Download Diminished stroke volume during inspiration

LABORATORY INVESTIGATION
VENTRICULAR PERFORMANCE
Diminished stroke volume during inspiration:
a reverse thoracic pump
CRAIG 0. OLSEN, M.D., GEORGE S. TYSON, M.D., GEORGE W. MAIER, M.D.,
JAMES W. DAVIS, M.S., AND J. ScoTT RANKIN, M.D.
ABSTRACT In 12 conscious dogs, a three-dimensional array of pulse-transit ultrasonic transducers
used to measure left ventricular anterior-posterior minor, septal-free wall minor, and basal-apical
major diameters. Matched micromanometers measured left ventricular, right ventricular, and intrapleural pressures. Electromagnetic ascending aortic blood flow and right ventricular transverse diameter were measured in five of the dogs. A major cause of the inspiratory decline in stroke volume in this
preparation appeared to be reflex tachycardia and autonomic changes associated with inspiration.
However, when heart rate was controlled by atrial pacing or pharmacologic autonomic attenuation
(propranolol and atropine), stroke volume still decreased around 10%, with an inspiratory decrease in
pleural pressure of 10 mm Hg. Based on the measurements of ventricular dimension, venous return to
the right ventricle appeared to be augmented significantly during inspiration and the transient increase
in right ventricular volume was associated with leftward interventricular septal shifting and altered
diastolic left ventricular geometry. However, left ventricular end-diastolic volume was changed minimally, implying that alterations in preload were not important. Moreover, transmural left ventricular
ejection pressure, calculated as intracavitary minus pleural pressure, was not significantly changed,
and it seemed that neither pressure nor geometric components of afterload were altered significantly by
inspiration. The inspiratory fall in left ventricular stroke volume correlated best with the decline in
intracavitary left ventricular ejection pressure referenced to atmospheric pressure. It is hypothesized
that during ejection, left ventricular pressure referenced to atmospheric pressure is the hydraulic force
effecting stroke volume and that the decline in this effective left ventricular ejection pressure is
responsible for the inspiratory fall in stroke volume through a reverse thoracic pump mechanism.
Circulation 72, No. 3, 668-679, 1985.
was
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THE EFFECTS of respiratory movement on cardiovascular function are numerous and have been the subject of several extensive monographs.' Systematic
investigation into these effects dates back to 1751
when Albrecht von Haller noted an inspiratory augmentation in venous return to the right ventricle of the
dog and cat.3 Eighteen years earlier Stephen Hales
reported his famous series of experiments in the horse
and may have been the first to record the inspiratory
fall in arterial blood pressure.4 Although Hales did not
make the association between inspiration and the periodic fall in the oscillatory pulse pressure of the carotid
artery, numerous subsequent investigators have conFrom the Departments of Surgery and Physiology, Duke University
Medical Center, Durham.
This work was supported by NIH grants 2R01 H 109315-17 and RO I
H129436-01, and by research grants from the Whitaker Foundation and
the North Carolina Heart Association.
Address for correspondence: Craig 0. Olsen, M.D., Box 3492, Duke
University Medical Center, Durham, NC 27710.
Received April 26, 1985; revision accepted June 20, 1985.
Dr. Rankin is a recipient of the John A. Hartford Foundation Fellowship.
668
firmed this phenomenon and have documented an inspiratory decline in left ventricular stroke volume in
both experimental animals5-" and man.'2-14
Several hypotheses have been advanced to explain
the inspiratory fall in left ventricular stroke volume,
including (1) delayed pulmonary venous transit
time,7 15. 16 (2) increased pulmonary venous capacitance and diminished left ventricular filling,'7 (3) reduction in left ventricular preload due to leftward interventricular septal shifting,'81' (4) increased left
ventricular afterload from altered geometry due to
leftward interventricular septal shifting,8 and (5) increased inspiratory left ventricular transmural pressure, which augments afterload.6 20 The present studies were undertaken to investigate the relative
importance of these phenomena during spontaneous
respiration in a conscious canine preparation.
Methods
Instrumentation and acquisition of data. Twelve healthy
adult mongrel dogs (20 to 32 kg) underwent surgical preparation
CIRCULATION
LABORATORY INVESTIGATION-VENTRICULAR PERFORMANCE
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for subsequent studies in the conscious state. The method of
implantation of instrumentation has been described previously.21 Briefly, in all dogs an array of pulse-transit ultrasonic
dimension transducers was used to measure three orthogonal
left ventricular dimensions: the anterior-posterior minor, septal-free wall minor, and basal-apical major diameters. All transducers, except the one in the septal position, which was positioned near the right ventricular subendocardial surface, were
placed epicardially. Silicone rubber introducers were implanted
in the right ventricle, left atrium, and intrapleural space of each
dog, as were bipolar atrial pacing electrodes. In five dogs, right
ventricular septal-free wall transverse diameter and electromagnetic ascending aortic blood flow were measured as well (figure
1 top left).
