Vol. 87, Issue 2, 561-566, August 1999
Ratio of active to passive muscle shortening in the canine
diaphragm
Aladin M.
Boriek1,
Joseph R.
Rodarte1, and
Theodore A.
Wilson2
1 Baylor College of Medicine,
Houston, Texas 77030; and
2 Department of Aerospace
Engineering and Mechanics, University of Minnesota, Minneapolis,
Minnesota 55455
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ABSTRACT |
Active and passive
shortening of muscle bundles in the canine diaphragm were measured with
the objective of testing a consequence of the minimal-work hypothesis:
namely, that the ratio of active to passive shortening is the same for
all active muscles. Lengths of six muscle bundles in the costal
diaphragm and two muscle bundles in the crural diaphragm of each of
four bred-for-research beagle dogs were measured by the radiopaque
marker technique during the following maneuvers: a passive deflation
maneuver from total lung capacity to functional residual capacity,
quiet breathing, and forceful inspiratory efforts against an occluded
airway at different lung volumes. Shortening per liter increase in lung
volume was, on average, 70% greater during quiet breathing than during
passive inflation in the prone posture and 40% greater in the supine
posture. For the prone posture, the ratio of active to passive
shortening was larger in the ventral and midcostal diaphragm
than at the dorsal end of the costal diaphragm. For both postures,
active shortening during quiet breathing was poorly
correlated with passive shortening. However, shortening during forceful
inspiratory efforts was highly correlated with passive shortening. The
average ratios of active to passive shortening were 1.23 ± 0.02 and
1.32 ± 0.03 for the prone and supine postures, respectively. These
data, taken together with the data reported in the companion paper (T. A. Wilson, M. Angelillo, A. Legrand, and A. De Troyer,
J. Appl. Physiol. 87: 554-560, 1999), support the hypothesis that, during forceful inspiratory efforts, the inspiratory muscles drive the chest wall along
the minimal-work trajectory.
respiratory muscles; mechanics; chest wall; work of breathing
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INTRODUCTION |
ONE LONG-STANDING HYPOTHESIS about respiratory muscle
activation is that inspiratory muscle activity is coordinated to drive the chest wall along the trajectory for minimal work. In the
accompanying paper (8), a theory of chest wall mechanics is presented,
and the minimal-work trajectory is shown to have the property that the
ratio of active to passive shortening is the same for all active
muscles. In that paper, data are also reported on the ratio of active
to passive shortening of the parasternal intercostal muscles of supine
anesthetized dogs. Here, we report data on active and passive muscle
shortening in the canine diaphragm, and we use these data as a further
test of the minimal-work hypothesis.
Active and passive shortening of the canine diaphragm have been
measured before (1, 3-6), but the data reported here are the most
comprehensive data on diaphragm muscle shortening reported to date. A
total of 30-32 markers was attached along eight muscle bundles (6 in the costal muscle and 2 in the crural muscle) of the left
hemidiaphragms of each of four dogs. Muscle lengths were determined
during passive deflation, during quiet breathing, and during forceful
inspiratory efforts against an occluded airway at different lung
volumes. Muscle shortening per unit change in lung volume
(VL) for the active maneuvers,
quiet breathing, and forceful inspiratory efforts was compared with
passive shortening. Active shortening during quiet breathing was found
to be poorly correlated with passive shortening, but active shortening
during forceful inspiratory effort was highly correlated with passive shortening. These results for the diaphragm are much like those for the
parasternal intercostals. Both show that, during quiet breathing in
anesthetized dogs, muscle coordination does not match that for minimal
work but that, during forceful inspiratory efforts, muscle activation
is distributed so as to drive the chest wall along the minimal-work trajectory.
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METHODS |
Experimental methods.
The experimental methods have been described previously (1, 4, 5, 9).
