Address correspondence to:Martin J. Tobin, M.D.
Division of Pulmonary and Critical Care Medicine
Edward Hines, Jr. VA Hospital, 111N
5th Avenue and Roosevelt Road
Hines, IL 60141
Tel: (708) 202-2705
STERNOMASTOID, RIB-CAGE AND EXPIRATORY MUSCLE ACTIVITY DURING
Sairam Parthasarathy, Amal Jubran, Franco Laghi, Martin J. Tobin
Running title: Respiratory muscle activity during weaning failure
From the Division of Pulmonary and Critical Care Medicine, Edward Hines Jr. Veterans
Administration Hospital, and Loyola University of Chicago Stritch School of Medicine,
Hines, Illinois 60141
Supported by grants of the Veterans Administration Research Service.
Page 1 of 36
Articles in PresS. J Appl Physiol (March 29, 2007). doi:10.1152/japplphysiol.00904.2006
Copyright © 2007 by the American Physiological Society.
We hypothesized that patients who fail weaning from mechanical ventilation
recruit their inspiratory rib-cage muscles sooner than they recruit their expiratory muscles,
and that rib-cage muscle recruitment is accompanied by recruitment of sternomastoid
muscles. Accordingly, we measured sternomastoid electrical activity and changes in
esophageal (∆Pes) and gastric pressure (∆Pga) in 11 weaning-failure and 8 weaning-
success patients. At the start of trial, failure patients exhibited a higher ∆Pga-to-∆Pes
ratio than did success patients (p=0.05), whereas expiratory rise in Pga was equivalent in
the two groups. Between the start and end of the trial, failure patients developed further
increases in ∆Pga-to-∆Pes ratio (p< 0.0014) and the expiratory rise in Pga also increased
(p < 0.004). At the start of trial, sternomastoid activity was present in 8 of 11 failure
patients contrasted with 1 of 8 success patients. Over the course of the trial, sternomastoid
activity increased by 53.0±9.3% in the failure patients (p=0.0005), whereas it did not
change in the success patients. Failure patients recruited their respiratory muscles in a
sequential manner. The sequence began with activity of diaphragm and greater-than-
normal activity of inspiratory rib-cage muscles; recruitment of sternomastoids and rib-
cage muscles approached near maximum within four minutes of trial commencement;
expiratory muscles were recruited slowest of all. In conclusion, not only is activity of the
inspiratory rib-cage muscles increased during a failed weaning trial, but respiratory
centers also recruit sternomastoid and expiratory muscles. Extradiaphragmatic muscle
recruitment may be a mechanism for offsetting the effects of increased load on a weak
Key words: sternomastoid muscles, respiratory muscles, mechanical ventilation, weaning
Page 2 of 36
Patients who fail a trial of weaning from mechanical ventilation develop marked
and progressive increases in mechanical load (16; 40; 49). In an attempt to maintain
alveolar ventilation over the course of a failed weaning trial, patients increase respiratory
effort to more than four times the normal level (15; 16; 19). In addition to experiencing an
increased load, patients undergoing ventilator weaning display severe diaphragmatic
weakness (19). Accordingly, patients failing a weaning trial may become more dependent
on assistance from other muscles of respiration in achieving the heightened respiratory
During resting tidal breathing, patients with chronic obstructive pulmonary
disease (COPD) recruit both their inspiratory rib-cage muscles and expiratory muscles
(31; 32; 51) in order to compensate for an overloaded and disadvantaged diaphragm. As
patients exercise to exhaustion, they further recruit their rib-cage muscles, and the
magnitude of this recruitment appears to depend on rib-cage muscle reserve during
resting breathing (51). With further increases in respiratory load, patients also recruit their
expiratory muscles (23; 51). This pattern of respiratory muscle activity suggests the
existence of a possible hierarchy of muscle recruitment (specific muscle groups recruited
in a particular sequence) when patients with a weakened diaphragm are subjected to
increased respiratory loads.
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We previously showed that weaning-failure patients displayed greater recruitment
of rib-cage and expiratory muscles than did weaning-success patients (19). We did not,
however, separate the relative contribution of each muscle group or the timing of
recruitment. Defining the relative activity of respiratory muscle groups during a failed
weaning trial may shed light on how the respiratory controller apportions work between
these muscle groups in patients with acute respiratory failure.