Seven to 14 days after recovery from the implantation procedure, each dog was studied in the conscious state while resting quietly on its right side. The dimension transducers were
coupled directly to a custom-designed sonomicrometer.21
Prewarmed matched micromanometers (PC-350, Millar Instruments, Houston) were passed via the introducers into the mid
left and right ventricles and pleural space. Airtight introducer
connectors prevented ventricular hemorrhage and pneumothorax. The aortic flow probes were coupled to a sine-wave
flowmeter (Statham, M4001, Los Angeles). The performance
characteristics of these instruments have been described
previously.22 25
Cardiac dimensions, pressures, and aortic blood flow were
recorded on magnetic tape for subsequent digital analysis. Data
were recorded in each experiment during normal spontaneous
respiration and deep spontaneous respiration against inspiratory
inflow resistance through a gauze sponge. Heart rate was controlled by atrial pacing at 10 min- l higher than the fastest heart
rate observed during the respiratory cycle. In six dogs, after
completion of initial studies, the autonomic nervous system was
pharmacologically attenuated with intravenous propranolol (1
mg kg- 1) and atropine (2 mg). Data were collected again during
normal and deep spontaneous respirations.
At the conclusion of all studies, the animals were killed, their
hearts were excised, and the volume of the left ventricular
muscle mass was calculated as the average of three volume
displacements of water in a graduated cylinder.
Data analysis. The recorded analog data were filtered once at
50 Hz and digitized at 200 Hz for analysis. Left ventricular
transmural pressure was calculated as left ventricular intracavitary pressure minus simultaneous intrapleural pressure. Right
ventricular transmural pressure was determined similarly, and
interventricular transseptal pressure was computed as left ventricular intracavitary pressure minus right ventricular intracavitary pressure. The first derivative of left ventricular transmural
pressure (dP/dt) was calculated from the digitized ventricular
pressure waveform with use of a five-point polyorthogonal approximation.25
FIGURE 1. Top left, Preparation used to assess the
three-dimensional geometry of the left ventricle. The
F b
/|
anterior-posterior minor (A to P), septal-free wall
minor (S to F), and basal-apical (Ba to Ap) major
diameters were measured in the conscious dog and fit
to a double hemiellipsoidal model. Biventricular and
pleural pressures were measured with micromano-
meters passed through implanted silicone rubber
tubes. In five preparations right ventricular transverse diameters (S to R) and ascending aortic blood
flow were measured as well. Top right, Model of left
ventricular latitudinal plane geometry of the left ventricular double hemiellipsoidal model to which dimensions were fitted. A, S, P, and F correspond,
respectively, to the placement positions of the anterior, septal, posterior, and lateral free wall dimension
transducers. b = external anterior-posterior minor
diameter; c = septal-free wall minor diameter; Rs
= left ventricular septal radius of curvature in the
latitudinal plane. Bottom, Postmortem transverse
section of myocardium from one dog demonstrating
the actual position of the four epicardial and one
endocardial dimension transducers. A anterior; S
septal; P posterior; F left ventricular lateral
free wall; R
right ventricular free wall.
=
Vol. 72, No. 3, September 1985
=
669
OLSEN et al.
Results
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Measurements of left ventricular dimension were modeled by
a double hemiellipsoidal geometry as described previously.2'
External left ventricular volume was calculated as the sum of the
two ellipsoidal segments inscribed by ASPA and AFPA from
figure 1, top right. Calculation of external left ventricular volume yielded results mathematically equivalent to the formula
for a general ellipsoid, (ff/6) a b c. where a is the major diameter, b is the anterior-posterior minor diameter, and c is the
septal-free wall minor diameter. Postmortem left ventricular
wall volume was subtracted from external left ventricular volume to yield intracavitary left ventricular chamber volume.
Aortic blood flow was either measured or derived from the
inverted first derivative of left ventricular chamber volume
(-dVI/dt). Geometric deformation of the left ventricle was
determined including the latitudinal septal and free wall radii of
curvature, as well as septal displacement, and regional left
ventricular septal and free wall tensions were calculated according to the Laplace relationship, as described previously.2'
Comparisons were made between end-diastolic dimensions,
chamber volume, regional wall tensions, and measured and
calculated pressures at end-expiration and peak inspiration for
both normal and deep respirations by an analysis of variance.
Similar comparisons were made for end-ejection dimension and
volume data from the same cardiac cycles during which enddiastolic data were obtained. In an analogous fashion, peak
ejection pressure, aortic blood flow, and calculated tension data
were compared at end-expiration and peak inspiration. Linear
regression analysis was used to determine the relationship between left ventricular pressures, intrapleural pressures, left ventricular end-diastolic volume, peak aortic blood flow, and left
ventricular stroke volumes throughout the respiratory cycle.
