Download Comparison of Contractile Performance of Canine Atrial and

Comparison of Contractile Performance of Canine Atrial and
Ventricular Muscles
By Ferdinand Urthaler, Alfred A. Walker, Lloyd L. Hefner, and Thomas N. James
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ABSTRACT
This study compared the contractile performance of a canine right atrial trabecula with
that of a macroscopically indistinguishable trabecula isolated from the right ventricular
apex. The heart was removed from nine mongrel puppies weighing 6-8 kg and placed in
Krebs-Ringer's bicarbonate solution. The bathing solution contained only 1.25 mmoles of
Ca2+ and was bubbled with a 95% O2-5% CO2 gas mixture. Each atrial trabecula was
specially selected from the right atrial appendage. Histologically, these trabeculae showed
a remarkable longitudinal orientation of the fibers. At Lmax (the length of the muscle at
which developed tension was maximum) under identical conditions of temperature, rate
of stimulation, ionic milieu, pH, and O2 and CO2 supply, right atrial trabeculae achieved
the same developed and total tensions but in a much shorter time than did ventricular
trabeculae. In both muscle groups the maximum developed tension averaged about 2.5
g/mm2. Since Lo (expressed as a fraction of Lmax) was less in atrial muscle than it was in
ventricular muscle, we concluded that atrial muscle can be stretched considerably more
than can ventricular muscle before optimum length is reached. At any given initial muscle
length, the maximum of tension rise for atrial trabeculae amounted to at least twice that
for ventricular trabeculae. At any given load up to 1.5 g/mm2, the maximum velocity of
shortening of an atrial trabecula was about three to four times that of a ventricular
trabecula. These results collectively indicate that the contractile performance of the right
atrial muscle is in many respects superior to that of the right ventricle, at least under the
conditions of these experiments.
• The working myocardial cells of the cardiac atria
differ morphologically from those of the ventricles
(1-14). Atrial myocytes are smaller, branch less
often, have fewer if any transverse tubules, and
contain specific granules that are not found in
ventricular myocytes. There are also significant
differences between the pharmacological responses
of atrial and ventricular muscles (15, 16). Whereas
abundant information is available about the mechanical behavior of ventricular myocardium
(15-23), much less is known about atrial myocardial performance, and conflicting results have been
reported (15, 16, 24). Differences in the reported
results may be due in part to considerable species
variability (15, 16) and in part to the fact that
published accounts have often failed to emphasize
how the results were obtained under significantly
different experimental conditions (15, 16). Although dogs are among the most frequently used
animals in the experimental cardiovascular laboratory, we can find no report comparing the mechanical properties of canine right atrial and right
ventricular trabeculae.
From the Department of Medicine, University of Alabama
Medical Center, Birmingham, Alabama 35294.
This work was supported by U. S. Public Health Service
Grant HL 11,310 from the National Heart and Lung Institute
and by MIRU Contract 4367-1441.
Received March 10, 1975. Accepted for publication September 12, 1975.
762
The present study was conducted to compare the
contractile performance of a canine right atrial
trabecula with that of its right ventricular counterpart under identical experimental conditions.
Methods
Nine mongrel puppies of either sex (12 ± 4 weeks of
age, 6-8 kg) were anesthetized with sodium pentobarbital (30 mg/kg, iv). The entire heart was then rapidly
removed and placed in a beaker of Krebs-Ringer's
bicarbonate solution that was being bubbled at 37°C
with a 95% O2-5% CO2 gas mixture. The bathing solution
contained (mmoles/liter): Na + 145, K+ 4.2, Ca2+ 1.25,
Mg2+ 1.2, Cl- 125, SO 4 2 - 1.2, H 2 PO 4 - 2.4, HCCV 25,
and glucose 5.6. The same continuously oxygenated and
stirred solution was also utilized for isolated muscle
perfusion. After equilibration, the solution had an oxygen tension (Po2) of 550 mm Hg or greater and a pH of
7.40 ± 0.02.
