiration
Table 6. Respiratory sensations using Borg scale
Resistance, %MIP
Dyspnea
Control*
MMD
Work of breathing
Control*†
MMD
Fatigue
Control*
MMD
0
20
40
60
0. ⫾ 0.1
0. ⫾ 0.1
1. ⫾ 0.4
1. ⫾ 0.4
2.1 ⫾ 0.5
3.5 ⫾ 0.8
3.4 ⫾ 0.8
4.6 ⫾ 1.0
0. ⫾ 0.1
0. ⫾ 0.1
2. ⫾ 0.5
2. ⫾ 0.3
3.5 ⫾ 0.5
5.8 ⫾ 0.9
4.9 ⫾ 0.7
6.9 ⫾ 0.8
0. ⫾ 0.1
0. ⫾ 0.1
1. ⫾ 0.3
2. ⫾ 0.5
2.0 ⫾ 0.4
3.5 ⫾ 0.7
2.9 ⫾ 0.7
4.9 ⫾ 0.9
Values are means ⫾ SE. Results of 2-way ANOVA: * Inspiratory
resistance effect, P ⬍ 0.05. † Disease-resistance interaction, P ⬍
0.05.
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In the past, abdominal muscles were considered to
act as a single unit during respiration (24). With the
development of more sophisticated EMG techniques, it
has been shown that individual abdominal muscles
contribute to breathing in normal controls (1, 2, 12, 16,
29, 45, 47, 48) and in subjects with chronic obstructive
pulmonary disease (41). To our knowledge, this is the
first study to describe abdominal muscle activity in
MMD subjects. This study demonstrates selective activity of the abdominal muscles in MMD subjects and
normal subjects during static pressure testing.
MMD and control subjects had different patterns of
abdominal muscle recruitment during MIP testing; in
the control group, all four abdominal muscles were
recruited as a unit with equal activity, whereas the TA
and IO muscles of the MMD group were recruited to a
greater degree than the EO and RA. This pattern
suggests that the TA and IO are accessory muscles of
inspiration in persons with weakened respiratory muscles. The abdominal muscle activity observed during
inspiratory effort, in this case, may be due to an attempt to maximize the contraction of the diaphragm in
the zone of apposition (18, 36).
In contrast to MIP, there were no differences between the MMD and control groups in the recruitment
patterns and percentage of EMG activity of the abdominal muscles during MEP testing. In both groups, the
TA and IO muscles had greater activity than the EO
and RA muscles. There are no prior reports of recruitment patterns during MEP testing. However, De
Troyer et al. (16) reported that, in seated, normal
subjects, the TA, EO and RA activity was equal during
expulsive maneuvers from functional residual capacity. Hodges et al. (29) and Goldman et al. (24) found
that all four abdominal muscles were collectively active
in expulsive maneuvers or during cough. These differences in recruitment may be due to the differences in
the method or differences in posture.
The expiratory activity of the abdominal muscles
observed during IRB exercise in both groups during
expiration was as expected from results of previous
studies in normal subjects (1, 2, 16, 25, 38, 48). In our
study, the patterns of recruitment were the same for
both groups. The TA and IO were recruited at lower
levels of IRB than the EO and RA. The EO was activated only at the highest level, and the RA was never
recruited. The consecutive recruitment of the TA, IO,
EO, and the RA has been seen in normal subjects (1, 2,
48) and in chronic obstructive pulmonary disease subjects (16) during carbon dioxide rebreathing.
We also observed EMG activity of the abdominal
muscles during inspiration. Abe et al. (2) reported
inspiratory abdominal muscle activity during carbon
dioxide rebreathing in normal subjects. However, the
activity they observed occurred primarily at the beginning of inspiration and was called postexpiratory expiratory activity (2). Hodges et al. (29), using inspiratory
resistance, reported midinspiratory activity when normal subjects were at rest in a standing position. During
upright posture, gravitational forces pull the abdominal contents down and outward along with the diaphragm. Abdominal muscles must contract to maintain
a favorable diaphragm position. With abdominal contraction in the upright position, abdominal compliance
decreases. Thus both tonic activity to counteract gravitational forces and selective contraction with respiration occur in upright postures (1, 2, 16, 29). The inspiratory EMG activity observed was quite variable
from person to person, with activity occurring during
the beginning, middle, and end of inspiration (Table 3).
