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1 Meakins-Christie
Laboratories, ABSTRACT Kenyon, C. M., S. J. Cala, S. Yan, A. Aliverti, G. Scano, R. Duranti, A. Pedotti, and Peter T. Macklem. Rib cage mechanics during quiet breathing and exercise in humans. J. Appl. Physiol. 83(4): 1242-1255, 1997.
respiratory kinematics; respiratory muscles; rib cage distortions; rib cage bending stiffness; diaphragm
INTRODUCTION DURING EXERCISE, large respiratory pressure swings are
generated that result in highly nonuniform pressures in the pleural space over the inner surface of the rib cage. The pressure over the
lung-apposed or pulmonary part of the rib cage is pleural pressure
(Ppl) over the costal surface of the lung, which falls during
inspiration, whereas over the diaphragm-apposed or abdominal part, Ppl
is approximated by abdominal pressure (Pab) (20), which normally rises
during a quiet inspiration. In addition, the diaphragm and some of the
abdominal muscles insert directly onto ribs 7-12 and have
inflationary and deflationary actions, respectively, on the abdominal
but not on the pulmonary part of the rib cage. Nondiaphragmatic
inspiratory muscles (scalenes, parasternal intercostals, and
sternocleidomastoids) insert on ribs 1-6 and have inflationary
actions on the pulmonary but not on the abdominal part (3, 9, 31). Rib
cage distortions caused by these nonuniform pressures and the resultant
restoring forces are unknown in exercise but have been measured during
isolated diaphragmatic contractions and quiet breathing (9, 31). We use
an extension of the two-compartment model of the rib cage used
previously (31) to calculate rib cage distortions and restoring forces
during exercise.
Unitary behavior of the rib cage requires that the net pressures acting
on the two rib cage compartments be equal, and this would require
considerable coordination of the respiratory muscles. Thus it is not
surprising that several studies have shown various degrees of departure
from the undistorted configuration of the rib cage during increased
respiratory efforts (27, 28) and in quiet breathing (21, 31). All these
studies have assessed distortion by measuring rib cage dimensions or
cross-sectional areas. Although from a respiratory point of view,
compartmental volume change or lack of it is the most crucial variable,
it has not been possible to measure the volume of chest wall
compartments directly. Recently, an optical tracking device (ELITE) has
been developed that can give the three-dimensional location of many markers with the high temporal (100 Hz) and spatial accuracy (±0.2 mm) required for respiratory measurements (5, 13). We have used this
device with a configuration of marker points (5) designed specifically
to measure the volume of three chest wall compartments, the pulmonary
and abdominal rib cage compartments and the abdomen, directly.
We report rib cage distortions measured by displacements of the
pulmonary and abdominal rib cage compartments away from their undistorted relaxation configurations during exercise at various power
outputs. From the measured distortions, we calculate the restoring
forces (expressed as a pressure) and, knowing these, the pressures
developed by the nondiaphragmatic inspiratory muscles. These pressures
have not been measured, except during quiet breathing (31).
To make these measurements, we model the two rib cage compartments
mechanically coupled to each other, with nondiaphragmatic inspiratory
muscles acting on the pulmonary rib cage and the diaphragm and
abdominal muscles acting on the abdominal rib cage. This model extends
that of Ward et al. (31) by including the actions of abdominal muscles
on the abdominal rib cage. These were not previously estimated,
inasmuch as only quiet breathing was being studied when expiratory
muscles were minimally activated. We use a normalization for rib cage
distortion (9) so different subjects can be directly compared for
distortability and for the amount of distortion during exercise.
Glossary
METHODS
During
exercise, large pleural, abdominal, and transdiaphragmatic pressure
swings might produce substantial rib cage (RC) distortions. We used a
three-compartment chest wall model (J. Appl.
