Respiratory muscle fatigue and breathing pattern

MJ Mador

Chest 1991;100;1430-1435
DOI 10.1378/chest.100.5.1430
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Respiratory Muscle Fatigue and Breathing Pattern*
M. Jeffery Mador, M.D., F.C.C.P

(Chest 1991; 109:1430-35) transmission of neural impulses through nerves or

across neuromuscular junctions. Contractile fatigue is
PS = transdiaphragmatic pressure; Pmax maximal transdia- a reversible impairment in the contractile response to
phragmatic pressure; P. mouth pressure; L, time to last
failure; T/T,., inspiratory time/total breath duration; neural impulses in an overloaded muscle. Transmission
TTateflSion4itfle index; TTteasion-time ribcage fatigue and contractile fatigue can be grouped together
as peripheral causes for fatigue.
T he respiratory muscles, like the heart, must work
DETERMINANTS OF RESPIRATORY MUSCLE FATIGUE
continuously with little opportunity to rest. Pal-
monary disease increases the load on the respiratory The majority of muscular work required for breath-
pump while at the same time decreasing the pressure- ing is performed during inspiration even in patients
generating capacity of the respiratory muscles. If the with chronic obstructive pulmonary disease.6 There-
respiratory muscles are subjected to sufficiently high fore, the inspiratory muscles, including the diaphragm,
loads for a prolonged period of time, they will even- are the muscles primarily at risk ofdeveloping fatigue.
tually fatigue. It has been postulated that respiratory In 1977, Roussos and Macklem7 demonstrated that the
muscle fatigue causes the respiratory pump to fail diaphragm could be fatigued in normal man when
resulting in hypercapnic ventilatory failure.’ This subjected to a sufficiently high load. In these experi-
postulate has led to a tremendous interest in respira- ments, an inspiratory resistive load was employed to
tory muscle fatigue. In this article, we will focus on require the diaphragm to generate a given target
the determinants of respiratory muscle fatigue, the pressure with each breath until task failure (defined
effects of respiratory muscle fatigue, the effects of as the inability to generate the target pressure). It was
respiratory muscle fatigue on breathing pattern and found that a target transdiaphragmatic pressure (Pa)
the clinical signfficance of these changes in breathing less than 40 percent ofthe maximal transdiaphragmatic
pattern. A complete review of respiratory muscle pressure (Pthmax) could be maintained indefinitely
fatigue is beyond the scope of this article and the while a target P,,, greater than 40 percent of Pmax
reader is referred e1sewhere)1 led to task failure within a finite period of time (less
than 45 mm). The greater the target pressure, the
DEFINITION AND TYPES
shorter the time to task failure. Subsequently, these
OF RESPIRATORY MUSCLE
authors have shown that fatigue ofboth the diaphragm
FATIGUE
and ribcage muscles can be achieved when subjects
Muscle fatigue can be defined as a condition in generate a high enough mouth pressure (Pm) With each
which there is a reduction in the force generating breath during inspiratory resistive loading.8 A target
capacity of the muscle resulting from muscle activity m less than 60 percent ofthe maximal mouth pressure
under load which is reversible by rest.5 Muscle weak- (Pmm#{248}i)(measured while performing a maximal in-
ness is a condition in which the capacity of the rested spiratory effort against an occluded airway at func-
muscle to generate force is impaired. Three general tional residual capacity) could be maintained indefi-
types offatigue have been described: central fatigue, nitely while a target greater than 60 percent of
transmission fatigue, and contractile fatigue. Central Pmmi3l led to task failure within a finite period of
fatigue is an exertion-induced reversible decrease in time. These experiments clearly show that the inten-
central neural respiratory drive. Transmission fatigue sity ofinspiratory muscle contraction and the strength
is an exertion-induced reversible impairment in the ofthe inspiratory muscles are important determinants
#{149}Fmmthe Division of Pulmonary Medicine, State University of
of the fatiguing process. Thus, increases in inspiratory
New York at Buffalo, and the Veterans Administration Medical load (by increasing the required Pm) and decreases in
Center, Buffalo. inspiratory muscle strength (by decreasing Pmmax) will
Supported by grants from the American Lung Association of New
York, American Heart Association ofNew York and by VA Medical predispose to the development of inspiratory muscle
Research Funds. fatigue. It is of interest to note that the target mouth
Reprint requests: Dt Mador, 3495 Bailey Avenue, VA Med4cal
Center, Buffalo 14215 pressure required to induce task failure is larger than

