British Journal of Anaesthesia 91 (1): 73±80 (2003)
DOI: 10.1093/bja/aeg145
The abdominal muscles in anaesthesia and after surgery
G. B. Drummond
University Department of Anaesthesia, Critical Care, and Pain Medicine, 51 Little France Crescent,
Edinburgh EH16 4SA, UK
E-mail: [email protected]
Br J Anaesth 2003; 91: 73±80
Keywords: anaesthesia; muscle skeletal; surgery, abdominal
`It is generally agreed that in normal man lying supine the
act of expiration is passive'. These are the opening words of
the classic paper on abdominal muscle activity during
anaesthesia, by Freund, Roos, and Dodd in 1963.32 They
had noted abdominal activity in clinical practice, so they
studied 24 normal male volunteer subjects. They gave no
premedicants and took care to relax the abdomen: they
found no activity in conscious subjects. During anaesthesia
with halothane, they found that the abdominal muscles
became active (Fig. 1) Their ®ndings have been amply
corroborated in later studies, although often overlooked by
investigators who have concentrated on inspiratory muscle
actions, and perhaps come to incorrect conclusions when
expiratory activity was a more logical explanation of their
®ndings. For example, many writers have clung to the
attractive early theory that the respiratory muscles are
depressed by anaesthesia in a form of `ascending paralysis',
leaving the diaphragm working alone.60
In his Hunterian Lecture to the Royal College of
Surgeons of England in 1947, Howkins noted that respiratory complications after abdominal surgery were related to
reduced diaphragm movement, and that this in turn could be
related to reduced abdominal movement.43 He suggested a
number of remedies that bear consideration today including
early mobilization and physiotherapy, although others have
vanished with medical progress: to prevent depression of
breathing, analgesia was restricted to aspirin and bromide
and an example of rapid recovery and good morale was to
get a rear gunner back in a bomber on day 17 after surgery!
Nevertheless, abdominal movement remains poorly understood in patients after major surgery. Expiratory activity can
be easily demonstrated in the lower ribcage and upper
abdomen,28 and causes large changes in abdominal pressure.29 Simultaneous measurements of several variables
must be made to correctly infer the mechanical behaviour of
the respiratory system,64 and previous theories based on
limited measurements of movement35 or pressure31 have
been re-considered and recently reviewed.22 Put simply, the
relaxation of abdominal muscles which have been acting
during expiration, will result in pressure changes in the
pleural space similar to those caused by ribcage inspiratory
activity. These changes can be mistaken for inadequate
diaphragm activity. The factors that activate abdominal
muscles after surgery appear to be opioid analgesia, airway
obstruction, and perhaps wakefulness.66 Even after limited
abdominal surgery, pressure increases during expiration can
be considerable (Fig. 2) and would be expected to reduce
FRC by about 20%.85 At present, we have no effective
means of reducing the activity, apart from perhaps epidural
analgesia.
Abdominal wall: anatomy and actions
There are three ¯at layers of muscle in the abdominal wall.
From the inside out, these are the transversus, the internal
oblique, and the external oblique. Together, they form the
anterior shell that completes the container of the abdominal
contents. Their ®bres and aponeuroses are a geodetic
continuum with the other sheet-like muscles of the trunk,
arranged so that the wall of the abdomen can generate
tension in all directions. However, as the radius of curvature
is least in the transverse plane, it is the ®bres of the
transversus, that describe this curve, that are the most active
and important in respiration,18 58 despite the assertions of
anatomy books that it `acts only on the abdominal contents'!
These anterior muscles are balanced by the quadratus
lumborum at the back: at the sides, the lower rib margin and
the iliac crest are almost opposed. The quadratus lumborum
acts in concert with the posterior, vertebral part of the
diaphragam, essentially as its extension, and thus has a
distinctly different action from the anterior abdominal
muscles. Inserted between these layers, the rectus abdominis appears to have a more postural role, and is often silent
during breathing manoeuvres.
Ó The Board of Management and Trustees of the British Journal of Anaesthesia 2003
Drummond
Fig 1 Abdominal muscle activity during anaesthesia. Top trace: gastric
pressure. Middle trace is respiratory ¯ow (inspiration down). Bottom
trace, left: electromyogram of lateral abdominal (probably external
oblique) muscles: this is integrated after the second respiratory cycle.
Note the decrease in abdominal pressure at the onset of inspiration: this
represents abdominal relaxation. At end inspiration, abdominal pressure
increases as the diaphragm descends, and decreases as the diaphragm
relaxes. From Freund, Roos, and Dodd,32 with permission from the
publisher.
Fig 2 Abdominal pressure (measured from the bladder) in a patient 6 h
after abdominal hysterectomy, receiving morphine by patient controlled
analgesia. Lower trace is respiratory ¯ow at the nose, inspiration down.