Physiol. 72: 1338-1347, 1992) to measure
distortions of lung- and diaphragm-apposed RC compartments (RCp and
RCa) along with pleural and abdominal pressures in five normal men. RCp
and RCa volumes were calculated from three-dimensional locations of 86 markers on the chest wall, and the undistorted (relaxation) RC
configuration was measured. Compliances of RCp and RCa measured during
phrenic stimulation against a closed airway were 20 and 0%,
respectively, of their values during relaxation. There was marked RC
distortion. Thus nonuniform distribution of pressures distorts the RC
and markedly stiffens it. However, during steady-state ergometer
exercise at 0, 30, 50, and 70% of maximum workload, RC distortions
were small because of a coordinated action of respiratory muscles, so
that net pressures acting on RCp and RCa were nearly the same
throughout the respiratory cycle. This maximizes RC compliance and
minimizes the work of RC displacement. During quiet breathing, plots of
RCa volume vs. abdominal pressure were to the right of the relaxation
curve, indicating an expiratory action on RCa. We attribute this to
passive stretching of abdominal muscles, which more than
counterbalances the insertional component of transdiaphragmatic pressure.
ABM,ins
Abdominal muscles acting to deflate RCa
ABM,nins
Abdominal muscles with no action on RCa
C
Static compliance of rib cage compartments measured during relaxation
C
Dynamic compliance of rib cage compartments measured during bilateral
phrenic nerve stimulation
FRC
Functional residual capacity
Pab
Abdominal pressure
Pabm
Pressure developed by abdominal muscles (Pab
Pabw)
Pabw
Elastic recoil pressure of abdomen
Pbs
Body surface pressure
Pdi
Transdiaphragmatic pressure (Pab
Px + Px Ppl, as measured by Pga Pes)
Pes
Esophageal pressure
Pga
Gastric pressure
Plink
Restoring pressure acting to diminish rib cage distortion, which arises
from distortions away from relaxation configuration of RCp and RCa and
bending stiffness of the rib cage
Pm
Mouth pressure
Ppl
Pleural pressure
Prc,a
Elastic recoil pressure of RCa
Prcm
Pressure developed by rib cage muscles
Prc,p
Elastic recoil pressure of RCp
Pv
Net pressure acting on RCp resulting from Ppl + Prcm before effects of
distortion are taken into account
Pw
Net pressure acting on RCa before effects of distortion resulting from
(Px
Ppl) + (Pab Py) are taken into account
Px
Imaginary pressure between Pab and Ppl; it partitions Pdi into a costal
component (Px
Ppl) and a
crural component (Pab Px)
Py
Imaginary pressure between Pab and Pabw; it partitions Pabm into an
insertional component (Py
Pabw), which has a deflationary action on RCa, and a noninsertional
component (Pab Py),
which has no action on RCa
RCa
Abdominal or diaphragm-apposed rib cage
RCp
Pulmonary or lung-apposed rib cage
TI
Inspiratory time
Vab
Volume of abdomen
VL
Lung volume
Vrc,a
Volume of RCa
Vrc,p
Volume of RCp
maxMaximum exercise workload
xPdi
Insertional component of Pdi or fraction of Pdi that has a direct
inflating action on RCa, where 0
x 1
yPabm
Insertional component of Pabm, where 0
y 1
Ppl in
the model), and a noninsertional component, which does not (Pab Px). ABM,ins acts hydraulically
in series with ABM,nins to displace the abdomen inward and to increase
Pab, which is transmitted through the diaphragm to act at the inner surface of RCa in the area of apposition of the diaphragm to the rib
cage. This inflationary action of Pab on RCa is counterbalanced by the
deflating action of ABM,ins given by
Py Pabw. Pabw is the
elastic recoil pressure of the abdominal wall, and Py (analogous to
Px) is an imaginary pressure partitioning the total pressure developed by abdominal muscles (Pabm)
into an insertional (Py Pabw) and a noninsertional (Pab Py) component. The role of the
abdominal muscles and their actions during exercise are extensively
discussed elsewhere (3). However, there is an important distinction
between our model of the abdomen and previous models. To the best of
our knowledge, all previous models have stated that the elastic recoil
pressure of the abdomen is given by Pab relative to body surface
pressure (Pbs) (12, 14, 16). Thus the elastic recoil of the abdomen includes passive stretching of the abdominal muscles. We specifically do not include passive stretching of abdominal muscles as contributing to the elastic recoil of the abdominal wall in our hydraulic model. Thus we take Pabw relative to body surface pressure as the elastic recoil pressure, not Pab, as in previous models.