Ventricular trabeculae were all removed from the
apical region of the right ventricle, and each trabecula
was obtained from the right atrial appendage. We have
found that certain trabeculae of the right atrial appendage are not randomly distributed (unpublished observation). In the present study we chose the trabecula
coursing from the crista terminalis adjacent to the sinus
node toward the vortex of the right atrial appendage
(Fig. 1). Histologically, these trabeculae showed a regular longitudinal orientation of the fibers (Fig. 2). In these
histological sections, atrial trabeculae did not appear to
have more interstitial connective tissue nor were they
surrounded by a greater amount of endocardium than
were ventricular trabeculae.
Circulation Research, Vol. 37, December 1975
ATRIAL AND VENTRICULAR MUSCLE MECHANICS
SVC
FIGURE 1
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Opening the right atrium along the crista terminalis (CT) and
the atrioventricular sulcus (AVS) exposes the entrance to the
atrial appendage. The open arrow indicates the anchorage of the
crista terminalis and the white arrow identifies the right atrial
trabecula utilized in this study. SN = sinus node and SVC =
superior vena cava.
The muscles were mounted in an experimental apparatus that has been described previously (20, 25, 26). One
end of the muscle was attached to a fixed force gauge
with no measurable nonlinearity in the tension signal
over applied forces up to 10 g. The other end of the
muscle was attached to a light aluminum pendulum for
determination of length changes. Positional changes of
the length lever were sensed by a linear differential
transformer whose small iron core was firmly attached to
the lever. The equivalent mass of the lever was 0.3 g,
which has negligible effect on muscle characteristics.
Lever displacements of up to 10 mm showed no measurable nonlinearity in the length signal. The frequency
responses for both systems were determined and found to
be accurate up to 100 Hz. The compliance of the tension
transducers and the lever system combined was less than
1.0 fi/g. An adjustable micrometer, which restrained the
lever movement, was used to set the muscle lengths.
Along the lever a small wire carrying electrical current in
a magnetic field generated the desired forces (load on the
muscle) to hold the lever against the micrometer.
Outputs from the force and length gauges along with
the stimulus signal were sent through an analog-to-digital converter to a PDP-7 computer. The computer then
sent a signal through a digital-to-analog converter back
to the apparatus to control the loading of the muscle.
Prior to a run of each isometric tension series, the computer checked and rezeroed the tension transducer if
necessary. Three contractions were then obtained and
averaged, and the following data were calculated and recorded on digital tape: the length and tension signals at
1000 samples/sec, resting tension, developed tension
(peak developed isometric tension at L max ), maximum
rate of tension rise, maximum change in length, maximum velocity of shortening, latency time (defined and
measured as the interval between the onset of the
stimulus and the point at which the developed tension
Circulation Research, Vol. 37, December 1975
763
reached 2% of its maximum value), time to maximum
tension, time to maximum rate of tension rise, time to
maximum shortening, time to maximum velocity of
shortening, and relaxation time. The cross-sectional
area was estimated at LmBI (the length of the muscle
at which developed tension was maximum) by dividing the weight of the muscle by its length. This value
was then utilized as the normalizing factor for the tensions.
After being mounted, the muscles were allowed to
shorten with a preload of about 200 mg. This load closely
approximates 50% of the resting tension subsequently
measured at Lmax. After 2 hours peak isometric tension
showed no significant further increase; it remained
constant for the next 30-36 hours. Each experiment
began on the fourteenth hour and was completed within
4 hours. After each incremental change in initial muscle
length, 5 minutes were allowed to elapse before the data
were recorded. This procedure was adopted to minimize
the effect of stress-relaxation. The temperature was
maintained constant (±0.1°C) through a feedback-controlled Peltier junction.
All of the preparations that we used were quiescent
unless they were stimulated. When not otherwise specified, the muscles were all stimulated 12 times/min by
square-wave pulses from a Grass stimulator. The stimulus duration was 5 msec, and the voltages used were
slightly (about 10%) above threshold. Unless otherwise
indicated, the results are expressed as means ± 1 SD. The
significance of differences was assessed by Student's ttest; the comparison of regression lines was done by
standard techniques (27).
Results
SELECTION OF AN APPROPRIATE TEMPERATURE ANO
STIMULATION RATE
In most species a change in temperature profoundly influences both the membrane potential
and the myocardial contractile performance. Temperature affects contractile performance in both
atrial and ventricular trabeculae. Pilot experiments conducted to select a temperature and a rate
of stimulation at which both the atrial and the
ventricular muscles would perform optimally for at
least 24 hours showed that a temperature of 25°C
and a stimulation rate of 12 beats/min satisfied
these requirements (Fig. 3).