1430 Respiratory Muscle Fatigue and Breathing Pattern (M. Jeffery Mador)

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Copyright © 1991 by American College of Chest Physicians
when a diaphragmatic target pressure is employed (60 C
vs 40 percent). The reasons for this difference are not 600
entirely clear. In these experiments, however, Pmax
E
was measured during a Mueller-expulsive maneuver E 400
(a maximal inspiration against an occluded airway with
0.
simultaneous contraction of the abdominal muscles). to
4,
The highest P(,max values are achieved during a 200
(sJ
Mueller-expulsive maneuver,9 but Pmax measured 0
.>
during such maneuvers may overestimate the inspira-
tory pressure generating capacity of the diaphragm 0
4 6 8 10
During breathing, the diaphragm contracts mainly
during inspiration and relaxes during expiration. In- Tlim (m1
creases in inspiratory time will increase the duration Ficuaz 1. Relationship between rate of 0, consumption due to
of diaphragmatic contraction, while decreases in ex- breathing task (Vo, resp) and time to task failure (F,,,.) in a single
subject. There was no systematic difference in the relationship
piratory time will shorten the period in which the between Vo, resp and L at different flow rates (low o, medium ,

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

CHEST I 100 I 5 I NOVEMBER, 1991 1431

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Copyright © 1991 by American College of Chest Physicians
 800 volume, respiratory rate or inspiratory flow rate would
affect Vo2resp has not been determined.

BREATHING PATTERN IN RESP1RATORY MUSCLE

FATIGUE
U
a)
U) 600 In a highly influential paper, Cohen and associatesss
measured the diaphragmatic EMG, respiratory rate
a) and rihcage-abdominal motion in 12 ventilator-de-
E pendent patients being weaned from mechanical yen-
tilation. Seven patients displayed power spectral shifts
400 in the diaphragmatic EMG consistent with diaphrag-
a)
U matic fatigue. Coincident with the changes in dia-
C phragmatic EMG, the patients developed tachypnea
0
and abnormalities in ribcage-abdominal motion; ab-