Following Ward et al. (31), we can now describe the pressures developed by various muscles and write pressure balance equations. Pdi is given by the sum of the pressures acting across the costal and crural parts of the diaphragm (12, 19): Pdi = (Pab
Px) + (Px Ppl). We assume that
the insertional component of Pdi
(Px Ppl) is a constant
fraction of Pdi and can be represented as
xPdi, where 0 
x 1. Similarly, we assume that the
insertional component of abdominal muscles
(Py Pabw) is a constant
fraction of the total pressure developed by the abdominal muscles (Pabm = Pab Pabw) and can be represented by
yPabm, where 0 y 1. Thus the pressure acting on
RCa before the contribution of distortion
(Plink) is taken into account is the output (Pw) of the
lowermost summing junction
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(1) |
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(2) |
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(3) |
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Pdi, which is proportional to the difference in pressure acting on
each compartment (9, 31).
is length
AB perpendicular to relaxation line divided by volume of RCp (Vrc,p) at
B taken as a percentage, as in
Chihara et al. (9). Vrc,a, volume of RCa.
Right: relaxation pressure-volume
curve of RCp is given by long line with positive slope. During phrenic
stimulation, RCp follows pathway BA;
point B, Vrc,p at functional residual
capacity. CD, change in Prc,p during
twitch; DA, change in esophageal
pressure (Pes). Inasmuch as Prc,p = Ppl + Plink,
Plink = AC.
Under equilibrium conditions, Prc,p when RCp is displaced off its relaxation line is balanced by other pressures acting on it. Thus
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(4) |
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max) was assessed by an incremental exercise test
on a cycle ergometer by increasing the work rate by 50-W steps until
exhaustion, which was at 250-300 W, depending on the subject.
Esophageal (Pes) and gastric (Pga) pressures were measured with
conventional balloon catheters and were used as indexes of Ppl and Pab.
Rib cage distortability was assessed by bilateral transcutaneous
phrenic stimulation at increasing intensities to obtain a range of
distortions.
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max), and exercising at 30, 50, and 70%
max. Each level was maintained for 3 min and 20 s,
and data were acquired during the last 20 s of each level. Subjects
breathed on a mouthpiece attached to a three-way valve, one way going
to a water displacement spirometer with a
CO2 absorber and the other to room
air. The subject was switched from room air to the spirometer for the
last 20 s at each level, and the bell was refreshed with room air
during the other 3 min. This was used to provide a check on the changes in VL calculated from the body
surface markers. Compartmental volume displacements were assessed from
surface markers that were optically tracked in three dimensions, and
rib cage volumes were subsequently calculated (5). While the subjects
were seated on the cycle ergometer, their forearms were supported away
from the sides of the body comfortably below shoulder height, allowing markers on the body surface to be tracked in three dimensions by
television cameras in front of and behind them.
Compartmental volume measurements.
Volumes were measured directly from the movements of surface markers on
the chest wall using an optical tracking system (ELITE) (5, 13). This
system has been previously described for respiratory use (13); however,
we used an extended marker configuration with 86 markers rather than 32 (5) to improve volume accuracy and to delimit anatomically the specific
rib cage compartments. Figure 3 shows the
anatomic placement of the markers, and Fig. 4 illustrates the construction of the
volume compartments. The markers were tracked in three dimensions by
four videocameras: two in front of the subject and two behind. Each set
of cameras was aligned vertically: one near the floor and the other
near the ceiling. Volumes for each compartment were calculated by
constructing a triangulation over the surface and then using Gauss's
theorem to convert the volume integral to an integral over this
surface, as described previously (5). The ELITE system calculates
absolute volumes, and we used the absolute volume of each compartment
at functional residual capacity (FRC) as the reference volume. Volumes are reported in absolute numbers or as deviations from FRC expressed as
percent vital capacity for that compartment.
We defined the abdominal compartment as extending caudally from the lower rib cage to the level of the anterior superior iliac crest and used the surface markers to calculate its volume (Vab). Thus the chest wall volume Vcw = Vrc,p + Vrc,a + Vab, and changes in VL can be calculated as
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Vrc,p, Vrc,a, and Vab during isovolume maneuvers and
during phrenic twitches against a closed airway when
VL = 0. Data collection was
carried out at 100 Hz. Length of collection was limited to 20 s by
system overload, which generally occurred with 86 markers after 25 s of
collection because of hardware limitations. Volume validations have
previously been presented with this system and marker configuration,
along with a sensitivity analysis, which assess accuracy as a function
of marker number and position (5).
Pressure measurements.