COMPARATIVE LENGTH-TENSION DIAGRAMS
In five atrial and four ventricular trabeculae,
isometric beats were obtained and analyzed at
twelve different initial muscle lengths. Figure 4 is
the composite graph obtained after the means of
their respective resting and developed tensions
measured at four selected initial muscle lengths
were plotted. Four points were chosen for comparative purposes because only these points were exactly common to each muscle of each group. Discrimination between loads varying from 0 to 50 mg
was difficult and often unreliable. For this reason,
764
URTHALER, WALKER. HEFNER. JAMES
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B
FIGURE 2
Two photomicrographs illustrating the remarkable longitudinal orientation (A) and the compartmentation (B) of individual muscle fibers in a right atrial trabecula. Note that the myocytes are slender
and show little branching.
in the present study, L o of atrial and ventricular
trabeculae was arbitrarily defined as the muscle
length at which the average preload was equal to 70
± 20 mg.
In the five atrial trabeculae, Lo averaged 0.866
mm/L max . The relationship between the resting or
the developed tensions and the corresponding initial muscle lengths was well estimated by a straight
line. In the four ventricular trabeculae, I<> averaged
0.920 mm/L max . The relationship between the resting or the developed tensions and the correspond-
ing initial muscle lengths was approximately a
straight line. Lo, expressed as a fraction of Lmax,
was less in atrial muscle than it was in ventricular
muscle (P < 0.05). Atrial muscle can thus be
stretched considerably more than can ventricular
muscle before optimum length is reached. At Lo,
atrial and ventricular muscles developed almost
the same tensions. This was also the case at Lmax
where the developed tension of atrial muscle was
2.43 ± 0.46 g/mm2 and that of ventricular muscle
was 2.63 ± 0.52 g/mm2. At Lmax, the resting
Circulation Research, Vol. 37, December 1975
765
ATRIAL AND VENTRICULAR MUSCLE MECHANICS
Lmax the cross-sectional area, weight, muscle
length, resting tension, and developed tension were
not significantly different. In contrast, all measurements of duration were significantly different (P <
0.01). For example, the latency period in the atrial
trabeculae was briefer and averaged only 66%
of that in the ventricular trabeculae. Other measurements of duration in the atrial muscles ranged
between 50% and 76% of the corresponding measurements in the ventricular muscles.
CHANGES IN MAXIMUM RATE OF TENSION RISE AS A FUNCTION
OF LENGTH
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200
400
600
800
Figure 5 shows measurements obtained in both
atrial and ventricular muscles and illustrates the
characteristic succession of changes in the maximum rate of tension rise as a function of length.
Again a straight line was chosen to express this
relationship. This diagram also indicates that at
any given initial muscle length the absolute values
for maximum rate of tension rise achieved by atrial
1000
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200
400
600
800
1000
y = -8.7 + 11.2x
y = - 1 5 . 6 + 18.2x
r = 0.78
1.2
Time in msec
FIGURE 3
Records illustrating the effect of three different temperatures on
the contraction of a canine right atrial and right ventricular
trabecula. Both muscles were studied at Lmax and stimulated 12
times/min. Note that tension is inscribed from bottom to top,
whereas shortening expressed as a fraction of Lmax is inscribed
from top to bottom. At 25°C both muscles generated a tension
amounting to approximately 2.5 g/mm2.
tensions were also similar, being 0.53 ± 0.12 g/mm2
in atrial muscle and 0.43 ± 0.17 g/mm2 in ventricular muscle.
'
%
•
0.8
Atrium
0.4
•
y = -3.20 + 3.76x
r = 0.89
0.84
0.88
0.92
0.96
1.00
Length in m m / L m a x
FIGURE 4
COMPARISON BETWEEN ATRIAL AND VENTRICULAR ISOMETRIC
BEATS STUDIED AT L^.x
Table 1 summarizes our data collected at L ma ,
with a comparative statistical evaluation of the
means obtained. These results indicate that at
Circulation Research, Vol. 37, December 1975
Length-tension curves of canine atrial and ventricular trabeculae compared at a temperature of25°C and a stimulation rate of
12 beats/min. These two length-tension diagrams were plotted
using the respective means of the resting and developed tensions
o/ five atrial and four ventricular trabeculae.