There is mild inspiratory obstruction, shown by the ¯attened trace. (A)
Onset of inspiration: abdominal pressure decreases. (B) End-inspiration
with pressure generated by diaphragm descent, followed by increase in
expiration from abdominal muscle action (G. B. Drummond, unpublished
data).
The anterior abdominal muscles have two distinct
respiratory effects (Fig. 3) First, they pull on the rib
margins. This pull is in a downward and inward direction,
and if unopposed will reduce the volume of the rib cage, and
press on the abdominal contents, displacing them and the
diaphragm cranially. This action can be directly opposed by
the costal ®bres of the diaphragm, which can act to elevate
the rib margins, if the central tendon is prevented from
descending. Secondly, the abdominal muscles can increase
intra-abdominal pressure. If not opposed, this pressure acts
to increase the volume of the lower rib cage, by forcing it
out by pressure across the pleural sulcus: the area of
apposition of the diaphragm to the inside of the rib cage.
The exact effects on the ribcage therefore depend on the
relative degree of activation of the different muscles of the
abdominal wall, and clinical inspection of the anaesthetized
patient often reveals differential activation. Activation of
both abdominal and lower rib cage expiratory muscles
during halothane anaesthesia causes rib cage constriction,83
presumably re¯ecting the downward pull on the rib margins,
rather than expansion which would result if the main action
were through the increase in intra-abdominal pressure. In
addition, the results of animal studies may not apply in man,
because of the different shape of the ribcage.14
As a whole, the abdominal muscles act on the hydraulic
core of the abdominal contents,36 50 altering its shape as the
different muscles generate tension in the abdominal wall,
which may be considerably anisotropic. Changing curvature
of the spine adds a further factor in the relationship between
ribcage and abdominal dimensions and the volume of the
lungs.56 Much remains to be understood about the more
subtle shape changes, and many early reports may be only
partly correct, in particular because some widely used
sensors of abdominal motion do not detect this distortion
very well.12
Much has been written of the importance of adjusting the
diaphragm to its optimal length and shape to generate a
maximal inspiratory force when it contracts. There is no
doubt that the force that the diaphragm can generate
depends on its length,69 but it is not clear how important this
theory is in practical terms.15 Even in patients with severe
chronic obstructive lung disease, with diaphragms shortened
by 20%, the motion and change of length during tidal
breathing is the same as in normal subjects. Perhaps in acute
circumstances such as exercise, in addition to aiding rapid
expiration, abdominal muscle contraction can assist the
diaphragm contract more strongly, although evidence
suggests that it is already at its optimal length. In addition,
the stretching effect does not usually persist in inspiration,
as abdominal pressure decreases promptly at the onset of
inspiration (see for example Fig. 2).
Control of the expiratory muscles
In a recent exhaustive review, Iscoe44 pointed out that in
contrast to the inspiratory muscles, the muscles of expiration are relatively little known: yet this review has 15 pages
of references, and a more complete account is not to be
found. Some of the more pertinent aspects will be
considered here. However, even his review does not
mention, for example, any aspects of the effect of opioids
on abdominal muscles.
The expiratory muscles are controlled by neurones in the
ventral respiratory group in the medulla, and project, mainly
though polysynaptic pathways, to the lower thoracic and
74
Abdominal muscles in anaesthesia and after surgery
end-expiratory volume by about 20%.40 This will augment
the tidal volume generated by the inspiratory muscles and
probably also increases the effectiveness of contraction of
the diaphragm.
The expiratory muscles of the rib cage are activated
during normal deep sleep,19 65 but the response to increases
in airway pressure are reduced.75 Positive airway pressure is
a stimulus for abdominal muscle activation.7 This is
mediated by vagal afferents, transmitted via myelinated
®bres, which probably represent activity from the classic
lung stretch receptors. Activation of C ®bres by lung
irritation such as i.v. capsaicin inhibits the effects of positive
airway pressure.41 This inhibition of the re¯ex response to
positive airway pressure may explain why patients with lung
disease, who may have lung in¯ammation, allow their lung
volume to increase when constant positive airway pressure
is applied, rather than re¯ex contracting their abdominal
muscles to offset the increase. However, some of the control
of the abdominal muscles must also be from muscle
afferents, as dorsal root section, which will interrupt stretch
receptor activity also inhibits the response to positive airway
pressure.