The animals are the same as those used in our study of passive
diaphragm muscle shortening (9). In a preparatory surgical procedure,
silicon-coated lead spheres and cylinders were stitched to the
peritoneal surfaces of the left hemidiaphragms of four
bred-for-research beagle dogs. In each dog, three or four markers were
placed at intervals of ~1 cm along each of six muscle bundles
situated at approximately equal intervals around the circumference of
the costal diaphragm. Three or four markers were placed along each of
two muscle bundles of the crural diaphragm: one near the midplane, and
one about halfway between the midplane and the junction of the crural
and costal muscles. A typical example of marker placement is shown in
Fig. 1. The animals were allowed to recover
for at least 3 wk.
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Fig. 1.
Planar view of diaphragm, showing marker placement along 6 muscle
bundles of costal diaphragm and 2 muscle bundles of crural
diaphragm.
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The animals were anesthetized with pentobarbital sodium, intubated with
a cuffed endotracheal tube, placed in the prone or supine position in a
radiolucent body plethysmograph situated in the test field of an
orthogonal biplane fluoroscopy system, and mechanically ventilated. The
dog was switched from the ventilator to a supersyringe, and the lungs
were manually inflated to total lung capacity (TLC), defined as volume
at an airway pressure of 30 cmH2O.
Biplanar fluoroscopic images were taken at TLC and at three equally
spaced volumes down to functional residual capacity (FRC). After the
animal resumed steady quiet breathing, images were taken at end
inspiration and end expiration. After another period of mechanical
ventilation, the airway was occluded at FRC. Three images were taken
during the fourth to sixth sustained inspiratory effort against the
occluded airway. Then the lungs were inflated to either TLC or halfway
to TLC, the airway was occluded, and three images were obtained during
inspiratory efforts at each of those
VL values. Then the animal was
rotated to the other posture, and the procedure was repeated.
The coordinates of the markers in the two orthogonal images were
determined, and the three-dimensional coordinates of the markers were
calculated from their coordinates in the two orthogonal images. The
values from the three images obtained during inspiratory efforts at
each of the three VL values were
averaged. The lengths of the muscle bundles were computed by adding the
distances between adjacent markers along each bundle.
Data analysis.
As we noted in our previous paper (9), passive shortening per liter
increase in VL was about the
same for the two volume steps above FRC but was smaller for the highest
volume step. Because we wish to describe linear relations between
muscle length and VL, the data
for muscle length at TLC, both passive and active, were not included in
the analysis.
A straight line was fit to the plots of passive muscle length vs.
VL. The value of muscle length
at FRC (LFRC)
was obtained from the intercept of the linear fit, and the slope of the
line was divided by
LFRC to obtain
the fractional change in muscle length per liter increase in
VL. The difference between
muscle lengths at end expiration and end inspiration was divided by
length at end expiration and tidal volume to obtain values of
fractional change in length (
L)
per unit volume change during quiet breathing. Finally, values of
L per unit volume change were
obtained from the data for inspiratory efforts against an occluded
airway by the following analysis. L
was assumed to be linearly related to
VL and airway opening pressure
(Pao) by the following equation, where Crs denotes the compliance of
the respiratory system
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(1)
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During
passive inflation, VL = Crs Pao, and the second term in Eq. 1 is zero. Thus coefficient
a describes fractional shortening per
liter during passive inflation. During active breathing, Pao = 0; thus,
coefficient b describes active
fractional shortening. The value of a
determined from the passive data and the values of
L, Pao, and
VL during inspiratory efforts
against an occluded airway were substituted into Eq. 1 to obtain b. The
values of b for inspiratory efforts at
FRC and FRC + 1/2 inspiratory capacity (IC) were averaged to obtain an
average value for each muscle bundle.
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RESULTS |
The values of body mass, IC, and Crs over the lower two-thirds of the
IC for the four dogs are listed in Table 1.
Values of Pao during inspiratory efforts are also shown. The values for mass, IC, and Crs are quite uniform for these bred-for-research beagles. The values of Pao are more variable among dogs and volumes, but there is no systematic dependence of Pao on VL, and the
mean values of Pao at different volumes are not significantly
different.