766
URTHALER, WALKER. HEFNER. JAMES
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CHANGES IN TIME TO MAXIMUM TENSION AS A FUNCTION OF
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trabeculae were significantly greater (P < 0.05)
than those developed by ventricular trabeculae.
Figure 6 represents changes in time to peak tension as a function of initial muscle length. The relationship is expressed as a straight line. Changes
in initial muscle length had no significant influence
on atrial time to peak tension, whereas comparable
changes in initial muscle length significantly affected time to peak tension in the ventricle. This
latter effect, however, was at best moderate, since
the difference was only significant (P < 0.05)
when the mean of the time to peak tension measured at Lo was compared with the mean of the
time to peak tension measured at L max .
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CHANGES IN DURATION OF CONTRACTION AND IN RELAXATION
TIME AS A FUNCTION OF LENGTH
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In both tissues the duration of the contraction
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FIGURE 5
Progressive increase in the maximum rate of tension rise as a
function of initial muscle length, compared in canine atrial and
ventricular trabeculae. At Lmal the mean rate of tension rise in
atrial trabeculae was more than twice that observed in ventricular trabeculae.
Circulation Research, Vol. 37, December 1975
767
ATRIAL AND VENTRICULAR MUSCLE MECHANICS
atrium than they were in the ventricle. The latency
period, the time to maximum velocity, and the
time to maximum shortening were all significantly
briefer (P < 0.01) in the atrial tissue.
550
450
Rate: 12 Beats/Minute
SHORTENING AS A FUNCTION OF LOAD
Temp: 25°C
Both atrial and ventricular muscles at Lmax
developed a comparable tension which averaged
approximately 2.5 g/mm2. From fifteen different
routine afterloaded contractions, three representative examples of these loads were selected for
comparative purposes. Figure 8 illustrates a progressive decrease in shortening with increments in
load. At loads of 1 g and less, any increment in load
resulted in a greater decrease in shortening in the
atrium than it did in the ventricle (P < 0.01). For
loads of 1.5 g or more, there was no significant
difference between the amount of shortening
achieved by the two specimens.
Ventricle
350
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Atrium
•
y = - 2 4 + 295x
r = 0.83
y = 262 - 29x
r = 0.068
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150
VELOCITY OF SHORTENING AS A FUNCTION OF LOAD
0.84
0.88
0.92
0.96
1.00
At Lmax any increment in load decreased the
velocity of shortening more in the atrial muscle
Length in m m / L m a x
FIGURE 6
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Changes in time to peak tension as a function of initial muscle
length compared in canine atrial and ventricular trabeculae. In
the ventricle, changes in initial muscle length from 94% of Lmal
up to Lmai barely influenced the time to peak tension.
1000
Rate: 12 Beats/Minute
Temp: 25°C
initial muscle length resulted in a corresponding
proportional change in the duration of either an
atrial or a ventricular contraction, but the latter
always required a longer time. Similarly, relaxation
time increased with increments in initial muscle
length in both types of muscle, but at any given
initial muscle length relaxation time was significantly shorter (P < 0.01) in the atrium.
ISOTONIC SERIES
Table 2 summarizes force-muscle shortening relationships obtained at L max with a constant afterload of 1 g. Lmax was chosen because at this length
both muscle specimens had similar resting, developed, and total tensions. Table 2 also shows a
statistical evaluation of the differences between the
respective means. Cross-sectional area, weight, and
length are the same as those cited in Table 1.
Under these experimental conditions, there was no
significant difference between the resting tension of
atrial and ventricular trabeculae. (There was also
no detectable difference between resting tension of
atrial and ventricular trabeculae when they were
studied under isometric conditions.) The distance
shortened and the maximum velocity of shortening
were both significantly greater (P < 0.01) in the
Circulation Research, Vol. 37, December 1975
900
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800
700
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°
y = - 1 2 4 7 + 2267x
r = 0.86
Atrium
y = - 7 3 0 + 1385x
•
r = 0.76
600
500
400
0.84
0 88
0.92
0.96
1.00
Length in mm/L m a x
FIGURE 7
Progressive increase in duration of contraction as a function of
initial muscle length compared in canine atrial and ventricular
trabeculae. At Lmal, the mean duration of contraction in a
ventricular trabecula was almost twice that in an atrial trabecula.