Unless otherwise specified, all reported data were obtained during control of heart rate by atrial pacing.
L V MINOR
60
Representative analog dimension, pressure, and
flow data obtained during three deep inspirations without atrial pacing are illustrated in figure 2. A marked
inspiratory increase in heart rate was evident. During
inspiration, the fall in intrapleural pressure produced a
similar decrease in right and left ventricular intracavitary pressures. Stroke shortening decreased in all three
left ventricular dimensions. The end-diastolic diameters and volume changed in a variable fashion because
of rate-dependent changes in ventricular filling. This
resulted in a progressive and significant inspiratory fall
in peak aortic blood flow and stroke volume as inspiration progressed (figure 2).
Atrial pacing (figure 3) and autonomic blockade
(figure 4) ablated the respiratory variation in heart rate.
End-diastolic diameters and volume changed minimally, but peak aortic blood flow and stroke volume continued to decline during inspiration. During normal
spontaneous respiration, intrapleural pressure decreased from an average of -1.6 + 0.7 mm Hg (mean
+ SEM) at end-expiration to -6.1 + 0.7 mm Hg at
peak inspiration. With deep spontaneous respiration
against inspiratory inflow resistance through a gauze
sponge, intrapleural pressure decreased from an averNA
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age of0.0 ± 0.5 mm Hg atend-expirationto1 1 1.7
± 0.9 mm Hg at peak inspiration. During inspiration,
left ventricular intracavitary
end-diastolic and peak
ejection pressures decreased by amounts similar to
the changes in peak inspiratory intrapleural pressure
(p K .01), while the corresponding right ventricular
intracavitary pressures only decreased by approxione-half that amount (p < .01; table 1). The
mately
resulting left ventricular transmural
end-diastolic
pressure increased slightly (p < .05) and peak ejection pressure remained essentially constant (p > .3)
_
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and flow data obtained from a conscious dog during two deep spontaneous
respirations with heart rate controlled by atrial pacing. EE and
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that
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during deep spontaneous inspirations,
left
a
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-151
EE
FIGURE 4.
tamned from
which heart
Osec
Representative digital
a conscious
rate
with propranolol
;ic
was controlled
Vol. 72, No. 3,
September
dimension
ob-
n
taousespi
autonomic blockade
pharmacolog
dog
and atropine.
andpressuredata
EE
198567
PI
as
are,
in figure
2.
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diameters increased
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was
end-diastolic volume remained essentially
slightly
during the respiratory
controlled
increasing
by
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atrial
(table
cycle
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heart rate
figure
5),
671
A
1
OLSEN et al.
TABLE 1
Mean end-diastolic and peak ejection hemodynamic data obtained during spontaneous deep respirations
End-diastole
EE
PI
PLP
(mm Hg)
RVP
(mm Hg)
LVP
(mm Hg)
RVTMP
(mm Hg)
LVTMP
(mm Hg)
TSP
(mm Hg)
0.0+0.5
-11.7 -+0.9
5.9+1.1
-0.7 +1.6
10.0+1.1
-0.1 + 1.2
4.4+1.0
9.5 -+1.2
11.8+0.8
13.4-4-0.9
7.1±+ 1.0
3.7 + 1.0
B
B
A
B
127.8+2.2
115.7 -+4.2
36.4+1.8
43.1 ±+2.0
130.0+4.8
129.9-+-4.6
88.2+5.0
82.3 ± 3.9
B
B
B
B
Peak ejection
EE
PI
36.9+3.1
-1.0+0.6
-12.6±+1.0
31.9 - 2.4
B
B
B
Data are presented as mean + SEM for all 12 experiments.
PLP = intrapleural pressure; RVP = right ventricular intracavitary pressure: LVP = left ventricular intracavitary pressure;
RVTMP = right ventricular transmural pressure; LVTMP left ventricular transmural pressure; TSP = transseptal pressure;
EE = end-expiration; PI = peak inspiration.
Ap < .05; Bp < .01 by multivariate analysis.
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in two dogs, and decreasing slightly in the rest. The
pattern of change in each individual dog varied from
inspiration to inspiration about a narrow physiologically insignificant range. The end-ejection volume increased slightly on a more consistent basis from dog to
dog with each inspiration. Stroke shortening (figures 3
and 4), peak aortic blood flow (figure 3), and stroke
volume (p < .05; figure 5), however, still fell during
inspiration.