The inspiratory and expiratory motoneurones are reciprocally activated during breathing, and the spinal cord
pathway for breathing control is separate from pathways
from the cortex that can activate the expiratory muscles4 or
pathways that control other functions such as cough.63 For
postural activity, the abdominal muscles have separate
distinguishable patterns of activity, whereas their activity is
coordinated during respiratory activity.37
The activity of the muscles is achieved by an increase
both in the number of active motor units and the frequency
of ®ring of motor units, in almost equal amounts. The
stimulation by hypoxia is reduced by hypocapnia.55
Fig 3 The actions of diaphragm and abdominal muscles. Top: diaphragm
activity will apply traction upwards to the costal insertions, if the
diaphragm is impeded in its descent by a rigid abdomen. At the same
time, abdominal pressure increase is transmitted through the pleural
sulcus (`zone of apposition') to act to expand the lower ribcage. Bottom:
the abdominal muscles can apply traction to the rib margins and pull
them down and in. At the same time, increased abdominal pressure acts
to distend the lower ribs and force the diaphragm cranially. The net
movement depends on the relative action of the different abdominal
muscles.
The effects of abdominal muscle contraction
Effects on the lung
If abdominal muscle contraction decreases thoracic volume
and transpulmonary pressure, then lung volume is reduced.
The exact effects of a decrease are not clear. If this decrease
was sudden, then airway resistance would increase as the
airway dimensions decrease.8 More importantly, small
airways could close as lung volume is reduced below
closing capacity. In circumstances where FRC was changed
acutely and passively, gas exchange is impaired with a
decrease in arterial oxygenation.11 Active expiration also
impairs oxygenation acutely.62 However, persistent expiratory activity may not have such an effect. If the chest wall is
restricted by binding, or even if subjects voluntarily activate
the expiratory muscles to reduce lung volume, the recoil
pressure of the lung increases,10 53 70 and the airways dilate
by a cholinergic mechanism,20 which might be expected to
offset the propensity of airways to narrow and close. In
addition, there are intrapulmonary re¯exes to redistribute
lumbar spinal cord.59 In the supine subject, the abdominal
muscles are usually inactive in quiet breathing. In the sitting
or standing position, they are active, and can have phasic
activity during expiration.13 27 The transversus abdominis is
the most easily activated,18 61 the obliques are less readily
brought into action, and the rectus abdominis has the least
prominent respiratory role.2 They become much more active
when breathing is stimulated, by exercise,37 chemical
stimuli,71 positive pressure on the airway,74 75 or voluntary
hyperventilation (Fig. 5). The responses to chemical stimuli
of hypoxia and hypercapnia appear to differ, with
hypercapnia generally more stimulant.48 86 In the upright
subject, exercise is a more effective and powerful stimulus
to activate the abdominal muscles than stimulation by
inhaled carbon dioxide, and serves to reduce the
75
Drummond
movement,80 although the link between these effects was
not clear. Nitrous oxide and morphine together cause
abdominal muscle activation33 as do other opioids.25
Effects of opioids during anaesthesia
After induction of anaesthesia with i.v. agents such as
thiopentone or propofol, FRC decreases by between 200 and
300 ml6 68 at a rate consistent with the rate of decrease of
tonic inspiratory activity in ribcage muscles such as the
sternomastoid and scalene,21 which act to elevate and ®x the
upper ribcage.27 After neuromuscular block, there is no
further change in FRC.6 However, in patients anaesthetized
with opioids, and breathing spontaneously, neuromuscular
block causes an increase in the end-expiratory lung volume
of about 400 ml. This is equivalent to removal of an
expiratory force on the respiratory system of about 10 cm
H2O.46 The contrasting effects of the loss of inspiratory
ribcage activity, and expiratory abdominal activity, in
relation to anaesthesia, are shown in Figure 4. When a
small dose of fentanyl is given to anaesthetized patients
breathing spontaneously, intra-abdominal pressure rapidly
increases by about 7 cm H2O25 and the pattern of abdominal
pressure change indicates contraction of the abdominal
muscles during expiration. This activity is enough to
contribute approximately 20% of the tidal volume.
Opioids increase skeletal muscle tone by a complex
pathway involving the locus coeruleus and several transmitters, including glutamine agonism34 and alpha 2
adrenergic inhibition.51 After giving opioids, the neural
pathway associated with rhythmic activation of the abdominal muscles is the usual pathway associated with respiratory activation of these muscles. In a neonatal rat
preparation, pre-inspiratory neurones near the nucleus
retrofacialis synapse with bulbospinal neurones in the
nucleus retroambigualis. This nucleus is the main location
of expiratory motoneurones. Activity passes from here to
the ®rst lumbar nerve root to generate abdominal muscle
contraction in a respiratory pattern, which persists after
opioid administration, even when inspiratory muscle activity is suppressed.45 Inspiratory and expiratory activity, at the
spinal level, appear to be reciprocally controlled by a
glycinergic inhibitory system. The action of opioids in this
preparation is to selectively depress inspiratory motoneurones by both pre- and post-synaptic actions.72 However,
others have found that opioids act on the rhythm generator,39 and certainly other depression by other neuromodulators affects pre-inspiratory neurones.5 Studies in less
elemental animal preparations show that opioids activate
thoracic motoneurons, but this activity may be entirely
caused by the hypercapnia after opioid administration.42 In
man, abdominal muscle activation during anaesthesia is
stimulated by hypercapnia, but giving an opioid will
increase the activity further. In the presence of an opioid,
hypercapnia seems to have little further effect.23
Fig 4 Diagrammatic representation of spirometry traces from Bergman6
and Kallos et al.46 At induction of anaesthesia, there is a prompt
decrease in FRC, which does not change further after giving a
neuromuscular blocking agent. In contrast, during anaesthesia with
fentanyl, FRC is increased after neuromuscular block, indicating the loss
of abdominal muscle contraction.