It is commonly believed that patients recruit not only the scalene muscles but also
the sternomastoids when they develop respiratory distress (8; 25; 29). This reasoning is
based on findings from surface electromyographic (EMG) recordings of the sternomastoids
or direct palpation of the neck muscles (3; 11). Surface EMG recordings of the
sternomastoids, however, may be unreliable in determining sternomastoid activity because
of contamination from scalene-muscle activity (9). Based on surface EMG recordings, it had
generally been accepted that patients with severe COPD commonly recruit their
sternomastoids (13; 42; 43). When EMG recordings were obtained using needle electrodes,
however, only 4% of patients displayed phasic activity of the sternomastoids; in contrast,
scalene contractions were present in all patients (9). That few patients with COPD recruit
their sternomastoids suggests that these muscles have a high threshold for activation.
Sternomasotid recruitment has also been reported in patients with extensive respiratory
muscle weakness, such as patients with transection of the upper cervical cord (7). Because
weaning-failure patients display respiratory muscle weakness and experience a rapid and
progressive increase in respiratory load, it is conceivable that the sternomastoids might be
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recruited in the early phase of a weaning trial. The pattern of sternomastoid activation
during a weaning trial using with needle electrodes has not been previously reported.
Accordingly, the aim of the study was to examine for the first time the pattern of
recruitment of inspiratory rib-cage, expiratory and sternomastoid muscles during a trial of
spontaneous breathing. We hypothesized that weaning-failure patients recruit their rib-
cage muscles and sternomastoids at an earlier point in time than they recruit their
expiratory muscles during the course of a weaning trial.
Nineteen critically ill male patients who were receiving mechanical ventilation
and whose primary physician considered them ready to undergo a trial of weaning were
recruited on a non-consecutive basis (Table 1). The patients had received 18.8 ± 4.2 days
of ventilator support. The decision to extubate patient or reinstitute mechanical ventilation
was made solely by the primary physician. The physician was blinded to the study design
and the measurements obtained, although arterial blood gas values were available. The
study was approved by the local Human Studies Subcommittee and informed consent was
obtained from each patient. Some aspects of data on esophageal pressure measurements
have been included in one other report that addresses a different research question (15).
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Flow and pressure measurements. Flow was measured with a heated Fleisch
pneumotachograph (Hans Rudolph, Kansas City, MO) placed between the endotracheal
tube and the Y-piece of the ventilator circuit. Airway pressure (Paw) was measured
proximal to the endotracheal tube. Esophageal pressure (Pes) and gastric pressure (Pga)
were separately measured with two thin-walled, balloon-tipped catheters (Erich Jaeger,
Wurzberg, Germany) coupled to pressure transducers (MP-45, Validyne, Northridge,CA)
(19; 35). Proper positioning of the esophageal-balloon catheter was ensured with the
occlusion technique (2). Transdiaphragmatic pressure (Pdi) was obtained by subtracting
Pes from Pga.
Electroymyogram measurements of the sternomastoid muscle.
electromyogram (EMG) of the sternomastoid muscle was obtained using bipolar fine-wire
electrodes introduced in the muscle’s belly midway between the mastoid process and the
medial end of the clavicle (7; 9; 20). EMG signals were filtered below 10 Hz and above
1000 Hz. EMG, flow, and pressures (Paw, Pes, Pga) were acquired at a sampling rate of
2,000 Hz, and recorded on a personal computer using digital acquisition systems (DATAQ).
After placement of all transducers, an arterial blood gas measurement was
obtained while the patient was still receiving mechanical ventilation. The patient was
then disconnected from the ventilator, and maximum inspiratory airway pressure (PImax)
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was measured during a 20-second occlusion (17; 30). The measurement was made using a
one-way valve that allowed exhalation but prevented inhalation, thus ensuring that PImax
was measured at low lung volume (17; 30). The patient was then placed back on the
ventilator for 2-3 minutes while the T-tube system for the weaning trial was set up. Next,
the patient was disconnected from the ventilator and began to breathe spontaneously
through the T-piece circuit with oxygen delivered at the same concentration as during
mechanical ventilation. Arterial blood samples were collected at two minutes after
starting the trial, and at its end. The criteria for weaning failure used by the primary
physician were tachypnea, hypoxemia (O2 saturation < 90% with a fraction of inspired
oxygen ≥ 0.4), tachycardia, arrhythmias, hypotension, diaphoresis, or evidence of increasing
effort (16; 19). Patients who met these criteria were returned to the ventilator and designated
as weaning failure patients. Patients who met none of these criteria at the end of the trial
were extubated. Patients who were extubated and sustained spontaneous breathing for more
than 48 hours were designated as weaning-success patients. Throughout data acquisition,
patients were studied while lying at 30o with their neck in the neutral position.
