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Respiratory Muscle Fatigue and Breathing Pattern
Respiratory Muscle Fatigue and Breathing Pattern
MJ Mador
Chest 1991;100;1430-1435
DOI 10.1378/chest.100.5.1430
The online version of this article, along with updated information and
services can be found online on the World Wide Web at:
http://chestjournal.org/cgi/content/abstract/100/5/1430
1430 Respiratory Muscle Fatigue and Breathing Pattern (M. Jeffery Mador)
diaphragm can relax between contractions. The duty high 0) or lung volumes (relaxation volume, closed symbols;
cycle (inspiratory time/total breath duration; T,i’F,) relaxation volume + 1 L, open symbols). Similar results were ob-
tamed in the other subjects. (From McCool FD, Tzelepis GD,
is an important determinant of the fatiguing process. Leith DE et al: Oxygen cost ofbreathingduringfatiguing inspiratory
Bellemare and Grassino” have shown that the duty resistive loads. J AppI Physiol 1989; 66:2045-55)
cycle (FI/TT0T) is equally as important as the pressure
generated during diaphragmatic contraction (Pd,! ventilatory requirements, TTd, threshold values ob-
Pd,max) in determining diaphragmatic endurance. tamed during inspiratory resistive loading are no
These authors found that a tension-time index longer applicable.
(FTcj Pd/PthmaxTjF,)could predict diaphragmatic What, then, determines diaphragmatic endurance?
endurance during inspiratory resistive loading. A TTd, McCool and colleagues’6 have recently shown that the
of less than 0. 15 could be maintained indefinitely time to task failure (endurance time) during inspira-
while a TTd, of greater than 0.18 led to task failure tory resistive loading is closely related to the oxygen
within a finite period of time. Thus, the fatigue cost of breathing (Vo2resp). The greater the increase
threshold was 0. 15-0. 18. A similar tension-time index in Vo2resp, the shorter the endurance time. Further-
has recently been devised for the ribcage muscles more, the relationship between Vo2resp and endur-
(FT). The TT,, = PJmmaxT,/T (Pmmax is meas- ance time could be described by a single relationship
ured during a maximal inspiratory effort against an under a wide variety of experimental conditions (Fig
occluded airway at functional residual capacity). Elec- 1) while the relationship between the tension-time
tromyographic (EMG) evidence of fatigue of the index and endurance time differed signfficantly be-
sternocleidomastoid muscles and the parasternal in- tween the various experimental conditions. Field and
tercostal muscles can be demonstrated when the TT(, colleagues’7 have shown that the TT,, and Vo2resp are
exceeds 0.26.12 strongly correlated during inspiratory resistive loading
The TTdI has been measured in patients with when the pattern ofbreathing is relatively constrained.
COPD.’3 A TT,, greater than 0.20 invariably resulted Thus, it is not surprising that under these conditions
in shifts in the power spectrum of the diaphragmatic the TT,, is an accurate predictor of diaphragmatic
EMG consistent with diaphragmatic fatigue. Con- endurance. In contrast, when the breathing pattern is
versely, a TTdI less than 0. 12 never produced change not as constrained, the TT,,, does not uniquely deter-
in the diaphragmatic EMG. Such studies have resulted mine Vo2resp and thus, poorly predicts diaphragmatic
in the TTdI being widely employed as an index of a endurance.
potentially fatiguing pattern of contraction. However, Collett and colleagues’8 have shown that work rate
it is important to appreciate that the factors incorpo- (mechanical work per breath’respiratory rate) is an
rated in the TT are not the sole determinants of important determinant of Vo2resp. At a constant
diaphragmatic or inspiratory muscle fatigue. Other tension-time index, a doubling of the work rate will
factors are also important. lead to a two- to threefold reduction in endurance
Evidence has been provided that diaphragmatic time19m (Fig 2). Another factor that is very important
fatigue can occur during high intensity cycle exercise’4 is hyperinflation. Inspiratory muscle endurance is
or voluntary hyperpnea to volitional exhaustion.’5 significantly reduced during inspiratory resistive load-
However, the TT,, averaged only 0. 10 (range 0.06- ing at lung volumes above FRC.8’2’ With increasing
0. 14) in these studies and the fatigue threshold of lung volume, inspiratory muscles shorten and reduce
0. 15-0. 18 was never exceeded in any of the subjects. their ability to generate pressure (length-tension re-
Clearly, in the presence of a marked increase in 1ationship). When the increase in lung volume is
1432 Respiratory Muscle Fatigue and Breathing Pattern (M. Jeffery Mador)
40
I000 20-
3- C
45 D
*
E
2- .0
I - I 15
B M E B M E
Time Time
FIGURE 4. Oxygen consumption (Vo), minute ventilation (V,), tidal volume (VT), and respiratory frequency
(I) during the first minute (B), the middle minute (M), and the final minute (E) of constant load bicycle
exercise at 90% of maximal capacity after induction of fatigue (V) and during the same time period
(isotime) in the absence offatigue (control exercise, o). Values are means ± SE of 10 subjects. Control curve
represents average of 2 control trials. *Sigiifijt difference from average of 2 control trials (p<O.Ol). At
any given time during exercise, V1 and f after induction of fatigue were greater than control values. (From
Mador MJ, Acevedo FA. Effect of respiratory muscle fatigue on subsequent exercise performance. J Appl
Physiol 1991; 70:2059-65.)