blood ¯ow that would offset any persistent impairment in
gas exchange. In patients after abdominal surgery, there is
no doubt that FRC is reduced and that gas exchange is
impaired, and the changes are correlated.3 However,
measurement of airway closure after abdominal surgery is
technically dif®cult and the explanation of hypoxaemia
solely in terms of increased airway closure is not well
supported.67
Effects on the chest wall
In exercise, or when the abdominal muscles are activated by
loading the inspiratory muscles, the action of the abdominal
muscles is to reduce the end-expiratory volume below
FRC.40 54 In this way, the abdominal muscles can contribute
to ventilation. In dogs, anaesthetized in the prone position,
about 40% of tidal volume may be generated by the
relaxation of the abdominal muscles, as this is a favourable
position for gravity to assist recoil of the abdominal wall.30
In man, abdominal activity may contribute about 20% of the
work of breathing.1
Effects of anaesthesia
In dogs, during stable isocapnic anaesthesia with pentobarbitone, abdominal muscle activity increased progressively:
this led to increased ribcage motion, despite constant
inspiratory activity.78 In man, halothane anaesthesia is
associated with increased abdominal muscle action particularly in men.32 83 Nitrous oxide augments abdominal muscle
action and is associated with a decrease in ribcage
76
Abdominal muscles in anaesthesia and after surgery
Fig 5 An example of distortion of the abdomen. Control breath: unloaded. Loaded breath: breathing through an expiratory resistance. Heavy solid line
is tidal volume, thin solid line is height of central abdomen, interrupted line height of lateral abdomen. During a control breath, both central and
lateral abdomen move out in synchrony. With the added load, paradoxical inward motion of the central abdomen is noted, because the central
abdomen protruded during active expiration. Data from Drummond and Duffy.24
properties of the respiratory system when respiration is
active (spontaneous) rather than passive (during mechanical
ventilation). It is a measure of `stiffness' of the respiratory
system, and attributed predominantly to the length/tension
relationship of actively contracting muscle: if a muscle's
shortening is impeded as it contracts, then the tension it
generates is increasedÐan intrinsic load compensation.
Derenne and co-workers16 noted that during anaesthesia
the ventilatory response was markedly reduced, indicated by
a decrease in the response of the mean inspiratory ¯ow rate
(VT/TI) to increased carbon dioxide. However, the mean
occlusion pressure values were not reduced during anaesthesia, although the slope of the response was less. In
consequence, the relationship between occlusion pressure
and mean inspiratory ¯ow (elastance) was substantially
different between the conscious and anaesthetized subjects,
suggesting that their inspiratory muscles had to generate far
more pressure to produce the same ¯ow during anaesthesia.
Their novel conclusion was that at least part of the
depression of ventilation was caused by increased stiffness,
or changed mechanics, of the respiratory system.
Is this conclusion justi®ed, and is there an alternative
explanation? There is no doubt that the occlusion pressure is
increased during anaesthesia, but at that time these workers
did not consider any contribution to this measure from the
abdominal muscles. During stimulation with carbon dioxide, they could be contracting during expiration, and the
Speci®c circumstances in anaesthesia
In normal breathing, there is remarkable coordination of the
activity of the respiratory muscles, so that the entire chest
wall moves synchronously and proportionally.47 Generally,
respiratory depression is attributed to a reduction in the
central drive to breathe, but it is certainly possible that
during anaesthesia, loss of coordination of the chest wall
muscles, or changes in the mechanical properties of the
respiratory system, may reduce the volume of breathing for
a given `effort' or central drive.
Derenne and co-workers16 favoured this possibility in a
study that compared subjects before and during anaesthesia.