#{149}0 200 dominal paradox, defined as a paradoxic inward ab-

C dominal motion during inspiration, and respiratory
Ui alternans, defined as phasic alterations between rib-
cage and abdominal breathing. The abnormalities in
thoracoabdominal motion were not observed in the
0 five patients who did not develop EMG evidence of
15 30 45 diaphragmatic fatigue. The authors suggested that
abdominal paradox and respiratory alternans may be
Breathing Frequency
reliable clinical signs of inspiratory muscle fatigue.
(b/mm) Implicit in this reasoning is the assumption that the
Ficuax 2. Diaphragmatic endurance times of five subjects at three abnormal thoracoabdominal motion was caused by
different breathing frequencies. Despite a constant TT,,, tidal
volume and work/breath, diaphragmatic endurance decreased as
inspiratory muscle fatigue. To determine whether this
breathing frequency and, thus, work rate increased. assumption is correct, Tobin and associates measured
ribcage-abdominal motion with a respiratory inductive
achieved by mechanical means, the reduction in plethysmograph in healthy subjects during inspiratory
inspiratory muscle endurance can be explained solely resistive loading. Increasing amounts of ribcage-ab-
by the decrease in inspiratory muscle strength (due to dominal asynchrony and paradox were observed with
muscle shortening).2’ When the increase in lung vol- increases in respiratory load during nonfatiguing resis-
ume is due to persistent inspiratory muscle activity tive runs. When subjects breathed through an inspir-
during expiration (as may occur in patients with atory resistance to fatigue (defined as the inability to
asthmatm), inspiratory muscle endurance is impaired generate a target pressure) increases in abdominal
to an even greater extent’ presumably due to the paradox were observed during the first minute of
additional negative work performed by the inspiratory loaded breathing and did not progress during the
muscles during expiration. Recently, Collett and remainder ofthe loaded breathing run (Fig 3). Clearly,
Engel” have measured Vo2resp in healthy subjects if fatigue was responsible for the abdominal paradox,
breathing against inspiratory resistive loads at FRC the degree of abdominal paradox should have pro-
and at a higher lung volume (45 and 66 percent of the gressed during the loaded breathing run as fatigue
vital capacity, respectively). Despite close matching of developed. The absence of such progression, the
ventilation, inspiratory flow rate, pressure-time prod- immediate appearance of abdominal paradox at the
uct, and work rate, Vo2resp was increased at the start of the loaded breathing run, and its immediate
higher lung volume-an increase of about 1 percent disappearance when the load was removed, suggest
in 02 cost per unit work for each percentage increase that abdominal paradox was due to the increase in
in vital capacity (efficiency was reduced). In this study, respiratory load rather than to muscle fatigue. Simi-
increases in tidal volume (from 600 to 1,600 ml) at a larly, in a study of patients weaning from mechanical
constant end-expiratory lung volume had no effect on ventilation, an increase in the degree of abdominal
Vo2resp suggesting that modest increases in the de- paradox was observed immediately following discon-
gree of muscle shortening during inspiration do not tinuation of mechanical ventilation without subse-
affect Vo2resp. Similarly, a threefold increase in in- quent progression during the remainder of the wean-
spiratory flow rate and respiratory rate had no effect ing trial, again suggesting that the increase in
on Vo2resp when the pressure-time product and work abdominal paradox was due to increases in respiratory
rate were held constant during inspiratory resistive load rather than to fatigue. In these studies, respi-
loading.as Whether more extreme changes in tidal ratory alternans was not observed in either the normal