Values of passive L per liter
increase in VL are shown in Fig.
2. For each muscle bundle, average values
and SDs for the four dogs are shown by the bars and lines,
respectively. Two values of active
L per liter are shown in Fig. 2:
one was obtained from the data for quiet breathing, and one was from
the data for forceful inspiratory efforts. Values of active shortening
for all individual muscle bundles in the four dogs for quiet breathing
are shown plotted vs. values of passive shortening in Fig.
3, and values of active shortening for
forceful inspiratory efforts are shown plotted against values of
passive shortening in Fig. 4.
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Fig. 2.
Means and SD (bars) of length change per liter increase in lung volume
for the eight muscle bundles for passive lung inflation (open bars),
quiet breathing (shaded bars), and forceful inspiratory efforts (solid
bars) in prone (A) and supine
(B) postures. Nos. (costal
1-6 and crural
1 and
2) refer to rows of markers in Fig.
1.
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Fig. 3.
Change in muscle length per liter increase in lung volume during quiet
breathing vs. change in length during passive inflation for all
individual muscles in 4 dogs in prone
(A) and supine
(B) postures. A total of 32 points
are shown in each panel, 8 for each of 4 dogs. Solid line, linear fit
to the data; dashed line, line of identity. On average, active
shortening is 70 ± 20% greater than passive shortening in prone
posture and 40 ± 10% greater in supine posture, but the
correlation between active and passive shortening is weak.
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Fig. 4.
Change in muscle length per liter increase in lung volume inferred from
data for forceful inspiratory efforts against an occluded airway vs.
change in length during passive inflation. Active shortening for
forceful inspiratory efforts is highly correlated with passive
shortening. Active shortening is 23 ± 2% greater than passive
shortening in the prone posture (A)
and 32 ± 3% greater in the supine posture
(B). Symbols are same as in Fig.
3.
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DISCUSSION |
With the radiopaque-marker technique, material points on the diaphragm
can be identified and tracked as the diaphragm contracts. Thus
individual muscle fibers can be followed as they move and shorten. The
number of markers used in this study is larger than in previous
studies, and lengths of eight muscle bundles approximately equally
spaced around the circumference of one hemidiaphragm were tracked.
Passive muscle shortening and active muscle shortening during two
inspiratory maneuvers (quiet breathing and forceful inspiratory efforts
against an occluded airway) were measured. The data on passive
shortening have been reported earlier (9). Here we focus on the
magnitude and distribution of active shortening and on the relationship
between active and passive shortening.
Active shortening.
The data for active shortening can be compared with more limited data
in the literature. Boriek et al. (1) measured strains in the midcostal
canine diaphragm during quiet breathing and mechanical ventilation in
prone and supine dogs, and Pean et al. (3) measured strains in this
region during quiet breathing and during inspiratory efforts against an
occluded airway in supine dogs. Tidal volumes in our experiments
averaged ~170 ml. For the values of length change per liter shown in
Fig. 2 and this tidal volume, bundles 2 and 3 would
shorten by 17 and 10% during quiet breathing in the prone and supine
postures, respectively. The value for the prone posture agrees well
with the value reported by Boriek et al. for the prone posture, but the
value for the supine posture is somewhat lower than those reported by
both Boriek et al. and Pean et al. Active shortening during quiet
breathing is nonuniform around the circumference of the
diaphragm in both the prone and supine postures. Shortening is much
greater in the ventral than in the dorsal costal diaphragm. Wakai et
al. (6) used sonomicrometry to measure the change in length of segments
of muscles distributed around the diaphragm and obtained a similar
topographic distribution of muscle shortening during quiet breathing
and during more forceful breathing.
Ratio of active to passive shortening.