Pes and Pga were measured using catheter-balloon systems connected to
pressure transducers (Validyne MP 45, ±100
cmH2O) and recorded digitally onto
the IBM-compatible PC, which was also used for the marker positions via
the ELITE system. Mouth pressure (Pm) was also recorded via a pressure
transducer (Validyne MP 45, ±100
cmH2O) attached to the mouthpiece.
Measurement of rib cage distortability and restoring pressures.
Relaxation characteristics were established for the chest wall by
having subjects breathe in to total lung capacity and then relax and
breathe out through a high resistance to FRC. Relaxation maneuvers were
repeated until curves were reproducible, Pm finished at zero, and Pdi
was zero throughout. A plot of Vrc,p vs. Vrc,a during relaxation
defined the undistorted rib cage configuration.
Distortions were measured during bilateral transcutaneous phrenic
stimulation with submaximal single twitches and supramaximal single and
double twitches. Twitches were 1 ms in duration and 50 ms apart for
double twitches and were repeated 10 times at 2-s intervals during
breath holding at FRC with the glottis closed. Electrical activity of
the diaphragm was monitored from surface electrodes in the sixth and
seventh intercostal spaces on each side. The mass action potentials for
any given stimulus mode were highly reproducible and for supramaximal
stimuli were independent of current. Distortability and
Plink were calculated as described above.
Data analysis.
Rib cage distortion and Plink were
calculated at each level of exercise from average breaths created for
each subject by linear stretch, so breaths of different duration could
be combined. Overall the breaths combined were very uniform, requiring
<10% stretching, except in one subject
(PG) at the lowest level of
exercise. We calculated average distortion and range of distortion over
these average breaths as well as the corresponding values of
Plink. Pdi was measured directly
as Pga Pes. Knowing Plink,
Pes, and Prc,p allowed us to calculate Prcm as the only unknown in
Eq. 4.
RESULTS
max). The worst coefficient of
variation of the two signals was 4%. The mean regression coefficient
between the two was 0.97 ± 0.04 (SD) (range 0.93-1.04), with a
mean intercept of 0.01 ± 0.04 (SD) liter (range 0.05 to
+0.06l) for all subjects at the highest level of exercise (Table
2).
0.05, where values are in liters,
coefficient of variation = 4%, and
r2 = 0.994.
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Vrc,p, Vrc,a, and Vab during twitch
diaphragm contractions was +0.059 ± 0.12l (SD) liter
(n = 104) with no relation to twitch
Pdi (r2 for
regression = 0.01). Vab increased and Vrc,p decreased by approximately
equal amounts in each twitch by up to 0.4 liter at a Pdi of 25 cmH2O. Vrc,a changed very little:
the maximum increase was 0.015 liter, and the maximum decrease was
0.010 liter. Regression relations were Vrc,p = 0.013Pdi 0.01 (r2 = 0.65), Vab = 0.012Pdi + 0.046 (r2 = 0.69), and
Vrc,a = 0.002Pdi 0.007 (r2 = 0.05),
using all the twitch data for all subjects.
Rib cage pressure-volume characteristics.
The pressure-volume relations of the rib cage compartments during
relaxation and phrenic twitches are shown in Fig.
6. Relaxation was from total lung capacity
to FRC, and twitches were also performed at FRC; linear extrapolation
was performed for volumes below FRC. The dynamic compliances during
phrenic stimulation of RCp and RCA (Crc,p and Crc,a) were
less than their static compliances (Crc,p and Crc,a), and Vrc,a
during phrenic stimulation was almost zero. These compliances were
calculated as Vrc,p/Pes and Vrc,a/Pga, respectively, during
relaxation and phrenic twitches and are shown in Table
3. Crc,a is roughly one-half
of Crc,p. Crc,p is only 21% of Crc,p, and Crc,a is
effectively zero. This indicates that compartmental compliance
decreases greatly if the rib cage is distorted; in fact,
Crc = Crc,p + Crc,a is 10% of Crc = Crc,p + Crc,a.
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Figure 8 shows restoring pressures (Plink) plotted against the rib cage distortions producing them during phrenic stimulation for the five subjects. The relation was generally nonlinear, with greater restoring pressure with increasing distortion in three subjects, slightly decreasing in one subject, and constant in another subject. Restoring pressures of up to 15 cmH2O were developed with distortions of up to 2.5%.