Intrinsic positive end-expiratory pressure (PEEPi): During spontaneous breathing
trial, total PEEPi was measured as the negative deflection in Pes between the point of its
rapid decline and the onset of inspiratory flow (33; 34) (Figure 1). Expiratory muscle
contribution to total PEEPi was measured as the rise in Pga between the onset of
expiratory flow and the point of rapid decline in Pes (Figure 1) (26; 35; 52). The rise in
Pga during expiration may result from activation of the abdominal muscles, expiratory
Page 7 of 36
rib-cage muscles, or a combination of the two; the relative contribution of each muscle
group to the expiratory rise of Pga cannot be determined.
Respiratory pressures: Maximal inspiratory pressures were calculated as
previously described (16; 19). Changes in Pes (∆Pes) during spontaneous breathing were
used as an estimate of overall respiratory muscle pressure output (16; 21). ∆Pes was
measured from the beginning of effort to its nadir. The inspiratory change in Pga (∆Pga)
was measured from the beginning of effort to its maximum excursion (19). When present,
expiratory muscle contraction can contribute to ∆Pes and ∆Pga (34). To correct for
expiratory muscle contraction, the rise in Pga during the preceding expiration was
subtracted from ∆Pes to yield corrected ∆Pes (c∆Pes), and from ∆Pga to yield corrected
∆Pga (c∆Pga). We reasoned that c∆Pes represents an estimate of inspiratory muscle effort
and that c∆Pga represents an estimate of diaphragmatic activity during inspiration, free
from the contribution of expiratory muscle contraction. The relative contributions of the
diaphragm and inspiratory rib-cage muscles to inspiratory effort were then estimated as
the ratio of corrected ∆Pga to corrected ∆Pes (c∆Pga/c∆Pes). In healthy volunteers, the
∆Pga/∆Pes ratio during resting breathing is normally more negative than -1 (n = 18;
normal = –1.95 (28). A ∆Pga/∆Pes ratio of +1 or greater indicates a totally ineffective
diaphragm (diaphragmatic paralysis). A ∆Pga-to-∆Pes ratio between -1 and +1 is highly
suggestive of impaired diaphragmatic activity (diaphragmatic weakness) (47); it could also
result from greater activity of the rib-cage muscles (relative to the diaphragm), relaxation
Page 8 of 36
of the abdominal muscles (5), or any combination of the above (54). Change in Pes over
time (dP/dt) (27) was taken as an estimate of respiratory drive.
Electromyography analysis: For each patient, the number of breaths with any
sternomastoid EMG activity during inspiration was expressed as a percentage of the total
number of breaths during the entire spontaneous breathing trial (45; 46). To assess extent
of sternomastoid phasic activity, the raw EMG was rectified and moving averaging (time
constant of 0.15 s) was performed. The change in the moving-time average of the
sternomastoid EMG signal over the course of a single respiratory cycle was taken as the
change in the magnitude of phasic muscle activity.
For the spontaneous breathing trial, EMG and pressure data were analyzed at six
points in time (sextiles): the first and last minute of the trial, and four one-minute periods
taken at equal time intervals between the first and last minute. Mean EMG and pressure
data were calculated based on eight representative breaths within each sextile. The mean
activity of sternomastoid muscle for each sextile was then referenced to the sextile in
which the patient had achieved the maximum sternomastoid phasic activity during the
entire weaning trial. To ensure that our data were normally distributed, we used the
Kolmogorov-Smirnov test of normality. Within a group, data at the six time points were
compared by one-way ANOVA with repeated measures and by Neuman-Keuls test of
multiple comparisons between individual means when appropriate. To define the
determinants of sternomastoid activity, the relationship between the EMG of the
Page 9 of 36
sternomastoids with various physiologic indices was examined using single and multiple
linear regression analysis. The breath-to-breath variability in the activity the various
muscle groups was quantified using coefficient of variation, calculated as standard
deviation divided by mean. Data between the groups were compared by two-way
ANOVA with repeated measures across time. Results are expressed as mean ± standard
Eleven patients met the criteria for weaning failure after 21 ± 6 minutes of
spontaneous breathing, and mechanical ventilation was reinstituted. Eight patients
tolerated the trial without distress and were extubated after 31 ± 3 minutes. PImax (before
the trial) was lower in the failure patients than in the success patients: 32.7 ± 3.5 (36% of
predicted) versus 51.6 ± 9.2 cm H2O (47% of predicted), p = 0.05.