They assessed central `effort' using occlusion pressure,
which was measured as the decrease in mouth pressure
when the airway was transiently occluded at the start of
inspiration. This provides an index of the force of activation
of the inspiratory muscles.84 It quanti®es the integrated
inspiratory effort of the respiratory system, with the muscles
contracting isometrically (although there may be shortening
of some muscles and lengthening of others if the system
distorts during this transiently occluded effort). The resultant measure of respiratory system activity can be combined
with the volume change during a normal breath to calculate
the `effective elastance' of the system. This value can
predict the response of the respiratory system when
inspiration is impeded by adding a load to the inspiration,52
and can be thought of as a measure of the mechanical
77
Drummond
early part of inspiration would be assisted by their
relaxation. Indeed inspection of the occlusion pressures
illustrated (their ®g. 3) show a similar substantial effect
early in inspiration, and they did show subsequently that
occlusion pressure was generated at least in part by
abdominal relaxation.38 Such a contribution, present during
anaesthesia, but not in the control measurements, can
explain their observations simply, without the hypothesis
that the active elastance of the respiratory system has been
affected. This explanation is also consistent with similar
observations of occlusion pressure and ventilation.
However, in other studies using the same agent (methoxy¯urane) the same workers argued that expiratory activity
was not present.17 As this agent is no longer used, it would
be helpful to study other current agents to establish the
contribution of abdominal muscle action to `occlusion
pressure', as there is no doubt that this is increased during
anaesthesia.9
Others have considered the change in pattern of respiratory movements to explain reduced ribcage responses to
stimulation.73 In a study of adolescents, ribcage responses to
stimulation of breathing with carbon dioxide were much
more reduced than the abdominal movements during
halothane anaesthesia. They attributed these changes to a
loss of the contribution of the intercostal muscles, and
present recordings that show the change with loss and
recovery of consciousness. However, these records also
show obvious paradoxical motion of the abdomen developing during anaesthesia, in contrast to the synchronous
movement present in the conscious subject. Abdominal
muscle action during expiration can expand the ribcage, by
generating outward pressure on the lower ribs: at the onset
of inspiration, as the abdominal muscles relax, the abdomen
changes shape suddenly, and an indrawing is noted,26
causing a pattern of motion exactly the same as those
illustrated in the report by Tusiewicz and colleagues. This
explanation is perhaps more valid than attributing the
changes to loss of intercostal activity as these muscles act
more to stabilise the ribcage than to expand it, and are
unlikely to be important agonists.49 Activation of abdominal
muscles during anaesthesia was demonstrated in a later
study,81 which was unable to replicate the large change in
ribcage movements found in the study of Tusiewicz.
Stimulation of respiration by re-breathing accentuated the
activation of abdominal expiratory activity.79 In most
subjects, the ribcage expanded in early expiration. One
dif®culty with interpreting the results of such studies is that
the dimensions are from single circumferences of the
ribcage and abdomen, and there is no doubt that the shape
changes that occur are complex and poorly expressed by a
single summative dimension. For example, the ribcage
above and below the zone of apposition to the abdominal
contents is exposed to different forces and can move in
different ways,57 76 and the lateral and central parts of the
abdomen can also move paradoxically in circumstances
such as loaded breathing (Fig. 5).
Conclusions
Anaesthesia disturbs the coordinated motion of the chest
wall. Although there is no doubt that central respiratory
drive is reduced by anaesthetic agents, abnormal movements may possibly contribute to reduced ventilation and
affect the distribution of ventilation and impair gas
exchange.77 82 To obtain more exact information about the
extent and impact of these changes, better methods for
assessment of chest wall movement are required, preferably
not involving big expensive apparatus or ionizing radiation.
In addition, with a model to investigate features such as how
opioids increase abdominal contraction, we might develop
treatments to modify these effects, and perhaps reduce
respiratory complications after surgery, the goal of Howkins
in 1947.
References
1 Abbrecht PH, Rajagopal KR, Kyle RR. Expiratory muscle
recruitment during inspiratory ¯ow-resistive loading and
exercise. Am Rev Respir Dis 1991; 144: 113±20
2 Abe T, Kusuhara N, Yoshimura N, Tomita T, Easton PA.
Differential respiratory activity of four abdominal muscles in
humans. J Appl Physiol 1996; 80: 1379±89
3 Alexander JI, Spence AA, Parikh RK, Stuart B. The role of airway
closure in postoperative hypoxaemia. Br J Anaesth 1973; 45:
34±40
4 Aminoff MJ, Sears TA. Spinal integration of segmental, cortical
and breathing inputs to thoracic respiratory motoneurons.