Figure 9 shows rib cage restoring pressures plotted against Pdi for the five subjects during phrenic stimulation. This describes how the pressure generating the distortion is transduced via distortion into a restoring pressure. The relation was linear in all cases, with mean slope of 0.40 ± 0.055 (SD) for the different subjects. This is as expected, inasmuch as most of the
Pes during a
twitch is due to Plink; the change
in Prc,p was small in comparison. Thus Plink 
Pes, Pdi = Pga Pes, and Pes/Pdi 0.5, so we expected Plink/Pdi 0.5, as
shown in Fig. 9.
Figure 10 shows the average time course of the raw data, i.e., the signals that were directly observed (Pes, Pga, Pdi, Vrc,p, Vrc,a, and Vab), for all the subjects during quiet breathing and exercise.
Important points that we will elaborate here and later (3) are as follows: 1) end-expiratory rib cage volume did not change, whereas end-inspiratory rib cage volume progressively increased from quiet breathing to exercise at 70%
max; 2)
end-inspiratory abdominal displacement changed little, whereas
end-expiratory abdominal displacement progressively diminished from
quiet breathing to exercise at 70% max;
3) Pga rose throughout inspiration
during quiet breathing, but during most of inspiration during exercise, even at 0% max, it fell, tending to parallel the
fall in Pes; 4) the slope
Pdi/TI (where
TI is inspiratory time) was
steeper during quiet breathing than during all levels of exercise
during most of inspiration; 5) at
all levels of exercise, Pdi was finite at the onset of inspiration
(probably because of passive stretching), and this increased
progressively with max. Thus, although active Pdi at
end inspiration increased from ~10
cmH20 during quiet breathing to
~20 cmH20 at 70%
max, Pdi during inspiration was lower during exercise than during quiet breathing, except at 70%
max.
During exercise a pattern of distortion different from that in phrenic
stimulation was observed. Figure 11 shows
data plotting Vrc,p vs. Vrc,a during quiet breathing and at each
exercise level for the average breath. The dotted lines are at
iso-Plink values of ±2.5,
±5, and ±10 cmH2O and are
parallel to the relaxation line for each subject. These data illustrate
that in all subjects the rib cage always moved parallel to its
relaxation line with different levels of exercise, and there was very
little distortion. On average, distortion was constant throughout the
respiratory cycle at any level of exercise. However, the Vrc,p vs.
Vrc,a trace tended to form a loop, which appeared to increase in width
as exercise level increased. Consequently, we measured mean rib cage distortion as the parallel shift of the trace and range of distortion as the width of the loop as a way of quantifying the change in distortion during a breath. These data are shown in detail in Table
4. Mean distortion and
Plink were less during quiet
breathing than during exercise. Mean rib cage distortion remained
<0.5%, with no consistent individual changes. Mean
Plink during exercise remained
nearly constant at an average value of 2.0
cmH2O, with no consistent change
with exercise level. Range of distortion over a breath increased
linearly from 0.36% at quiet breathing to 1.00% at 70%
max. The corresponding range of
Plink over a breath increased
linearly from 1.34 to 3.99 cmH2O.
As a percentage of the pressure generated by the inspiratory rib cage
muscles at end inspiration, this was 20 ± 3.9% (SE) during quiet
breathing and 13 ± 4.1% (SE) at 70% max. The
maximum contribution of Plink was
at 0% max, when it was 27 ± 6.5% (SE) of the
peak values of the pressures developed by the nondiaphragmatic
inspiratory muscles.
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Vrc,a/Pab was
greater during quiet breathing than during relaxation, as would be
expected if Pab and the insertional component of Pdi
(xPdi) were the only agencies acting
on RCa during quiet breathing. Evidently, one or more additional
agencies diminish the combined effect of Pab and
xPdi on RCa.
DISCUSSION
Using a two-compartment model to describe the rib cage (31) and
calculating compartmental volumes from surface markers (5, 13), we have
found that the human rib cage distorts very little in exercise up to
70% max, averaging about 0.3% (Table 4), leading to restoring pressures of ~17% of those generated by the nondiaphragmatic inspiratory muscles at the highest level of exercise. During respiration the range of distortions increased linearly with
exercise level from 0.36 to 1.00%, but the resulting restoring pressure expressed as a percentage of the pressure generated by the rib
cage muscles remained roughly constant: 20% during quiet breathing and
13% at 70% max. In comparison, distortions during phrenic stimulation, with Pdi of up to 30 cmH2O, were substantial (Fig. 7)
and resulted in restoring pressures of >10
cmH2O in four of five subjects.