Differences between our study and others may be due
to differences in the challenged breathing protocol
and/or differences in posture (supine vs. standing or
sitting).
Inspiratory abdominal muscle contraction may theoretically improve biomechanical advantage by increasing abdominal pressure along the costal margins
to provide a counterforce for the descending diaphragm
at the area of apposition. This counterforce allows
expansion of the distal rib cage, thereby placing the
costal diaphragm fibers in the zone of apposition in a
favorable biomechanical position to enhance the inspiratory force of the crural diaphragm (17). Other
theories as to the presence of inspiratory abdominal
activity include possible “braking” of inspiration and
prevention of hyperinflation of the lungs (1, 39).
404
ABDOMINAL MUSCLE RECRUITMENT IN MMD
In this study, no significant EMG activity was recorded during tidal breathing in the supine position
in either group. The absence of abdominal muscle activity in the supine posture with quiet breathing concurs with other reports of tidal breathing in normal
subjects (12, 21, 24, 38, 45). However, Abe et al. (1)
observed very slight, but significant, expiratory activity during supine tidal breathing in normal subjects.
The difference between our study and that of Abe et al.
may be interpretation of what constitutes significant
activity.
Hypothesis 2: MMD Subjects Recruit Abdominal
Muscles at an Inspiratory Resistance That is
Significantly Less Than the Resistance Required
for the Recruitment of Abdominal Muscles in
Control Subjects
Hypothesis 3: Mechanical Responses to Expiratory
Abdominal EMG Activity Are an Increase in
Gastric Pressure and a Relative Reduction in
Abdominal Volume
In the past, studies have assumed that an increase in
expiratory gastric pressure indicated an increase in
abdominal muscle recruitment (37). Prior studies have
found an association between abdominal muscle activity and gastric pressure during expiration with subjects in upright positions (14, 38). In our IRB study,
which was performed with subjects in a supine position, neither the MMD group nor the control group
demonstrated an association between EMG activity
and peak gastric pressure during the IRB protocol.
Although both the control and MMD groups had statistically significant EMG activity of the TA and IO
during IRB exercise, the level of EMG activity was low
(2–14% of maximal EMG activity), even at the highest
level of IRB exercise (60% IRB). This low level of
abdominal EMG activity during expiration in IRB may
not have been great enough to produce an increase in
gastric pressure. However, during MIP, where there
was high EMG activity, there was a high correlation
between TA EMG activity and gastric pressure in the
control group (r ⫽ 0.92) and in the MMD group (r ⫽
0.79), respectively. During MEP, even though the EMG
activity of both the MMD and control groups was high,
there was a correlation between gastric pressure and
TA activity only in the control group (r ⫽ 0.62) and not
Hypothesis 4: Expiratory Activity of the Abdominal
Muscles is Associated With a Reduction in EELV
A theoretically advantageous mechanical consequence of expiratory abdominal muscle activity is a
reduction in EELV (Fig. 3). Reduction in EELV could
assist inspiration by two mechanisms. 1) Prolonged
expiration and increased expiratory flow pushes the
diaphragm into the thorax. This cephalad displacement of the diaphragm during expiration increases the
elastic energy of the diaphragm. Initial inspiration can
then be passive. Thus the abdominal muscles indirectly assist in the work of inspiration. 2) Reduction in
EELV also lengthens the diaphragmatic fibers, placing
them in a more optimal position in the muscle’s lengthtension curve with contraction, especially if the diaphragm is flattened (1, 16, 28, 51, 52). We observed
decreased EELV in control subjects, but not in the
MMD group. Our control subjects had a reduction in
the EELV of 0.25 liters, which is 5% of vital capacity
(0.25 liters/4.8 liters), whereas the MMD subjects had
a reduction of 2% (0.1 liters/3.8 liters). The lack of
reduction of EELV in MMD subjects is likely due to
disordered breathing patterns. Even though the expiratory abdominal muscle activity was small in control
subjects, it may be responsible for the reduction in
EELV that we observed. Henke et al. (28) found a
reduction in EELV during exercise and hypothesized
that this reduction aids inspiration by optimizing diaphragmatic length and permitting elastic recoil of the
chest wall. The clinical significance of the reduced
volume observed in our study is unclear.