Respiratory muscle effort
Estimates of electrical activation of sternomastoids were available for all 19
patients. Because the gastric balloon malfunctioned in one patient, estimates of
diaphragmatic pressure output were available in 18 patients (10 of whom failed).
Mechanical estimates: At the start of the trial, the generation of respiratory muscle
pressure, inferred from ∆Pes, was equivalent in the failure and success groups, 10.7 ± 1.5
and 11.4 ± 1.7 H2O, respectively (p = 0.4). Likewise, when ∆Pes was corrected for
expiratory muscle contraction (c∆Pes), values were equivalent in the failure and success
Page 10 of 36
groups, 8.9 ± 1.3 and 11.3 ± 1.7 H2O, respectively (p = 0.27). At the end of the trial, ∆Pes
(not corrected for expiratory muscle contraction) increased to 23.0 ± 1.5 cm H2O in the
failure group (p < 0.0001) and to 14.6 ± 1.7 cm H2O in the success group (p = 0.005). At
the end of the trial, c∆Pes (corrected for expiratory muscle contraction) was 18.7 ± 1.5 cm
H2O in the failure group. The values of c∆Pes and ∆Pes in the success group at the end
of the trial were nearly identical. Over the course of the trial, ∆Pes (not corrected for
expiratory muscle contraction) was higher in the failure group than in the success group
(p = 0.0004); a similar pattern was observed when ∆Pes was corrected for expiratory
muscle contraction (p = 0.0015).
At trial onset, the c∆Pga/c∆Pes ratio was greater in the failure group than in the
success group: 0.11 ± 0.08 versus -0.15 ± 0.09 (p=0.05) (Figure 2, upper panel). Over
the course of the trial, c∆Pga/c∆Pes remained greater in the failure patients (p= 0.0014).
At the end of the trial, the ratio had increased to 0.39 ± 0.12 in the failure group (p=0.04)
and was unchanged in the success group, -0.14 ± 0.09.
Expiratory muscle pressure output (i.e., increase in Pga during exhalation),
expressed as a percentage of the subsequent ∆Pes (i.e., global respiratory muscle pressure
output), increased from 9.1 ± 3.7 % at the onset to 22.6 ± 7.3 % at the end of the trial in
the failure group; in some patients, expiratory muscle effort constituted as much as 40%
of the subsequent global respiratory muscle pressure output. In the success group,
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expiratory rise in Pga remained unchanged at 0.9 ± 0.9 % of ∆Pes over the course of the
Electrical estimates: Sternomastoid activity was evident in 82.5 ± 9.1% of all the breaths
in the failure group and in 18.6 ± 10.1% of all breaths in the success group (p=0.002).
Plot of sternomastoid EMG activity during a weaning trial in a representative failure patient
are shown in Figure 3. Sternomastoid activity became evident within the first minute of
the trial in 8 of the 11 failure patients and 1 of the 8 success patients. By the end of the
trial, sternomastoid activity was noted in all failure patients. In contrast to the failure
patients, only 3 of the 8 success patients exhibited sternomastoid activity during the trial,
and even this activity was modest as compared with that recorded in the failure patients
(Figure 2, middle panel).
Sternomastoid activity (expressed as the percentage of highest activity that an
individual patient manifested during the course of the trial) increased by 53.0 ± 9.3% in
the failure group over the course of the trial (p=0.0005), whereas it did not change in the
success group (p=0.91) (Figure 2, middle panel). Sternomastoid activity correlated with
c∆Pga/c∆Pes ratio (r=0.54 [0.1-0.8, 95% CI], p=0.02) and PEEPi (r=0.66 [0.28-0.86],
p=0.002), and it tended to correlate with PImax (r= -0.43 [-0.74-0.03], p=0.07). On
multiple linear regression analysis, in which sternomastoid EMG activity recorded
throughout the trial was the dependent variable and PImax, c∆Pga/c∆Pes ratio and PEEPi
recorded throughout the trial were the independent variables, 70% of the variance in
sternomastoid activity resulted from these 3 variables: adjusted R2 = 0.70.