The slope of the volume-pressure relaxation line is the compliance of
RCp or Crc,p (Fig. 6). During phrenic stimulation, this slope
Crc,p was only 21% of Crc,p, and Crc,a was effectively
zero. The mechanical linkage between RCp and RCa markedly stiffens the
whole rib cage when it is distorted. Indeed, we found that rib cage
compliance during phrenic stimulation was only 10% of that during
relaxation, confirming the work of Chihara et al. (9). Although this
enhances the inspiratory function of the diaphragm, defined as the
fraction of Pdi that is converted to a fall of Ppl (9), it means that a
substantial fraction of respiratory muscle force may be used to distort
the rib cage rather than to change the volume of the respiratory
system.
max
and only doubled from quiet breathing to exercise at 70%
max. Prcm, in contrast, increased on average
4.5fold from quiet breathing to 70% max (see
Ref. 5 for details on rib cage and abdominal muscle contribution).
During exercise, tidal volume increases (15, 29), diaphragm excursion
increases (15, 16, 30), and the upper boundary of the diaphragm-apposed
rib cage may descend (22, 25). Thus the boundary between RCp and RCa is
continuously changing. This clearly affects the dynamics of the lower
rib cage, the boundary of which in the present model was fixed. It has
smaller effects on the upper rib cage, because even at very low
VL the zone of apposition does
not extend far above the xiphisternum (22). In this presentation we
ignore these sources of error. Fortuitously, we found that rib cage
distortions were small and varied little throughout a breath. The
sources of error do not affect this observation, which must mean that
the net pressures acting on both rib cage compartments were not very
different. This would act to minimize the errors. Furthermore, to the
extent that abdominal displacement is the principal determinant of the
upper boundary of the area of apposition, the similarity of this
displacement at end inspiration during quiet breathing and at all
levels of exercise suggests that its caudal excursion during
inspiration was not greatly affected by exercise. We believe that the
error introduced by a changing boundary of the upper limit of the area
of apposition on the dynamics of RCa and RCp is small and that it can
be ignored.
The model used here does not deal with intracompartmental distortions
but only distortions between compartments. A surprising finding of this
study is that volume distortion of the rib cage is very small in
exercise; this contrasts with previous investigations in normal adults,
in which significant cross-sectional shape or area changes have been
found during voluntarily and involuntarily increased ventilation (1,
11, 22, 27, 28). Rib cage distortion in exercise has not been
previously studied, although it has been shown that the rib cage is not
on its volume-pressure relaxation characteristic (14-16). It is
not obvious how to incorporate intracompartmental distortion into the
present analysis, and available work on more detailed models of the rib
cage is generally incomplete in terms of incorporating all the relevant
muscular anatomy (e.g., omission of the diaphragm) and the mechanical
properties of component tissues (bones, muscles, and connective tissue)
(10, 17). Incorporating these variables leads to considerable
complexity in producing a truly rigorous analysis. By employing
simplifying assumptions, we are able to estimate rib cage
distortability, restoring forces, and the Prcm instantaneously during
inspiration and expiration. This has not been possible previously.
Critique of methods.
Surface markers were used for compartmental volume calculation. This is
inevitably imprecise, in that there can be movement of skin relative to
the underlying bone structure during increased ventilation. We
carefully observed marker movements relative to anatomic features and
found a maximum of ±1.5 cm of marker displacement relative to the
lower costal margin in the anterior auxiliary lines in our subjects.
Movement at other points on the intercompartmental boundaries was much
less and became negligible at the bottom of the sternum, lateral
margins, and posteriorly. This could lead to errors in compartmental
volume changes of RCa vis-à-vis the abdomen. The errors relative
to the absolute volume of the compartments (~4 liters for RCa and
~12 liters for the abdomen) were <10% for Vrc,a and <2.5% for
Vab. We neglected these errors.
Data were gathered after 3 min at each level of exercise, a time
sufficient for normal subjects to reach a steady state (8). However,
the subjects' posture with arms supported away from the body was not
that normally used during cycling. We do not know whether this altered
rib cage elastic properties, and strictly speaking our results apply
only to the type of exercise performed in this study. We did not
observe entrainment of respiratory rate to cycling rate in this study;
when this occurs, as in swimming, results might be different. Finally,
although changes in blood flow, autonomic activity, and so forth during
exercise might conceivably have altered relaxation configurations, we,
like others (14, 16, 21, 27, 28), made no attempt to control these
variables.