Diastolic left ventricular shape was significantly altered during inspiration, with most of the change resulting from leftward displacement of the interventricular septum. The altered left ventricular diastolic
geometry during inspiration was indicated by the deTABLE 2
Mean end-diastolic and end-ejection dimension data obtained during spontaneous deep respirations
a
(cm)
End-diastole
EE
PI
%1
b
(cm)
d
(cm)
7.63+0.20 6.32+0.21 2.35+0.11
7.65+0.20 6.33+0.20 2.27+0.11
--0.2+0.3
0.1 +0.4 -5.4±0.9
0.2
A
End-ejection
EE
PI
%1A
RVD
(cm)
3.00±0.29
3.25+0.30
9.0+ 1.3
B
7.50+0.19 5.91+t0.19 2.13+0.13 2.83+0.35
7.52+0.20 5.93+0.19 2.10±0.13 2.96+0.32
5.5 + 1.9
0.3 - 0.2
0.2 + 0.2 - 0.9 + 0.8
B
Data are presented as mean ± SEM for all 12 experiments.
a = basal-apical left ventricular major diameter; b = anterior-posterior left ventricular minor diameter; d = left ventricular septal displacement (segment OS from figure 1); RVD = right ventricular transverse
diameter (observations from five experiments); %A = percent change
determined as (PI- EE)/EE x 100%; other abbreviations and notes are
as in table 1.
672
crease in left ventricular septal displacement (table 2).
This resulted in an increased septal radius of curvature
during inspiration, as shown in figure 6. Peak developed septal tension, however, decreased during inspiration (p < .05; table 3), while peak developed free
wall tension remained unchanged (p > .3; table 3).
Calculated peak aortic blood flow decreased by an
average of 9% during inspiration (p < .01; table 3) and
measured aortic blood flow showed similar changes
(table 3). The inspiratory fall in measured peak ascending aortic blood flow (figure 7, A) and left ventricular
stroke volume (figure 7, B) in the five aortic flow
studies correlated with the fall in mean left ventricular
intracavitary ejection pressure (p < .001) and did not
correlate with peak left ventricular transmural pressure
or with left ventricular end-diastolic volume during the
respiratory cycle (p > . 1). Inspiratory correlations
were observed between intrapleural pressure and left
ventricular intracavitary pressure during diastole and
systole (figure 7, C and D; p < .001).
The pattern and direction of the changes in dimension, pressure, and flow observed during normal spontaneous respirations were qualitatively similar to those
recorded during deep spontaneous respiration. The
magnitude of peak inspiratory change during deep respiration was proportionally greater than that observed
during normal spontaneous respiration (p < .01 by
analysis of variance). Similarly, the results obtained
during autonomic attenuation with propranolol and
atropine were no different than those obtained during
atrial pacing.
Discussion
The model of left ventricular geometry we used requires certain assumptions about cardiac shape in order
CIRCULATION
LABORATORY INVESTIGATION-VENTRICULAR PERFORMANCE
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diameters measured in the current study, upon which
assumptions about left ventricular shape were based,
corresponded closely to the three principal axes (directions) of deformation derived from the eigenvector
analysis of left ventricular geometry in an intact dog
preparation by Walley et al.26 The deformations in
these principal axes were similar in magnitude and
direction to those observed in the present model.2'
The interventricular septum was shifted leftward
during diastole by the inspiratory augmentation in venous return to the right ventricle (table 2). This resulted in an altered left ventricular geometry that reduced
chamber compliance, as demonstrated by the upward
shift of the normalized pressure-volume curve in figure
8. This observation was consistent from dog to dog and
from inspiration to inspiration in each dog. Detailed
discussions of this methodology and the normalization
procedures have been published previously.21 23-25 The
reduction in left ventricular chamber compliance that
occurs during direct ventricular interactions has been
demonstrated previously,21 and indicates one effect of
p
a)
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15(19.42
21.66
\+1.92/
EE
\+2.23/
1
I
S
PI
FIGURE 5. Top, Left ventricular end-diastolic volumes recorded during the 12 experiments at end-expiration (EE) and peak inspiration (PI).
The order of individual studies from top to bottom at EE is: 9, 1, 2, 11,
6, 5, 4, 3, 10, 8, 12, 7. Means ± SEM are shown in parentheses; p >
.06. Middle, Left ventricular end-ejection volumes for all 12 experiments at EE and PI. The order of individual studies from top to bottom at
EE is: 9, 1, 6, 7, 5, 11, 8, 4, 12, 3, 10, 7 (p > .35). Bottom, Left
ventricular stroke volume recorded during the 12 experiments at EE and
PI. The order of individual studies from top to bottom at EE is: 9, 2, 1,
11, 4, 3, 6, 5, 10, 12, 8, 7 (p < .05).
that conclusions about volume changes can be derived.