First, the ratio of active shortening for quiet breathing to passive
shortening will be discussed. The average ratio of active to passive shortening (1.7 ± 0.2 in the prone posture and 1.4 ± 0.1 in the supine posture) is relatively large. For the prone posture,
the ratio of average active to passive shortening systematically changes from a value of ~2 for the muscle bundles of the ventral and
midcostal diaphragm to a value of ~1 for the muscle bundles at the
dorsal end of the costal diaphragm. The correlation between active and
passive shortening of individual muscle bundles in the prone position,
shown in Fig. 3, is very weak. For the supine posture, no topographic
distribution of the ratio of active to passive shortening is apparent
in the data shown in Fig. 2, and the correlation between active and
passive shortening shown in Fig. 3 is stronger than for the supine
posture, but it is still weak.
During forceful efforts, the average ratio of active to passive
shortening is somewhat smaller (1.23 ± 0.02 and 1.32 ± 0.03 in
the prone and supine postures, respectively). The topographic distribution of active shortening during more forceful inspiratory efforts shown in Fig. 2 is similar to the distribution of passive shortening for both the prone and supine postures. More striking is the
correlation between active and passive shortening for individual muscle
bundles (Fig. 4). The ratio of active to passive shortening is nearly
the same for all muscle bundles in each dog and nearly the same for all dogs.
Work of breathing.
In the companion paper (8), the chest wall is modeled as a linear
elastic system, and the distribution of muscle forces for which the
work of chest wall expansion is minimal is computed. For the
minimal-work distribution, the ratio of active to passive muscle
shortening is the same for all muscles. If the muscles can drive the
chest wall along the relaxation trajectory, the ratio is 1.0. If not,
the ratio of active to passive shortening is >1.0. The ratio of the
work of active chest wall expansion to the work of passive chest wall
expansion equals the ratio of active to passive muscle shortening.
These theoretical results provide a means to test the long-standing
hypothesis that the respiratory muscles are coordinated so as to expand
the chest wall with minimal work.
The data for active diaphragm muscle shortening during quiet breathing
in anesthetized dogs show that active shortening is only weakly
correlated with passive shortening. The parasternal intercostal muscles
show a similar weak correlation between active shortening during quiet
breathing and passive shortening (8). This implies that, during quiet
breathing, the distribution of inspiratory muscle activation does not
closely match the distribution for minimal work. Perhaps other
metabolic costs (such as a fixed cost of muscle activation or a
metabolic cost that depends on variables such as active stress), rather
than work alone, are relatively more important during quiet breathing
when the work of breathing is small.
On the other hand, during forceful inspiratory efforts, the correlation
between active shortening and passive shortening is remarkable. The
fact that this correlation does not hold for quiet breathing shows that
it is not the result of an intrinsic cohesiveness of diaphragm
behavior; it must be caused by a particular distribution of muscle
activation. Thus these data support the hypothesis that, during
forceful inspiratory efforts, the distribution of muscle activation
within the diaphragm drives the diaphragm along its minimal-work
trajectory. The parasternal intercostals show a similar, if less
striking, greater correlation for forceful efforts (8). Perhaps most
significant is the agreement between the magnitudes of the ratios of
active to passive shortening for the diaphragm and parasternals for the
supine posture (1.32 ± 0.03 and 1.4 ± 0.1, respectively). This
supports the more general hypothesis that the muscles of the chest wall
are coordinated to drive the chest wall along the minimal-work
trajectory. This common ratio provides a consistent estimate for the
ratio of the minimal work of active breathing to the work of passive
inflation; the minimal work of active breathing is ~35% greater than
the work of passive inflation.
Distortion of the chest wall could be classified into two types. The
first is the result of the difference between the sign of the change of
pleural pressure during passive and active lung inflation and the
consequent difference in the change in blood volume in the thorax.
Warner et al. (7) measured a 30-ml increase in liquid volume in the
thorax during spontaneous breathing and a 9-ml decrease in liquid
volume during mechanical ventilation with the same tidal volume of 200 ml. For the same change in gas volume in the lung, they
observed a 25% greater change in thoracic volume during spontaneous
breathing than during passive inflation. If the chest wall followed the
same trajectory for the two maneuvers, linear displacements would be
~8% greater during spontaneous breathing, and muscle shortening
would be uniformly ~8% greater.