J Physiol 1971; 215: 557±75
5 Ballanyi K, Onimaru H, Homma I. Respiratory network function
in the isolated brainstem-spinal cord of newborn rats. Prog
Neurobiol 1999; 59: 583±634
6 Bergman NA. Reduction in resting end-expiratory position of the
respiratory system with induction of anesthesia and
neuromuscular paralysis. Anesthesiology 1982; 57: 14±7
7 Bishop B. Re¯ex control of abdominal muscles during positivepressure breathing. J Appl Physiol 1964; 19: 224±32
8 Briscoe WA, DuBois AB. The relationship between airway
resistance, airway conductance and lung volume in subjects of
different age and body size. J Clin Invest 1958; 37: 464±71
9 Canet J, Sanchis J, Zegri A, Llorente C, Navajas D, Casan P.
Effects of halothane and iso¯urane on ventilation and occlusion
pressure. Anesthesiology 1994; 81: 563±71
10 Caro CG, Butler J, DuBois AB. Some effects of restriction of
chest cage expansion on pulmonary function in man: an
experimental study. J Clin Invest 1960; 39: 573±83
11 Craig DB, Wahba WM, Don HF, Couture J, Becklake MR.
`Closing volume' and its relationship to gas exchange in seated
and supine positions. J Appl Physiol 1976; 31: 717±21
12 De Groote A, Verbandt Y, Paiva M, Mathys P. Measurement of
thoracoabdominal asynchrony: importance of sensor sensitivity
to cross section deformations. J Appl Physiol 2000; 88: 1295±302
13 De Troyer A. Mechanical action of the abdominal muscles. Bull
Eur Physiopathol Respir 1983; 19: 575±81
14 De Troyer A, Estenne M. Functional anatomy of the respiratory
muscles. Clinics Chest Med 1988; 9: 175±93
15 Decramer M. Hyperin¯ation and respiratory muscle interaction.
Eur Respir J 1997; 10: 934±41
16 Derenne J-P, Couture J, Iscoe S, Whitelaw WA, Milic-Emili J.
78
Abdominal muscles in anaesthesia and after surgery
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
Occlusion pressures in men rebreathing CO2 under
methoxy¯urane anesthesia. J Appl Physiol 1976; 40: 805±14
Derenne J-P, Whitelaw WA, Couture J, Milic-Emili J. Load
compensation during positive pressure breathing in anesthetized
man. Respir Physiol 1986; 65: 303±14
DeTroyer A, Estenne M, Ninane V, VanGansbeke D, Gorini M.
Transversus abdominis muscle function in humans. J Appl Physiol
1990; 68: 1010±6
Dick TE, Parmeggiani PL, Orem J. Intercostal muscle activation
during sleep in the cat: an augmentation of expiratory activity.
Respir Physiol 1982; 50: 255±65
Douglas NJ, Drummond GB, Sudlow MF. Breathing at low lung
volumes and chest strapping: a comparison of lung mechanics.
J Appl Physiol 1981; 50: 650±7
Drummond GB. Reduction of tonic ribcage muscle activity by
anesthesia with thiopental. Anesthesiology 1987; 67: 695±700
Drummond GB. Diaphragmatic dysfunction: an outmoded
concept. Br J Anaesth 1998; 80: 277±80
Drummond GB. Separate effects of respiratory stimuli and
depressants on abdominal muscle action. In: Dahan A, Teppema
L, Van Beek JHGM, eds. Physiology and Pharmacology of CardioRespiratory Control. Dordrecht: Kluwer Academic Publishers,
1998: 101±8
Drummond GB, Duffy ND. A video-based optical system for
rapid measurements of chest wall movement. Physiol Meas 2001;
22: 489±503
Drummond GB, Duncan MK. Abdominal pressure during
laparoscopy: effects of fentanyl. Br J Anaesth 2002; 88: 384±8
Drummond GB, Nimmo AF. Thoracoabdominal mechanics and
respiration after abdominal surgery. Br J Anaesth 1995; 74: 486P
Druz WS, Sharp JT. Activity of respiratory muscles in upright and
recumbent humans. J Appl Physiol 1981; 51: 1552±61
Duggan J, Drummond GB. Activity of lower intercostal and
abdominal muscle after upper abdominal surgery. Anesth Analg
1987; 66: 852±5
Duggan JE, Drummond GB. Abdominal muscle activity and
intraabdominal pressure after upper abdominal surgery. Anesth
Analg 1989; 69: 598±603
Farkas GA, Schroeder MA. Mechanical role of expiratory
muscles during breathing in prone anesthetized dogs. J Appl
Physiol 1990; 69: 2137±42
Ford GT, Whitelaw WA, Rosenal TW, Cruse PJ, Guenter CA.
Diaphragm function after upper abdominal surgery in humans.
Am Rev Respir Dis 1983; 127: 431±6
Freund F, Roos A, Dodd RB. Expiratory activity of the abdominal
muscles in man during general anesthesia. J Appl Physiol 1964; 19:
693±7
Freund FG, Martin WE, Wong KC, Hornbein TF. Abdominal
muscle rigidity induced by morphine and nitrous oxide.
Anesthesiology 1973; 38: 358±62
Fu M-J, Tsen L-Y, Lee T-Y, Lui P-W, Chan SHH. Involvement of
cerulospinal glutamatergic neurotransmission in fentanyl-induced
muscular rigidity in the rat. Anesthesiology 1997; 87: 1450±9
Gilbert R, Auchincloss JH, Peppi D. Relationship of rib cage and
abdomen motion to diaphragm function during quiet breathing.