Downloaded from http://jap.physiology.org/ by 10.220.33.4 on June 18, 2017
Although the abdominal muscle activities of the
MMD and control groups appear to be similar when
measured as a percentage of their MIP (Fig. 6), the
absolute pressure at which the muscles of the MMD
group were recruited is one-half that at which the
controls recruited the muscles (Fig. 7). When measured
at the same inspiratory pressure (cmH2O), MMD subjects demonstrated approximately twice the EMG activity of control subjects (Fig. 6). The greater EMG
activity for the same level of resistance in the weakened muscles of MMD subjects is consistent with myopathic recruitment principles (20, 34). To lift an identical load, a dystrophic muscle typically recruits a
greater number of motor units than a normal muscle.
in the MMD group (r ⫽ ⫺0.01). However, the lack of
correlation of abdominal activity in MEP with gastric
pressure in only the MMD group is difficult to explain,
but it may be related to several observations. 1) At 60%
IRB in the MMD group, the abdominal motion was
outward during expiration, whereas the abdominal
motion of the controls was inward during expiration.
The outward motion of the abdomen during expiration
in the MMD group may be enough to dissipate any
increase in gastric pressure generated by abdominal
muscle contraction. It is likely that, at maximal expiratory effort, a similar abdominal motion pattern
would be demonstrated. Unfortunately, we do not have
reliable abdominal motion measurements during MEP
testing to confirm this explanation. 2) A decrease in
lung compliance during expiration in the MMD group
may also lead to lower gastric pressure given the supine posture. However, we did not have a measure of
lung compliance. 3) The marked weakness of abdominal muscles and an inability to generate significant
gastric pressure in the MMD group is another possible
explanation. However, the correlation of abdominal
EMG activity and gastric pressure during MIP measurements makes this explanation less likely. It is
clear that further study is needed to understand the
relationship between abdominal muscle activity and
gastric pressure in MMD subjects.
ABDOMINAL MUSCLE RECRUITMENT IN MMD
Hypothesis 5. MMD Subjects Exhibit Dysynchronous
Breathing Patterns When Challenged With Low
Levels of Inspiratory Resistance and at Higher
Levels of Inspiratory Resistance Demonstrate
Abdominal Paradox
The reduced rib cage volumes that we observed at all
IRB levels in comparing the MMD subjects with control subjects may be associated with decreased rib cage
compliance. However, comparing the relative contribution of the ribs vs. the abdominal volumes to the tidal
volume, we found marked increases in the rib cage
contribution during increasing workloads. Our findings indicate that the rib cage expands to a greater
degree than the abdomen with increasing IRB. Thus
the rib cage compliance is probably not reduced in our
subjects, although we did not have a direct measure of
compliance. Teramoto et al. (46) found a decrease in rib
cage contribution in upright exercise in the aged compared with younger controls. Unlike the aged controls,
our MMD subjects can expand the rib cage to increase
tidal volume during exercise. Although controls demonstrated a high correlation between vital capacity and
MIP (r ⫽ 0.76; Fig. 4), there was no significant correlation in the MMD group in our study. De Troyer et al.
(17) suggest that, when MIP does not directly correlate
with vital capacity, factors other than muscle weakness are the cause; e.g., poor lung compliance may
contribute to alterations in vital capacity in the MMD
group. Esophageal pressure measurements would have
been helpful in understanding lung compliance in our
subjects (18). A potential bias in our study was the
difference in gender distribution between the two
study groups, with the control group having more female subjects than the MMD group. In examining the
control group for this bias, we found no gender differences in their EMG responses. However, the female
controls had significantly smaller rib cage volume and
abdominal volume than the male controls. Because the
MMD subjects had significantly smaller volumes than
the control group did, this gender bias would reduce
the significance found between the MMD and control
groups and therefore did not affect the interpretation
of our results.