1432 Respiratory Muscle Fatigue and Breathing Pattern (M. Jeffery Mador)

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Copyright © 1991 by American College of Chest Physicians
 following induction of fatigue. Furthermore, at any
50
given level of CO2. minute ventilation, peak transdia-
phragmatic pressure and peak electrical activity of
both the intercostal muscles and the diaphragm were
reduced following induction of fatigue. Thus, in this
study, induction offatigue led to a reduction in motor
outflow to the inspiratory muscles, a form of “central
ci fatigue.” These studies demonstrate that the develop-
E ment of inspiratory muscle fatigue in animals is
associated with a rapid shallow pattern of breathing.
25 The mechanism by which fatigue elicits changes in
breathing pattern has not been delineated. However,
0
activation of thin fiber afferents within the fatigued
0 inspiratory muscles may be important. Diaphragmatic
0 afferents have been shown to be capable of modulating
0
motor outflow to the respiratory muscles.
0
0 Gallagher and colleagues have measured the breath-
ing pattern before and after induction of inspiratory
muscle fatigue in healthy human subjects. Fatigue
was induced by breathing against an inspiratory resis-
0
1st 5th tive load to task failure (inability to generate the target
Baseline LLoad Breathfrjj Recovery pressure). At the same level of ventilation, breathing
(mins)
was faster and shallower following induction of fatigue
Ficun 3. Effect of breathing against a fatiguing resistive load on compared with control. Since minute ventilation was
the amount of inspiratory abdominal paradox at baseline, during
transiently increased following discontinuation of re-
the first mm ofloaded breathing, a mm at the middle of the run, a
mm near the end of the run and during the first and fifth mm of the sistive loading (likely a reflection of neuronal after
recovery period. Values are mean ± SE of six subjects. Abdominal discharge), ventilation was stimulated during the con-
paradox increased during the first mm ofloaded breathing, did not
trol period by rebreathing CO2 to allow comparison of
progress during the loaded breathing run, and returned to baseline
levels immediately following discontinuation ofthe load. (Modffied the breathing pattern at the same minute ventilation.
from Tobin MJ, Perez W, Guenther SM, et al. Does ribcage- However, the breathing pattern may differ depending
abdominal paradox signify respiratory muscle fatigue. J Appl Physiol
on the method employed to stimulate ventilation so
1987; 63:851-60.)
that CO2 hyperpnea may not be an optimal control.
subjects during resistive 1oading or in the patients Nevertheless, the results obtained in this study are
during weaning from mechanical ventilation.as Other quite consistent with the studies in animals and
investigators have also been unable to detect respira- supports the notion that induction of inspiratory
tory alternans in patients weaning from mechanical muscle fatigue results in a rapid shallow pattern of
ventilation#{176} or in subjects breathing against an breathing in conscious humans.
inspiratory load3’ suggesting that respiratory alternans My colleagues and P#{176}have examined the breathing
may be more uncommon than originally believed. pattern before and after induction of inspiratory
In the study by Cohen and colleagues, all subjects muscle fatigue in healthy volunteers under a variety
who developed hypercapnia and EMG signs of dia- of experimental conditions. The breathing pattern
phragmatic fatigue also developed progressive tach- following induction of fatigue was not significantly
ypnea during the weaning trials. The question arises different from control during resting breathing and
as to whether the tachypnea was due to fatigue or to when ventilation was modestly increased by CO2
other factors. Road and co1leagues have examined rebreathing or exercise.’#{176}’37 In contrast, when venti-
the breathing pattern in anesthetized dogs before and lation was stimulated more rigorously by high intensity
after induction of diaphragmatic fatigue by electro- exercise on a bicycle, minute ventilation and respira-
phrenic stimulation. Following induction of diaphrag- tory rate were signfficantly increased following induc-
matic fatigue, minute ventilation and respiratory rates tion of fatigue compared with control (Fig 4) while
were larger while tidal volume was smaller than tidal volume was slightly but not significantly de-
control values. Oliven and colleagues have measured creased37’ (the decrease in tidal volume was less
the breathing pattern during CO2 rebreathing in awake pronounced than the increase in respiratory rate
goats before and after induction of inspiratory muscle similar to the results obtained by Road et al in the
fatigue. Fatigue was induced by prolonged inspiratory anesthetized dog). It is likely that the degree of
resistive loading. At any given level ofventilation, tidal peripheral fatigue elicited in healthy volunteers during
volume was reduced and respiratory rate increased inspiratory loading is less than that achieved in animal

CHEST I 100 I 5 I NOVEMBER, 1991 1433

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Copyright © 1991 by American College of Chest Physicians
 2500 A
o-oControl
I00- B
v-vFatigue
C 80#{149}
E
60

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)

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Copyright © 1991 by American College of Chest Physicians
 SUMMARY 16 McCool FD, Tzelepis GE, Leith DE, Hoppin FG. Oxygen cost
of breathing during fatiguing inspiratory resistive loada J Appl
The major determinants of Vo2 resp and, thus, Physiol 1989; 66:2045-55
diaphragmatic endurance are the tension-time index, 17 Field 5, Sanci 5, Grassino A. Respiratory muscle oxygen
work rate and lung volume. Changes in breathing consumption estimated by the diaphragm pressure-lime index.
pattern that adversely affect any of these factors can J Appl Physiol 1984; 57:44-51
18 Collett PW, Perry C, Engel LA. Pressure-lime product, work
impair diaphragmatic endurance. A above 0.15-
rate and endurance during resistive breathing in humans. J AppI
0. 18 indicates a potentially fatiguing pattern of con- Physiol 1985; 58:1263-72
traction. However, fatigue may occur at a TT, below 19 Dodd DS, Kelly 5, Collett LW, Engel LA. Pressure-time
0. 15 if the work rate is sufficiently high or the P,,max product, work rate and endurance during resistive breathing in

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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 Respiratory muscle fatigue and breathing pattern
MJ Mador
Chest 1991;100;1430-1435
DOI 10.1378/chest.100.5.1430
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