Chest 1981; 80: 607±12
Gilroy RL, Lavietes MH, Loring SH, Mangura BT, Mead J.
Respiratory mechanical effects of abdominal distension. J Appl
Physiol 1986; 58: 1997±2003
Goldman JM, Lehr RP, Millar AB, Silver JR. An electromyographic
study of the abdominal muscles during postural and respiratory
maneuvers. J Neurol Neurosur Psychatry 1987; 50: 866±9
Grassino AE, Derenne J-P, Almirall J, Milic-Emili J, Whitelaw WA.
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
79
Con®guration of the chest wall and occlusion pressure in awake
humans. J Appl Physiol 1981; 50: 134±42
Greer JJ, Carter JE, Al-Zubaidy Z. Opioid depression of
respiration in neonatal rats. J Physiol 1995; 485: 845±55
Henke KG, Sharratt M, Pegelow D, Dempsey JA. Regulation of
end-expiratory lung volume during exercise. J Appl Physiol 1988;
64: 135±46
Hollstein SB, Carl ML, Schelegle ES, Green JF. Role of vagal
afferents in the control of abdominal expiratory muscle activity
in the dog. J Appl Physiol 1991; 71: 1795±800
Howard RS, Sears TA. The effects of opiates on the respiratory
activity of thoracic motoneurones in the anaesthetized and
decerebrated rabbit. J Physiol 1990; 437: 181±99
Howkins J. Movement of the diaphragm after operation. Lancet
1948; 85±8
Iscoe S. Control of abdominal muscles. Prog Neurobiol 1998; 56:
433±506
Janczewski WA, Onimaru H, Homma I, Feldman JL. Opioidresistant respiratory pathway from the preinspiratory neurones
to abdominal muscles: in vivo and in vitro study in the newborn
rat. J Physiol 2002; 545: 1017±26
Kallos T, Wyche MQ, Garman JK. The effects of Innovar on
functional residual capacity and total chest compliance in man.
Anesthesiology 1973; 39: 558±61
Konno K, Mead J. Measurement of the separate volume changes
of the rib cage and abdomen during breathing. J Appl Physiol 1967;
22: 407±22
Ledlie JF, Pack AI, Fishman AP. Effects of hypercapnia and
hypoxia on abdominal expiratory nerve activity. J Appl Physiol
1983; 55: 1614±22
Legrand A, Wilson TA, DeTroyer A. Rib cage muscle interaction
in airway pressure generation. J Appl Physiol 1998; 85: 198±203
Loring SH, Mead J, Griscom NT. Dependence of diaphragmatic
length on lung volume and thoracoabdominal con®guration.
J Appl Physiol 1985; 59: 1961±70
Lui PW, Lee TY, Chan SHH. Involvement of coerulospinal
noradrenergic pathway in fentanyl-induced muscular rigidity in
rats. Neurosci Lett 1990; 108: 183±8
Lynne-Davies P, Couture J, Pengelly LD, Milic-Emili J. Immediate
ventilatory response to added inspiratory elastic loads in cats.
J Appl Physiol 1971; 30: 512±6
Manco JC, Hyatt RE. Relationship of air trapping to increased
lung recoil pressure induced by rib cage restriction. Am Rev
Respir Dis 1975; 111: 21±6
Martin JG, De Troyer A. The behaviour of the abdominal
muscles during inspiratory mechanical loading. Respir Physiol
1982; 50: 63±73
Mateika JH, Essif E, Fregosi RF. Effect of hypoxia on abdominal
motor unit activities in spontaneously breathing cats. J Appl
Physiol 2003; 81: 2428±35
McCool FD, Kelly KB, Loring SH, Greaves IA, Mead J. Estimates
of ventilation from body surface measurements in unrestrained
subjects. J Appl Physiol 1986; 61: 1114±9
McCool FD, Loring SH, Mead J. Rib cage distrotuion during
voluntary and involuntary breathing acts. J Appl Physiol 1985; 58:
1703±12
Mier A, Brophy C, Estenne N, Moxham J, Green M, De Troyer
A. Action of abdominal muscles on rib cage in humans. J Appl
Physiol 1985; 58: 1438±43
Miller AD, Ezure K, Suzuki I. Control of abdominal muscles by
brain stem respiratory neurons in the cat. J Neurophysiol 1985;
54: 155±67
Miller AH. Ascending respiratory paralysis under general
anesthesia. J Am Med Assoc 1925; 34: 201±2
Drummond
74 van der Schans CP, de Jong W, de Vries G, Postma DS,
Koeter GH, van der Mark ThW. Effect of positive expiratory
pressure on breathing pattern on healthy subjects. Eur Respir
J 1993; 6: 60±6
75 Wakai Y, Welsh MM, Leevers AM, Road JD. Expiratory muscle
activity in the awake and sleeping human during lung in¯ation and
hypercapnia. J Appl Physiol 1992; 72: 881±7
76 Ward ME, Ward JW, Macklem PT. Analysis of human chest wall
motion using a two-compartment rib cage model. J Appl Physiol
1992; 72: 1338±47
77 Warner DO. Diaphragm function during anesthesia: still crazy
after all these years. Anesthesiology 2002; 97: 295±7
78 Warner DO, Joyner MJ, Rehder K. Electrical activation of
expiratory muscles increases with time in pentobarbitalanesthetized dogs. J Appl Physiol 1992; 72: 2285±91
79 Warner DO, Warner MA. Human chest wall function while
awake and during halothane anesthesia: II. Carbon dioxide
rebreathing. Anesthesiology 1995; 82: 20±31
80 Warner DO, Warner MA, Joyner MJ, Ritman EL. The effect of
nitrous oxide on chest wall function in humans and dogs. Anesth
Analg 1998; 86: 1058±64
81 Warner DO, Warner MA, Ritman EL. Human chest wall function
while awake and during halothane anesthesia: I. Quiet breathing.