models of fatigue possibly accounting for the greater muscle fatigue. Fatigue was induced by inspiratory
difficulty in eliciting changes in breathing pattern in threshold loading. Subjects breathed through a large
unstressed human subjects. Nevertheless, it is appar- inspiratory resistive load for 5 mm before and imme-
ent that induction of inspiratory muscle fatigue in the diately after induction of fatigue. No differences in
presence of an increased inspiratory load results in breathing pattern were observed following induction
characteristic changes in the breathing pattern in of fatigue compared with controls. These results are
healthy human subjects similar to those obtained in contrary to what might be anticipated. However, with
animal models of fatigue. high external resistances, elastic work is a negligible
My colleagues and V”’ also found that the ventila-
fraction of total work and mean inspiratory pressure
tory response to exercise was increased following
is almost exclusively a function of mean inspiratory
induction of fatigue compared with control. In these
flow rate. Under these circumstances, a slow deep
experiments, induction of fatigue resulted in an in-
pattern of breathing minimizes inspiratory muscle
crease in central respiratory drive. Similarly, Cohen
work and respiratory sensation while rapid shallow
et al#{176}
observed an increase in minute ventilation in
breathing is maladaptive at least from the point of
patients undergoing a weaning trial who displayed
view of minimizing inspiratory muscle work.”#{176}These
electromyographic evidence ofdiaphragmatic fatigue.
findings suggest that the tachypnea usually elicited by
In contrast, motor outflow to the inspiratory muscles
inspiratory muscle fatigue can be suppressed under
was clearly reduced following induction of fatigue in
the awake goat.’ It has been suggested that the neural certain circumstances. It would be of interest to
response to fatigue may vary with the conditions used examine the breathing pattern response to elastic
to induce fatigue and, thus, both excitatory and loading before and after induction of fatigue. With
inhibitory responses may be seen. elastic loading, rapid shallow breathing is the most
In a subject study, Mador and colleagues examined economical pattern of breathing and we hypothesize
the breathing pattern during inspiratory resistive that the tachypneic response to fatigue would be
loading before and after induction of inspiratory enhanced rather than suppressed.
1434 Respiratory Muscle Fatigue and Breathing Pattern (M. Jeffery Mador)
is not measured at the prevailing lung volume. humans. J Appl Physiol 1988; 64:1397-1404
20 Cerny FJ, Lawler MJ, Mador MJ. Breathing frequency affects
Inspiratory muscle fatigue usually elicits an increase
diaphragm fatigue. Physiologist 1988; 31:A37
in minute ventilation and respiratory rate and to a 21 Tzelepis GE, McCool FD, Leith DE, Hoppin FG. Increased
lesser degree a reduction in tidal volume. However, lung volume impairs endurance of inspiratory muscles. J Appl
fatigue may not always be accompanied by changes in Physiol 1988; 64:1796-1802
breathing pattern. Furthermore, fatigue may some- 22 Pengelly LD, Alderson AM, Milic-Emili J. Mechanics of the
diaphragm. J Appl Physiol 1971; 30:797-805
times result in a reduction rather than an increase in
23 Martin J, Pbwell E, Shore 5, EmTICIS J, Engel LA. The role of
motor outflow to the respiratory muscles. Finally, respiratory muscles in the hyperinflation of bronchial asthma.
abdominal paradox initially considered to be charac- Am Rev Respir Dis 1980; 121:441-48
teristic clinical sign of inspiratory muscle fatigue 24 Collett PW, Engel LA. Influence oflung volume on oxygen cost
appears to be due to increases in respiratory load ofresistive breathing. J Appl Physiol 1986; 61:16-24
25 Dodd DS, Collett PW, Engel LA. Influence of inspiratory flow
rather than to muscle fatigue.
rate and frequency on O cost of resistive breathing in humans.
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