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At the onset of the trial, total PEEPi (not corrected for expiratory muscle
contraction) was similar in the failure group, 2.5 ± 0.7 cm H2O, and success group, 2.3 ±
0.6 cm H2O (p = 0.8). At the end of the trial, total PEEPi increased to 6.9 ± 1.2 cm H2O
in the failure group (p = 0.0001), but it did not change in the success group, 2.5 ± 0.7 cm
H2O (p = 0.6). Over the course of the trial, total PEEPi was higher in the failure group
than in the success group (p=0.04). At the onset of the trial, PEEPi corrected for
expiratory muscle contraction, was not different between the failure and success groups:
1.6 ± 0.5 versus 2.2 ± 0.6 cm H2O (p = 0.36). At the end of the trial, corrected PEEPi was
2.6 ± 0.8 cm H2O in the failure patients (p = 0.3) and 2.5 ± 0.7 cm H2O in the success
patients (p=0.75). Over the course of the trial, corrected PEEPi was not different between
the failure patients and the success patients (Figure 4).
Expiratory muscle activity
Expiratory muscle activity, as indicated by an expiratory rise in Pga, was present
in all but one of the failure patients – the exception being a patient with paraplegia
(excluding this patient from analysis does not change the findings of the study).
Expiratory muscle activity was absent in all but three of the success patients. At the onset
of the trial, the expiratory rise in Pga was equivalent in the failure and success groups, 0.9
± 0.5 and 0.1 ± 0.1 cm H2O, respectively (p = 0.3) (Figure 2, lower panel). At the end
of the trial, the expiratory rise in Pga increased to 4.4 ± 1.1 cm H2O in the failure group
(p = 0.0005), whereas it did not change, 0.1 ± 0.1 cm H2O, in the success group (p = 0.4)
(Figure 2, lower panel). Compared with the success group, the failure group exhibited
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larger increases in expiratory rise in Pga (p=0.004). In the failure group, expiratory
muscle activity accounted for 53 + 4 % of total PEEPi throughout the weaning trial.
Throughout the trial, expiratory rise in Pga correlated with drive, estimated as change in
Pes over time (dp/dt): r=0.57 [0.12-0.82], p= 0.02.
Variability in the pattern of muscle activation in weaning failure
During the first sextile, the coefficient of variation for sternomastoid activity was
higher than that for c∆Pga/c∆Pes ratio (41 + 10 vs 6 + 3 %, p< 0.006); the coefficient of
variation for sternomastoid activity was similar to that of the expiratory rise in Pga (57 +
23%, p = 0.54). Likewise, at the last sextile, the coefficient of variation for sternomastoid
activity remained higher than that for c∆Pga/c∆Pes ratio (65 + 20 vs 10 + 5 %, p< 0.01)
but was similar to that of the expiratory rise in Pga (36 + 12%, p = 0.23).
Arterial blood gas measurements
During mechanical ventilation, PaO2, PaCO2, and pH were not different between
the groups (Table 2). By the end of the trial, the failure group developed an increase in
PaCO2 (p = 0.001) and a decrease in pH (p = 0.001). None of the success patients
developed hypoxemia (PaO2 < 60 mm Hg with a FIO2 of 0.40) or respiratory acidosis (pH
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This is the first study of systematic measurements of respiratory muscle
recruitment in patients being weaned from mechanical ventilation. In patients failing a
weaning trial, the sequence of respiratory muscle recruitment began with greater activity
of inspiratory rib-cage muscles than was the case in the success patients; recruitment of
sternomastoids and rib-cage muscles was near maximum early in the weaning trial in the
failure patients, and was followed by progressive activity of the expiratory muscles.