Implication and Summary
Observations from this study increase our understanding of basic respiratory physiology in MMD. In a
group of MMD subjects with normal or mild reduction
in FVC, MEP was markedly reduced, indicating abdominal muscle weakness. The recruitment patterns of
the abdominal muscles overall were similar to those of
normal subjects, demonstrating selective activity of the
TA and IO. However, MMD subjects recruited the
abdominal muscles at lower absolute pressure during
IRB compared with control subjects. In addition, abdominal muscle EMG activity of MMD subjects is significantly higher than that of controls during IRB
when compared at the same absolute pressures. This is
consistent with recruitment patterns observed with
myopathic muscles. Despite this greater EMG activity
of the abdominal muscles seen in the MMD subjects,
corresponding mechanical changes (increased gastric
pressure and inward abdominal motion) were not seen
in the MMD group; this was likely due to the severity
of the abdominal weakness. Abdominal wall motion
was dyssynchronous and paradoxical in the MMD
Downloaded from http://jap.physiology.org/ by 10.220.33.4 on June 18, 2017
In our study, MMD subjects demonstrated synchronous breathing patterns during tidal breathing. These
results differ from those of Serisier et al. (43), who in
his study of MMD patients at rest, observed abdominal
paradox in 1 of 19 subjects and chaotic breathing patterns in 7 of 19 subjects. The differences may be due to
greater severity of the dystrophy in the MMD subjects
in the study of Serisier et al. Nevertheless, we did show
that MMD subjects exhibited abdominal asynchrony
when breathing against low levels of inspiratory resistance, and 6 of 10 exhibited paradoxical abdominal
motion at the highest level of resistance (60% IRB). In
comparison, control subjects exhibited a synchronous
pattern of breathing until 60% MIP, when their breathing became asynchronous with 1 of 10 showing paradoxical abdominal motion at the highest level of resistance.
Ewig et al. (22) reported that individuals who were
lacking abdominal muscles (prune belly syndrome)
breathed synchronously when in the supine position
but exhibited abdominal paradox during exercise. Our
MMD subjects with abdominal muscle weakness demonstrate chest wall mechanics similar to those of subjects with absent abdominal muscles.
Ewig et al (22) also noted that the asynchrony caused
inefficient breathing patterns, respiratory fatigue, and
increased work of breathing. Our observations showed
a significant increase in the perception of work of
breathing in both groups with increasing levels of IRB.
However, when the MMD group was breathing more
asynchronously (Table 4), they had a greater increase
in the perception in the work of breathing than the
control group. This increased perception may be related to the increased activation of the weakened muscles or to the alterations of chest wall motion of MMD
group. Although the perception of work of breathing
was greater in the MMD group, we found that the two
groups had similar increases in the perception of dyspnea and fatigue with increasing IRB levels.
Work by Cala et al. (11) suggests that dyssynchronous patterns of breathing may also be related to chest
wall compliance, as well as to abdominal muscle weakness. Particularly in the supine position, changes in rib
cage motion can affect abdominal wall motion without
any abdominal activity because of the connection between the rib cage and abdomen (11). It is possible that
the rib cage muscles, which are involved in active
expiration, could be partially responsible for the asynchrony. A limitation of the present study is the lack of
a direct measure of diaphragmatic or rib cage muscle
activity to assist in the understanding of changes in rib
cage volume and compliance. However, in a study of rib
cage muscles using surface EMG, MMD subjects demonstrated expiratory lower rib cage muscle activity,
whereas there was no activity in the control group (31).
405
406
ABDOMINAL MUSCLE RECRUITMENT IN MMD
group with exercise. The theoretical advantage of expiratory abdominal activity in decreasing EELV was
seen only in controls and not in MMD subjects. The
inspiratory EMG activity we observed may provide a
biomechanical advantage by providing support to enhance the inspiratory descent of the crural diaphragm.
During MIP testing, the MMD group demonstrated
greater activity compared with controls, indicating the
TA and IO are likely accessory muscles of inspiration
in MMD. Marked differences in chest wall mechanics
and minute ventilation during exercise, most likely due
to abdominal muscle weakness, can be seen in MMD
subjects with minimal to no loss in FVC. As a result,
inefficient patterns of breathing lead to increased perception in work of breathing.
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We thank Dr. Rahman Azari for generously advising us on statistical procedures, Julie Ann Walby for technical assistance, and
Michael Cronan for providing ultrasound consultation.
This work was supported by grants H133B30026 and
H133B980008 from the National Institute on Disability and Rehabilitation Research and by an Educational Research Foundation
grant from the American Academy of Physical Medicine and Rehabilitation.
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