While it is difficult to validate these assumptions, the
volume data we obtained by this technique correlate
well with those obtained by two other independent
methods, namely intraventricular balloon and electromagnetic determination of ascending aortic blood flow
(see Appendix). The three principal left ventricular
Vol. 72, No. 3, September 1985
1F
F
/
A
End-Expiration
o---o Peak Inspiration
FIGURE 6. Model of the left ventricle latitudinal plane representing
change in the average end-diastolic shape during the respiratory cycle
over all 12 experiments. During peak deep inspiration (open circles and
broken line) the interventricular septum was shifted toward the left
ventricle, indicating direct ventricular interaction. A, S, P, and F represent the anterior, septal, posterior, and lateral free walls, respectively.
The end-diastolic latitudinal septal radius of curvature was greater during inspiration (RS2 = 4.41 cm 0.49 cm) than during end-expiration
(RS, = 4.25 cm ± 0.49 cm; p < .05).
673
OLSEN et al.
TABLE 3
Mean ejection data obtained during spontaneous deep respirations
EE
PI
Ao max
(ml sec -1)
V1 max
(ml sec -)
T5 max
(mm Hg cm)
TF max
(mm Hg cm)
(mm Hg sec -1)
334.8 + 60.7
306.1 ± 55.6
8.4± 1.0
313.9± 15.8
285.2 ± 14.2
-9.0+ 1.1
349.0 ± 22.4
325.1 ± 21.2
-6.7± 1.5
401.4± 14.4
397.4 -+13.5
-0.8± 1.1
2429 ± 89
2249 ± 116
-6.5±2.0
B
B
A
Pmax
Data are presented as mean ± SEM for all 12 experiments.
Ao max = peak measured ascending aortic blood flow (observations from five experiments); V, max ± peak calculated aortic
blood flow; Ts max = peak left ventricular transseptal tension; TF max = peak left ventricular free wall tension; P max = peak
positive left ventricular transmural dP/dt; other abbreviations and notes are as in tables 1 and 2.
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gravitational gradients throughout the chest, measurement of esophageal or peripheral pleural pressure may
yield inaccurate results.27 The use of balloon or fluidfilled catheters may increase the magnitude of impact
artifacts and baseline pressure shifts.20 28
In the present studies, the pericardium was left
widely open to avoid the potential restrictive effects of
scarring or reapproximation of surgically manipulated
pericardium. At postmortem examination, the pericardium remained widely open and nonadherent to the
right or left ventricles. The effect of an intact pericardium on the results of the present study probably
would have been minimal since there were no large
changes in ventricular volumes. Moreover, changes in
intrapericardial pressure during respiration closely parallel intrapleural pressure changes in the conscious
dog.27 29 Opening the pericardium in an intact, closed-
respiration on cardiac function. Figure 8 also attests to
the need for accurate measurement of pleural pressure
in the assessment of ventricular function, as well as the
need for differentiation of end-expiratory from peak
inspiratory cardiac cycles in the analysis of diastolic
properties.
The accurate measurement of pleural pressure was
critical in this study. Pleural pressure should be measured on the surface of the heart at approximately the
same vertical level as the intracavitary manometer.
The placement of the pleural micromanometer within a
large-bore silicone rubber tube with multiple side holes
protected the manometer face from motion artifacts but
still allowed free communication with the potential
space of the pleural cavity. In this manner, reproducible and accurate measurements were made of the pleural pressure affecting cardiac function. Because of the
20,
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V.
115
120
125
130
135
Meon Left Ventricular
Ejection Pressure (mmHg)
674
140
-20
-15
-1O
-5
Pleurol Pressure
(mmHg)
FIGURE 7. A, Representative relationship between
mean left ventricular intracavitary ejection pressure
and peak ascending aortic blood flow during deep
spontaneous respirations in one experiment. Linear
regression coefficients for the five experiments in
which ascending aortic blood flow was measured
were m = 8.045 + 3.860 and b = -772.220 ±
485.785 (r . .503, p < .005). B, Relationship between mean left ventricular intracavitary ejection
pressure and left ventricular stroke volume measured
from ascending aortic blood flow during the same
deep spontaneous respirations as in A. For all five
experimentsm = 0.302 ± 0.089andb = -18.249
± 10.950 (r ' .560, p < .01). C, Representative
end-diastolic relationship between left ventricular intracavitary pressure and simultaneous intrapleural
pressure during the same deep spontaneous respirations as in A. For all five experiments m = 0.922 +
0.084 and b = 12.593 ± 2.438 (r . .835, p <
.001). D, Same relationship as in A except during
ejection. For all five experiments m = 1.370 +
0.230 and b = 142.067 ± 5.733 (r . .835, p <
.001).