Sternomastoid muscle and rib cage inspiratory muscle recruitment
Within the first minute of the spontaneous breathing trial, three-quarters of our
failure patients recruited their sternomastoids; in contrast, only one of eight success
patients recruited their sternomastoids within the same time frame. Similarly, within the
first minute of the spontaneous breathing trial, the c∆Pga/c∆Pes ratio, a surrogate of rib-
cage inspiratory muscle recruitment, was greater in the failure patients than in the success
The preferential (more prevalent) recruitment of the sternomastoids and greater
inspiratory rib-cage muscle contribution to tidal breathing in the failure patients at the start
of the trial is most likely secondary to decreased capacity of the inspiratory muscles to
generate pressure. This notion is supported by two observations. First, overall inspiratory
muscle strength (PImax) before the trial was less in the failure group than in the success
group. Second, from the start of the trial, c∆Pga/c∆Pes ratio was less negative (positive) in
the failure group than in the success group: 0.11 and -0.15 (p = 0.05; Figure 2). While a
Page 15 of 36
c∆Pga/c∆Pes ratio of less than one indicates that the diaphragm was active and capable of
generating pressure (14; 47) (in both patient groups), the higher c∆Pga/c∆Pes ratio in the
failure group suggests greater diaphragmatic impairment than in the success group
(resulting in recruitment of extra-diaphragmatic inspiratory muscles). Although the increase
in c∆Pga/c∆Pes ratio could be secondary to relaxation of the abdominal muscles (5), this is
unlikely. When computing the c∆Pga/c∆Pes ratio, the expiratory rise in Pga (an estimation
of the magnitude of expiratory muscle recruitment) was subtracted from tidal excursions
in Pga and Pes.
Decreased capacity of the inspiratory muscles to generate pressure is also one of the
likely mechanisms for greater recruitment of the sternomastoids and rib-cage inspiratory
muscles during the course of the trial in the failure patients. First, the degree of
sternomastoid activity throughout the trial tended to correlate negatively with PImax
recorded before the trial (r = -0.43, p=0.07). Second, development of dynamic
hyperinflation during a trial will further aggravate respiratory muscle weakness (10; 24; 36).
Of the 10 failure patients, 7 developed an increase in corrected PEEPi between the start and
end of the trial: 1.6 ± 0.5 to 2.6 ± 0.8 cm H2O (p=0.01). Recruitment of the sternomastoids
as a compensatory mechanism for a decrease in the capacity of the diaphragm and rib-cage
muscles to generate pressure has also been reported in patients with high tetraplegia. (7).
Sternomastoid and inspiratory rib-cage muscle recruitment can also occur in
response to an increase in mechanical load (50; 51). An increase in load (assessed by c∆Pes)
at the beginning of the trial, however, is an unlikely cause of sternomastoid and inspiratory
Page 16 of 36
rib-cage muscle recruitment in the failure patients because c∆Pes at the beginning of the
trial was similar in the two groups of patients. In contrast, increased load (combined with
decreased capacity of the inspiratory muscles and diaphragm to generate pressure) was a
likely mechanism for sternomastoid and rib-cage inspiratory muscle recruitment observed
over the course of the trial. This notion is supported by the progressive increase in c∆Pes,
PEEPi and in c∆Pga/c∆Pes ratio observed between the start and end of the trial in the
failure patients. Moreover, multiple regression analysis revealed that 70% of the variance
in EMG activity resulted from PImax, c∆Pga/c∆Pes ratio, and PEEPi.
That heightened sternomastoid and rib-cage muscle activity in the failure patients
represents a compensatory response to the high mechanical load and weak diaphragm is
supported by observations in healthy volunteers (50) and in ambulatory patients with
COPD (51). When healthy volunteers sustain fatiguing inspiratory loads (tidal excursions
in Pdi greater than 50% of maximum), they demonstrate sternomastoid recruitment and
proportionately greater use of rib-cage muscles than of the diaphragm (50). Similarly, in
patients with COPD during exercise to exhaustion, increased respiratory loads are met
with a proportionately greater use of rib-cage muscles than of the diaphragm (51). Rib-
cage pressure contribution predominates during the period of inspiratory flow, not only
for overcoming the elastic load of the respiratory system but also in compensating for the
gradual loss of diaphragmatic contribution to inspiratory flow (51).
Page 17 of 36
Expiratory muscle recruitment
Over the course of the trial, most failure patients activated their expiratory
muscles – indicated by a rise in Pga during exhalation (26; 35). In contrast, expiratory
muscle recruitment was negligible-to-absent in success patients.