Rib cage compliance and distortion.
We found that, during relaxation, Crc,p was approximately twice Crc,a:
0.112 and 0.059 l/cmH2O,
respectively. This is probably accounted for by the larger volume of
Crc,p. However, during bilateral phrenic twitch, Crc,p declined
to 21% of its previous value and Crc,a was effectively zero,
confirming the findings of Chihara et al. (9), who used cross-sectional
areas to represent volume changes. Thus the compliance of the rib cage
during distortion is reduced to 10% of its undistorted value, at least
in normal subjects. This implies that when the action is inflationary
on one part of the rib cage and deflationary on the other part, the net
effect will generate only 10% of the volume change that would occur if
the agencies acting on the rib cage were properly coordinated to move
it along its relaxation configuration. This provides an excellent
teleological reason for the small amount of distortion we found during
exercise; as a result, restoring pressures were usually small relative
to inspiratory rib cage muscle pressure generation.
Implications of lack of rib cage distortion in exercise.
The small amount of observed distortion during exercise requires that
the muscles acting on the upper and lower rib cages be precisely
coordinated throughout each breath to avoid a pressure difference that
would cause distortion. From the pressure balance equations on RCp and
RCa derived from the model shown in Fig. 1, we can write the condition
for no rib cage distortion
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(5) |
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Vrc,a/Pab was greater
during quiet breathing than during relaxation. This difference could be
due to the fact that our subjects were seated on a cycle ergometer and
so had a different posture. It is likely, however, that we estimated smaller distortions because we measured volume distortion, whereas Ward
et al. measured shape distortion. The latter appears to be greater than
volume distortion, and this may have exaggerated the estimate of
Plink reported by Ward et al., who
assumed that the shape distortion that they measured reflected volume
distortion. Under the circumstances, deducing volume from a single
dimension would lead to a systematic overestimation of Vrc,a,
explaining their finding of an increased Vrc,a/Pab during quiet
breathing. In the present analysis we measured the pressures producing
volume distortions (Pdi) and the restoring pressures
(Plink). The pressures producing
shape distortion within RCp and RCa and their resulting restoring
forces are unknown.
Distortion of the rib cage/abdomen relative to their relaxation
configuration has been analyzed by Goldman, Grimby, and Mead (14, 16),
who showed that these deformations were substantial. However, the
pressure cost of rib cage/abdomen deformation is sufficiently small
that it can be neglected (4).
To conclude, this investigation demonstrates that the diaphragm, rib
cage, and abdominal muscles are coordinated during exercise so that rib
cage distortions, although measurable, are minimized. The pressure cost
of these distortions is only a small percentage of the pressures
applied to RCp during exercise. The net pressure acting on the two rib
cage compartments must therefore be closely similar. Inasmuch as the
abdominal rib cage is exposed to a large positive Pab at end expiration
in exercise, this must be counterbalanced by a strong expiratory action
resulting from active contraction of expiratory muscles. We believe
that the insertional component of abdominal muscles is a major
contributor to this expiratory action and thus plays a key role in
minimizing rib cage distortion. This minimization prevents a marked
reduction in rib cage compliance, which would substantially increase
elastic work of breathing. Finally, we believe that passive stretching
of abdominal muscle is important in preventing rib cage distortion
during quiet breathing. In doing so, it plays a previously unrecognized
role in displacing the dynamic Pab-rib cage volume curve to the right
of the relaxation line, which more than compensates for the combined
inflationary action of the Pab insertional component of Pdi.
ACKNOWLEDGEMENTS
This work was supported by the Medical Research Council of Canada, Respiratory Health Network of Centre of Excellence, Montréal Chest Institute, Allen and Hanburys Thoracic Society of Australia and New Zealand Fellowship, J. T. Costello Memorial Research Fund, and Fondazione Pro Juventute, Italy, Telethon Italy.
FOOTNOTES
Address for reprint requests: P. T. Macklem, Montréal Chest Institute, 3650 St. Urbain, Montreal, Quebec, Canada H2X 2P4.
Received 24 July 1996; accepted in final form 17 April 1997.
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