The second type of distortion is a distortion of the configuration of
the chest wall with no change in enclosed volume. It seems likely that
there are many differences in detail between the configuration of the
chest wall during active and passive inflation. A prominent and
well-documented example is the difference between the directions of the
displacement of the sternum in the dog (2). During active breathing,
the sternum moves caudally, but during passive inflation, it moves
cranially. It would seem that the caudal displacement of the sternum
would augment muscle shortening locally and that the ratio of active to
passive shortening would be higher for the parasternals than for the
diaphragm. However, for the minimal-work trajectory, the ratio of
active to passive shortening is the same for all active muscles. The
distribution of muscle activation for minimal work must compensate for
the local distortion (by shifting some volume expansion from the rib cage to the abdomen, for example) so that the ratio of active to
passive shortening is the same for both the parasternals and the
muscles of the diaphragm. In fact, Warner et al. (7)
observed that the ratio of the volume displaced by the
diaphragm to the volume displaced by the rib cage is greater during
spontaneous breathing than during passive inflation.
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ACKNOWLEDGEMENTS |
This work was supported by National Heart, Lung, and Blood
Institute Grant HL-46230.
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FOOTNOTES |
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: T. A. Wilson,
107 Akerman Hall, 110 Union St. SE, Minneapolis, MN 55455 (E-mail:
wilson{at}aem.umn.edu).
Received 29 July 1998; accepted in final form 12 April 1999.
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REFERENCES |
1.
Boriek, A. M.,
T. A. Wilson,
and
J. R. Rodarte.
Displacements and strains in the costal diaphragm of the dog.
J. Appl. Physiol.
76:
223-229,
1994[Abstract/Free Full Text].
2.
De Troyer, A.,
and
S. Kelly.
Chest wall mechanics in dogs with acute diaphragm paralysis.
J. Appl. Physiol.
53:
373-379,
1982[Abstract/Free Full Text].
3.
Pean, J. L.,
C. J. Chuong,
and
R. L. Johnson, Jr.
Regional deformation of the canine diaphragm.
J. Appl. Physiol.
71:
1581-1588,
1991[Abstract/Free Full Text].
4.
Sprung, J.,
C. Deschamps,
R. D. Hubmayr,
B. J. Walters,
and
J. R. Rodarte.
In vivo regional diaphragm function in dogs.
J. Appl. Physiol.
67:
655-662,
1989[Abstract/Free Full Text].
5.
Sprung, J.,
C. Deschamps,
S. S. Margulies,
R. D. Hubmayr,
and
J. R. Rodarte.
Effect of body position on regional diaphragm function in dogs.
J. Appl. Physiol.
69:
2296-2302,
1990[Abstract/Free Full Text].
6.
Wakai, Y.,
A. M. Leevers,
and
J. D. Road.
Regional diaphragm shortening measured by sonomicrometry.
J. Appl. Physiol.
77:
2791-2796,
1994[Abstract/Free Full Text].
7.
Warner, D. O.,
S. Krayer,
K. Rehder,
and
E. L. Ritman.
Chest wall motion during spontaneous breathing and mechanical ventilation in dogs.
J. Appl. Physiol.
66:
1179-1189,
1989[Abstract/Free Full Text].
8.
Wilson, T. A.,
M. Angelillo,
A. Legrand,
and
A. De Troyer.
Muscle kinematics for minimal work of breathing.
J. Appl. Physiol.
87:
554-560,
1999[Abstract/Free Full Text].
9.
Wilson, T. A.,
A. M. Boriek,
and
J. R. Rodarte.
Mechanical advantage of the canine diaphragm.
J. Appl. Physiol.
85:
2284-2290,
1998[Abstract/Free Full Text].
J APPL PHYSIOL 87(2):561-566
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ABSTRACT
INTRODUCTION