CIRCULATION
LABORATORY INVESTIGATION-VENTRICULAR PERFORMANCE
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0.10
0.15
LV Volume Strain (CE )
FIGURE 8. The effects of respiration on the normalized left ventricular
diastolic pressure-volume relationship in one experiment. The solid
curve was obtained by fitting all end-diastolic end-expiration data during a transient vena caval occlusion to the exponential function P =
(eP' - 1), where a and are nonlinear coefficients describing the curve
and were 0.837 and 13.188, respectively. Superimposed on this curve
are data digitized at 200 Hz from two separate cardiac cycles: one from
end-expiration (EE, closed circles) and one from peak inspiration (PI,
open circles). Peak inspiratory intrapleural pressure was - 12.7 mm Hg.
a
chest canine preparation had no effect on right and left
ventricular pressures, left ventricular volumes, or ejection fraction, suggesting that at normal end-diastolic
volumes and pressures, the pericardium has minimal
influence on ventricular function.26 An intact pericardium may augment inspiratory leftward septal shifting
via the direct ventricular interaction that results from
increased right ventricular end-diastolic volumes.
However, it is doubtful that such direct ventricular
interaction significantly impairs left ventricular function or contributes to the inspiratory fall in left ventricular stroke volume. 19 In a series of unpublished studies
from this laboratory in which the pericardium remained intact, the inspiratory changes in the principal
measured diameter were similar in direction and magnitude to those observed in the present study.29
The marked respiratory variation in heart rate observed during deep, and to a lesser extend during normal respiration, resulted in rather large fluctuations in
beat-to-beat left ventricular end-diastolic volume. Several mechanisms have been proposed for this.3032 Both
atrial pacing and pharmacologic autonomic attenuation
with propranolol and atropine effectively ablated the
respiratory change in heart rate and neither resulted in
a significant change in left ventricular end-diastolic
Vol. 72, No. 3, September 1985
volumes (in some dogs volume increased slightly
while in others it decreased minimally). Similar results
have recently been observed on radionuclide ventriculograms from healthy human subjects during deep inspirations against resistance.33
The inspiratory decrease in left ventricular end-diastolic volume has been thought to result from increased
pooling of blood in the lungs'7 or delayed pulmonary
transit time of blood.7 34 Both would cause a decrease
in left ventricular end-diastolic volume (preload) and
account for the subsequent fall in left ventricular stroke
shortening and peak aortic blood flow that is so
apparent in figure 3. Increases in heart rate alone can
cause a fall in left ventricular end-diastolic and stroke
volumes.22 30 However, when heart rate was kept constant by atrial pacing or by pharmacologic autonomic
attenuation, as demonstrated in figures 3 and 4, the left
ventricular end-diastolic volume remained relatively
unchanged, suggesting that under these conditions, increased venous pooling in the lungs or delayed pulmonary transit time was insufficient to prevent adequate
left ventricular filling and played only a minor physiologic role.
In addition, leftward shifting of the interventricular
septum did not seem to significantly inhibit left ventricular filling when heart rate was kept constant. This
is graphically apparent in figure 3. During the prolonged second inspiration, the interventricular septum
initially was shifted leftward (reduced minor-axis septal-free wall diameter), with augmented venous return
to the right ventricle (increased right ventricular transverse diameter). As inspiration progressed, augmented
venous return became less apparent and the septum
shifted back to the right, presumably as left ventricular
end-diastolic volume increased due to delayed return
of the increased pulmonary pooling of blood. Aortic
blood flow, however, continued to decrease apparently independent of these events. Similar changes in left
ventricular end-diastolic volume and aortic blood flow
were observed in several dogs during prolonged deep
inspirations.
Another proposed hypothesis has been that leftward
shifting of the interventricular septum during inspiration alters ventricular geometry and increases the geometric component of left ventricular afterload.'8 '9
Flattening of the interventricular septum might increase the septal radius of curvature, augment septal
wall tension, and impede left ventricular stroke volume during ejection. Although the present studies
demonstrated an inspiratory leftward shifting of the
septum with altered diastolic geometry that persisted
into systole, the increase in septal radius of curvature
675
OLSEN et al.
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was small and was outweighed by the larger fall in the
transseptal pressure gradient (table 1). Thus, left ventricular septal wall tension actually decreased during
inspiration (table 3), and the augmentation in the geometric component of left ventricular afterload from
septal shifting did not occur.