Increased activation of the expiratory muscles represents an automatic component
of the response of the respiratory system to very high levels of ventilatory stimulation (12;
33; 55; 56). Consistent with this viewpoint is the observed correlation between expiratory
muscle activation and respiratory drive (r=0.57, p= 0.02)
It has been reasoned that the goal of expiratory muscle recruitment is to assist the
inspiratory muscles by decreasing end-expiratory lung volume (22). Most of our patients
had COPD and airflow limitation. Therefore, it is unlikely that expiratory-muscle
recruitment in the failure patients lowered end-expiratory lung volume. If anything, end-
expiratory lung volume appeared to have increased despite the presence of expiratory
muscle contraction: PEEPi (after correcting for expiratory muscle recruitment) increased
between the start and end of the trial in 7 of the 10 patients. Lastly, expiratory muscle
recruitment induces additional energy expenditure during respiration (54). This
consideration raises the possibility that expiratory muscle recruitment itself could have
contributed to weaning failure.
Page 18 of 36
Hierarchy of muscle recruitment during weaning failure
The extent of sternomastoid recruitment and inspiratory rib-cage muscle activity
in failure patients increased over the course of the trial: sternomastoid activity was 25, 76,
71, 88, 85, and 100% of the normalized value (expressed as percentage of highest activity
that an individual patient manifested during the course of the trial) (Figure 2, middle
panel), and c∆Pga/c∆Pes ratio was 27, 79, 47, 80, 85 and 100% of the value obtained at
the final sextile (Figure 2, upper panel). As such, more than three-quarters of the
increase in sternomastoid activity and inspiratory rib-cage muscle activity were reached
by the second sextile (~4 minutes into the trial). The immediate increase in sternomastoid
activity with little change thereafter casts doubt on the notion that sternomastoid activity
is a marker of impending diaphragmatic fatigue (3; 37). Instead, activation probably
results from a combination of decreased capacity of the respiratory muscles to generate
pressure and (as we have previously shown (16)) an increase in respiratory load that
occurs early on in the weaning trial.
While the sternomastoid and rib-cage muscles had similar timings of activation,
indirect evidence suggests that their patterns of activation differed. At a given level of
∆Pes, the coefficient of variation of sternomastoid EMG activity was higher than that for
the c∆Pga/c∆Pes ratio. The greater variability in activation of sternomastoids than in that
of the rib-cage muscles raises the possibility that behavioral factors may have a greater
influence on activation of the sternomastoids than of the rib-cage muscles in weaning-
failure patients (4).
Page 19 of 36
Unlike the rapid increases in sternomastoid and inspiratory rib-cage muscle
activities, recruitment of the expiratory muscles was slower throughout the trial (Figure
2, lower panel). Moreover, half the increase in expiratory muscle activity in the failure
patients did not occur until the fourth sextile (~13 minutes into the trial): the expiratory
rise in Pga was 22, 44, 47, 59, 69 and 100% of the final value for each successive sextile
between the start and end of the trial. Of note, the largest increase in expiratory rise in
Pga occurred between the fifth and sixth sextile (17-20 minutes into the trial). The
relatively late activation of the expiratory muscles suggests a hierarchy of muscle
recruitment (specific muscle groups may be recruited in a particular sequence). The
existence of such a hierarchy is supported by the known delayed activation of the
expiratory muscles in healthy volunteers (23; 53) and in ambulatory patients with COPD
In summary, the respiratory muscles of patients who fail a weaning trial present a
sequential pattern of recruitment. The sequence begins with activity of the diaphragm
and greater-than-normal activity of the inspiratory rib-cage muscles; recruitment of
sternomastoids and rib-cage muscles is near maximum within four minutes of trial
commencement; and the expiratory muscles are recruited at the slowest pace of all. In
conclusion, not only is activity of the inspiratory rib-cage muscles increased during a
failed weaning trial, but the respiratory centers also recruit the sternomastoid and
expiratory muscles as a mechanism for offsetting the effects of an increased load on a
Page 20 of 36
Figure 1 Representative tracings from the first and last minute of a spontaneous
breathing trial in a weaning failure patient. Flow, esophageal pressure
(Pes), and gastric (Pga) pressure are shown. Total intrinsic positive end-
expiratory pressure (PEEPi) was estimated as the drop in Pes from the
onset of inspiratory effort (second vertical line) to onset of inspiratory
flow (third vertical line). Estimation of expiratory muscle contribution to
changes in Pes and PEEPi were obtained by measuring rise in Pga from
onset of expiratory flow (first vertical line) to onset of inspiratory effort
(second vertical line). Note increases in changes in Pes swing, PEEPi and
expiratory rise in Pga between start and end of trial.