Anesthesiology 1995; 82: 6±19
82 Warner DO, Warner MA, Ritman EL. Atelectasis and chest wall
shape during halothane anesthesia. Anesthesiology 1996; 85:
49±59
83 Warner DO, Warner MA, Ritman EL. Mechanical signi®cance of
respiratory muscle activity in humans during halothane
anesthesia. Anesthesiology 1996; 84: 309±21
84 Whitelaw WA, Derenne J-P, Milic-Emili J. Occlusion pressure as
a measure of respiratory center output in conscious man. Respir
Physiol 1975; 23: 181±99
85 Wyche MQ, Teichner RL, Kallos T, Marshall BE, Smith TC.
Effects of continuous positive-pressure breathing on functional
residual capacity and arterial oxygenation during intra-abdominal
operations: studies in man during nitrous oxide and
d-tubocurarine anesthesia. Anesthesiology 1973; 38: 68±74
86 Yasuma F, Kimoff RJ, Kozar LF, et al. Abdominal muscle
activation by respiratory stimuli in conscious dogs. J Appl
Physiol 1993; 74: 16±23
61 Misuri G, Colagrande S, Gorini M. et al. In vivo ultrasound
assessment of respiratory function of abdominal muscles in
normal subjects. Eur Respir J 1997; 10: 2861±7
62 Morrison SC, Stubbing DG, Zimmerman PV, Campbell EJM. Lung
volume, closing volume, and gas exchange. J Appl Physiol 1982; 52:
1453±7
63 NewsomDavis J, Plum F. Separation of descending spinal
pathways to respiratory motoneurons. Exp Neurol 1972; 34:
78±94
64 Nimmo AF, Drummond GB. Respiratory mechanics after
abdominal surgery measured with continuous analysis of
pressure, ¯ow and volume signals. Br J Anaesth 1996; 77:
317±26
65 Plowman L, Lauff DC, Berthon-Jones M, Sullivan CE. Abdominal
muscle-activity in conscious dogsÐeffect of sleep and route of
breathing. Respir Physiol 1990; 81: 321±36
66 Rahman MQ, Kingshott RN, Wraith P, Adams WH, Drummond
GB. Association of airway obstruction, sleep, and phasic
abdominal muscle activity after upper abdominal surgery. Br J
Anaesth 2001; 87: 198±203
67 Rehder K, Marsh HM, Rodarte JR, Hyatt RE. Airway closure.
Anesthesiology 1977; 47: 40±52
68 Rutherford JS, Logan MR, Drummond GB. Changes in endexpiratory lung volume on induction of anaesthesia with
thiopentone or propofol. Br J Anaesth 1994; 73: 579±82
69 Smith J, Bellemare F. Effect of lung volume on in vivo contraction
characteristics of human diaphragm. J Appl Physiol 1987; 62:
1893±900
70 Sybrecht GW, Garrett L, Anthonisen NR. Effect of chest
strapping on regional lung function. J Appl Physiol 1975; 39:
707±13
71 Takasaki Y, Orr D, Popkin J, Xie A, Bradley TD. Effect of
hypercapnia and hypoxia on respiratory muscle activation in
humans. J Appl Physiol 1989; 67: 1776±84
72 Takeda GW, Eriksson LI, Yamamoto Y, Joensen H, Onimaru H,
Lindahl SGE. Opioid action on respiratory neuron activity of the
isolated respiratory network in newborn rats. Anesthesiology
2001; 95: 740±9
73 Tusiewicz K, Bryan AC, Froese AB. Contributions of changing
rib cage-diaphragm interactions to the ventilatory depression of
halothane anesthesia. Anesthesiology 1977; 47: 327±37
80