Yet another proposed hypothesis is that the inspiratory decline in pleural pressure increased left ventricular transmural pressure (left ventricular intracavitary
pressure minus pleural pressure), causing a fall in
stroke volume.6 9, 12 20. 3436 Intracavitary left ventricular ejection pressure decreased by an amount similar to
that by which pleural pressure is decreased during inspiration such that left ventricular transmural ejection
pressure remained unchanged (table 1). Thus, augmentation of the intraventricular pressure component
of left ventricular afterload did not appear to account
for the inspiratory fall in left ventricular stroke volume. Similar observations have been made by others.7"
From the present data, an alternative explanation is
proposed for the inspiratory fall in left ventricular
stroke volume. The correlations between peak aortic
blood flow, left ventricular stroke volume, and mean
intracavitary left ventricular ejection pressure (figure
7, A and B) has led us to the hypothesis that the intracavitary left ventricular pressure referenced to atmospheric pressure is actually the effective ejection pressure of the left ventricle and that the inspiratory
decrease in this pressure accounts for the fall in stroke
volume. During diastole, the heart is the chamber at
the end of the blood flow and pleural pressure is the
appropriate external pressure. However, during ejection, when the aortic valve is open and the left ventricle
is in continuity with the systemic arterial system, the
peripheral vasculature is at the end of the blood flow
and atmospheric pressure is the appropriate external
pressure. During inspiration, the hydraulic force effecting ejection (intracavitary left ventricular pressure)
is decreased by an amount equal to the decline in
intrapleural pressure, and left ventricular stroke volume falls as a result of the decrease in this effective left
ventricular ejection pressure.
Intrathoracic aortic pressure referenced to atmospheric pressure is reported to fall during inspira20 but to a lesser degree than the inspiratory
tion,6, 12h
reduction in intracavitary left ventricular pressure.
This is reported to increase left ventricular afterload
and decrease stroke volume. In unpublished observations from this laboratory simultaneously measured
high-fidelity left ventricular, ascending and descending thoracic aortic, and abdominal aortic pressures
were all observed to fall by a similar amount equal to
676
the inspiratory decline in pleural pressure during normal and deep inspiration. Thus, the transmural pressures referenced to pleural pressure at these four simultaneous points of measurement along the central and
systemic vascular system did not rise during inspiration, but instead remained essentially unchanged. An
increase in left ventricular or transthoracic aortic afterload that might account for the inspiratory fall in stroke
volume was not apparent in these studies, or in others.7" The impedance in effective left ventricular ejection pressure induced by the inspiratory decline in
pleural pressure had an effect on left ventricular stroke
volume similar to that of an increase in left ventricular
afterload, but it apparently occurred by a different
mechanism since no measurable increase in transmural
left ventricular or transthoracic aortic afterload could
be demonstrated. It is therefore more appropriate to
refer to the inspiratory effect of pleural pressure on left
ventricular function as an impedance of the effective
ejection pressure rather than an increase in left ventricular afterload in terms of systolic wall stress.33
Right ventricular ejection is not effected during inspiration by the same mechanism that effects left ventricular ejection. During right ventricular ejection,
when the pulmonary valve is open, the right ventricle
is in continuity with the pulmonary circulation and the
left atrium, all of which are subjected to the same
inspiratory fall in intrapleural pressure. Thus, pleural
pressure is the appropriate external pressure for the
right ventricle during ejection and during diastole. Accordingly, during inspiration, the hydraulic force effecting ejection from the right ventricle is not decreased relative to its appropriate external pressure and
right ventricular stroke volume would not be expected
to fall on the basis of a decreased effective ejection
pressure. In fact, the effective ejection pressure of the
right ventricle (right ventricular transmural pressure)
was increased during inspiration (table 1) as a result of
increased venous return (preload), and right ventricular stroke volume was augmented. Right ventricular
cavitary volume was not assessed directly in the current study, although increases in the end-diastolic
transverse diameter during inspiration (table 2) were
believed to represent increased right ventricular enddiastolic volume and were found to correlate linearly
with postmortem right ventricular intracavitary balloon volumes (see Appendix). Similar results have
been reported by others.19
Clinically, an exaggeration of the normal inspiratory decline in left ventricular stroke volume may result in pulsus paradoxus, the absence of a peripheral
pulse despite the presence of a cardiac contraction.38
CIRCULATION
LABORATORY INVESTIGATION-vENTRICULAR PERFORMANCE
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Conditions that accentuate the swings in pleural pressure (such as asthma, pulmonary embolism, or pulmonary edema), and conditions that increase the interactive coupling between the right and left ventricles
(such as cardiac tamponade or acute right heart failure)
may result in either pulsus paradoxus or an increased
widening of the inspiratory fall in peak systemic blood
pressure. Conversely, the marked increases in the
pleural pressure that occur with coughing may produce
reversed pulsus paradoxus, the presence of a peripheral pulse in the absence of a cardiac contraction.39'40
Conditions that elevate the intrathoracic pressure, such
as positive pressure ventilation, Valsalva maneuver, or
coughing, augment left ventricular stroke volume as
well as forward flow of blood from the thoracic aorta
via a thoracic pump mechanism.40 Factors elevating
pleural pressure augment left ventricular pressure and
favor left ventricular ejection, while conditions reducing pleural pressure lower the effective left ventricular
ejection pressure and impede left ventricular stroke
volume. In this regard, deep inspiration may be referred to as a reverse thoracic pump mechanism.