Figure 2Ratio of change in gastric pressure corrected for expiratory muscle
contraction (c∆Pga) over change in esophageal pressure corrected for
expiratory muscle contraction (c∆Pes) (upper panel), amplitude of phasic
activity in sternomastoid electromyogram (EMGscm) (middle panel), and
expiratory rise in gastric pressure (Pga) (lower panel) during the course of
a weaning trial in failure (closed symbols) and success patients (open
symbols). Between the onset and the end of the trial, increases in
c∆Pga/c∆Pes ratio (p = 0.04), EMGscm (p = 0.0005), and expiratory rise
in Pga (p = 0.0005) occurred in failure patients but not in the success
patients. Over the course of the trial, failure patients had higher values of
Page 21 of 36
c∆Pga/c∆Pes ratio (p = 0.0014), EMGscm (p = 0.0003), and expiratory
rise in Pga (p = 0.004) than success patients. Bars represent + 1 SE.
Figure 3 Representative tracings of flow, esophageal pressure (Pes) and
sternomastoid electromyogram (EMGscm) in a weaning-failure patient.
Recordings were obtained during the first minute of the weaning trial,
40% of trial duration, and last minute of the trial. Phasic inspiratory
activity of the sternomastoid muscle was evident within the first minute
of the trial, and it increased progressively over the course of the trial.
Note that phasic activity of the sternomastoids persists into expiration.
Figure 4 Total intrinsic positive end-expiratory pressure (PEEPi, closed symbols)
and intrinsic positive end-expiratory pressure corrected for expiratory
muscle contraction (corrected PEEPi, open symbols) during the course of a
weaning trial in failure (upper panel) and success (lower panel) patients.
Between the onset and the end of the trial, total PEEPi increased in the
failure group (p = 0.0001), whereas corrected PEEPi remained the same.
In the success patients, total PEEPi and corrected PEEPi remained
unchanged over the course of the trial.
Page 22 of 36
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Table 1: Characteristics of patients
Age ET Tube
Days of ventilatorn support
1COPD 70 8 5
2COPD 80 8 25
3COPD 60 8 27
4Pneumonia 64 8 22
5COPD 79 8 14
6COPD 60 8 23
7 Paraplegia 82 8 74
8COPD 50 7.5* 11
9CHF, COPD 80 8 8
10 COPD 54 8 8
11 COPD 56 8 12
1COPD 69 8 19
2COPD 64 8 1
3Pneumonia 44 8 17
4 Pneumonia 47 7.5 2
5Sepsis, COPD 55 8 11
6 CHF, COPD 64 8 58
7 CHF 56 8 13
8 COPD 44 8 7
Definition of abbreviations: ET tube = endotracheal tube; ID mm = internal diameter in
millimeters; COPD = chronic obstructive pulmonary disease; CHF = congestive heart failure.
Page 31 of 36
Table 2: Arterial blood gas measurements *
pH 7.44 + 0.01 7.4 + 0.02 7.37 + 0.02 p=0.001
PaCO2(mm Hg) 36.1 + 3.0 39.3 + 6.3 45.01 + 3.6p=0.001
PaO2(mm Hg) 110.7 + 11.1 134 + 15.8 122.1 + 19.3 NS
38.9 + 0.7 40 40 NS
pH 7.44 + 0.01
7.40 + 0.02 7.41 + 0.02 NS
PaCO2(mm Hg) 36.6 + 2.9 40.1 + 2.5 39.5 + 2.5 p=0.01
PaO2(mm Hg) 105.6 + 14.7 78.8 + 9.8 101.3 + 16.7NS
39.2 + 0.8 40 40 NS
Definition of abbreviations: FIO2= fractional inspired oxygen concentration.
* Values are mean + SE
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(cm H2O)(cm H2O)
(cm H2O)(cm H2O)
Onset of exp flow
Onset of insp effortOnset of insp effort
Onset of insp flowOnset of insp flow
Onset of exp flow
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in Pga (cm H2O)
Spontaneous Breathing Trial, Sextiles
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40% of Trial
Pes, cm H2O
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PEEPi, cm H2O
Spontaneous Breathing Trial, Sextiles
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