Thus, a hypothesis is proposed that is consistent
with, as well as an extension of, the thoracic pump
mechanism to explain the long-observed differential
effects of inspiration on right and left ventricular stroke
volumes. Conceptually, this hypothesis provides a
more accurate explanation of cardiorespiratory interaction during inspiration than has previously been offered. Other mechanisms, such as altered preload or
afterload, appear to contribute only secondarily, if at
all, to the inspiratory fall in left ventricular stroke
volume. The principal factor diminishing left ventricular stroke volume during inspiration is the inspiratory
fall in the effective intracavitary ejection pressure of
the left ventricle.
Appendix
The modified ellipsoid used in the current studies to model
left ventricular shape and volume represents the concatenation
of two ellipsoidal segments and has been discussed in detail
previously.21 The current model accurately predicted left ventricular stroke volume over a wide range of left ventricular
volumes and under various conditions of ventricular interaction
with both high and low right ventricular volumes. The stroke
volumes and flows calculated from the dimension measurements as - dV1/dt correlated very well over a wide range of
physiologic volumes, with minimal variability when compared
with the stroke volumes and flows measured by an ascending
aortic electromagnetic flow probe.2'
The dimension transducers were positioned at approximately
90 degree points around the latitudinal and longitudinal circumferences of the left ventricle. The true three-dimensional position of each transducer was determined in separate validation
studies by measurement with the linear chords from all possible
paired combinations of the septal and epicardial crystals. The
results of one such experiment are shown in figure 9, where the
Vol. 72, No. 3, September 1985
true three-dimensional position of each transducer determined
by the chord measurements was compared with the assumed
position of these transducers based on the double hemiellipsoidal model (figure 1). The difference in volume calculated from
the assumed model and that computed from the actual position
based on a three-point derivation of an ellipsoidal segment was
minimal (0.9 to 1.8 ml) and accounted for less than a 3%
difference in corresponding calculated chamber volumes.
In four studies, in which the hearts were excised with the
ultrasonic dimension transducers still in place and before determination of left ventricular wall volume displacement, both
atria, the tricuspid and mitral valves, and chordae tendineae
were removed. The semilunar valve orifices were individually
sutured closed, compliant balloons attached to Lucite disks
were introduced into each ventricle, and the sewing rings of the
disks were sutured to the anuli of the tricuspid and mitral valves.
The excised heart was then suspended in a water bath and left
ventricular balloon volumes were varied over a wide range at
various right ventricular balloon volumes while recording left
and right ventricular ultrasonic dimensions. At various levels of
right ventricular balloon volume ranging from 0 to 60 ml, the
correlation between the absolute measured and calculated left
ventricular chamber volumes was excellent, and the line of
regression was very near the line of identity, despite marked
differences in relative septal position (figure 10, A). In a similar
fashion, right ventricular transverse diameter was linearly related to right ventricular cavitary balloon volume (figure 10, B).
These data, coupled with those published previously,2' indicate the validity of the current model in accurately assessing left
ventricular volume and geometry.
We are grateful to Mr. James Bradsher and his staff for
technical assistance, to Ms. Sandra Justice for preparing the
manuscript, and to the Duke Audiovisual Department for the
illustration.
POSTERIOR
BASE
BASE
POSTERIOR
--------
APEX
B
SEPTAL
TERIOR
~ ~
~
-
FREEWALL
APEX
FIGURE 9. Comparison of left ventricular geometry derived from the
position of the dimension transducers assumed by the model (thin solid
lines) with geometry obtained from the actual position of the dimension
transducers calculated from the chord measurements (broken and heavy
solid lines). A, Latitudinal plane; B, longitudinal plane through the
anterior and posterior transducers; C, longitudinal plane through the
septal and free wall transducers. The difference in the actual and assumed volumes calculated by the two methods was less than 3%.
677
OLSEN et al.
r - U. Jvo}
_
60 f
r -
RV Chamber Volume
:
mI
'4.0
-
V= 60 m1
20 40
3.-
40
-
.-
>
40 6*
20
Meosured LV Chamber Volume (m1)
20
0
80
40
60
80
sured RV Chomber V@olume (mli)
Downloaded from http://circ.ahajournals.org/ by guest on April 29, 2017
FIGURE 10. A, Calculated chamber volume vs measured left ventricular intracavitary balloon volume from four postmortem
studies at various levels of right ventricular volume. LV = left ventricle; RV right ventricle. B, Correlation between right
ventricular transverse diameter and right ventricular intracavitary balloon volume from one postmortem study.
=
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Vol. 72, No. 3, September 1985
679
Diminished stroke volume during inspiration: a reverse thoracic pump.
C O Olsen, G S Tyson, G W Maier, J W Davis and J S Rankin
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Circulation. 1985;72:668-679
doi: 10.1161/01.CIR.72.3.668
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