768
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FIGURE 8
Progressive decrease in shortening (AL) as a function of load
compared in canine atrial and ventricular trabeculae at Lmax.
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tension, shortening of an atrial trabecula was almost twice that
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than it did in the ventricular muscle (Fig. 9). In
both types of trabeculae, the relationship fit a
straight line for the loads selected. At all loads from
0.5 g to 1.5 g, the velocity of shortening was
significantly greater (P < 0.01) in the atrial
muscles. Figure 10 illustrates a characteristic forcevelocity curve for each type of muscle, indicating
that the maximum velocity of shortening (Vmax)
was about four times greater in the atrial muscle
than it was in the ventricular muscle.
COMPARISON BETWEEN TIME TO MAXIMUM VELOCITY OF
SHORTENING AND TIME TO MAXIMUM RATE OF TENSION RISE
Figure 11 illustrates the progressive increase in
time to maximum velocity with increasing load. At
all loads studied, atrial trabeculae reached maximum velocity in a significantly shorter period of
time (P < 0.01) than did ventricular trabeculae.
The relationships were estimated by straight lines.
Extrapolation of the straight lines gave y-intercept
Circulation Research, Vol. 37, December 1975
769
ATRIAL AND VENTRICULAR MUSCLE MECHANICS
Discussion
1.2
1.0
Atrium
•
y = 1.03 - 0.40x
r = 0.83
Ventricle
y = 0.29 - O.llx
0.8
°
r = 0.81
1 0.6
£• 0.4
Rate: 12 Beats/Minute
0.2
0.5
1.0
Load in g/mm
1.5
2
FIGURE 9
-
Progressive decrease in maximum velocity of shortening as a
function of load compared in canine atrial and ventricular
trabeculae at Lmas. At low loads, the velocity of shortening of an
atrial trabecula was about four times that of a ventricular
trabecula.
TIME TO MAXIMUM SHORTENING AND DURATION OF ISOTONIC
CONTRACTIONS
In both atrial and ventricular trabeculae, an
increase in load from 0.5 to 1.5 g did not significantly change the time to maximum shortening. At
all loads studied, the time to maximum shortening
of an atrial muscle was approximately half that of a
ventricular trabecula. In both specimens, the duration of isotonic contraction increased with load. At
any load studied, the duration of an atrial contraction was significantly briefer (P < 0.01) than the
duration of a ventricular contraction.
Circulation Research, Vol. 37, December 1975
V
Rate: 12 Beats/Minute
N-
3
Temp: 25°C
0.8
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y == 1.05 -- 0.44x
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values of 111 msec for the atrium and 170 msec for
the ventricle, which closely approximate (within
4% and 12%, respectively) the values representing
the time needed by the muscles to reach their
maximum rates of tension rise. At Lmax in both
atrial and ventricular trabeculae, the time to
maximum rate of tension rise during an isometric
contraction thus allows a good estimate of the time
to maximum velocity of shortening in an unloaded
isotonic contraction.
1.0
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Ventricle
\ °
0.4
y = 0.31 -- 0.12x
= 0.99
r
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Temp: 25°C
One well-known property of atria is their
distensibility. In fact, recent investigations in the
frog have shown that sarcomere lengths up to 3.5/u
can readily be obtained when an appropriate
stretch is applied to atrial trabeculae (24, 28, 29).
We can now consider whether canine atria have
comparable sarcomere properties. The present
study demonstrates that canine right ventricular
muscle clearly offers far greater resistance to
stretch than does canine right atrial muscle, since
at L max the former has undergone only about twothirds of the elongation of the latter.
One of the most distinctive features of the
contractile performance of right atrial trabeculae
was that they achieved the same developed and
total tensions in a much shorter time than did
ventricular trabeculae. One might speculate that
the slower development of tension characteristic of
the contraction of a ventricular trabecula is due to
a different anatomical arrangement of the myofibers. However, it also could reflect a functional
difference, such as a faster rate of appearance of
active sites in atrial trabeculae. In both muscle
\
'0.2
1
0
0.5
1.0
1.5
2.0
2.5
Load in g/mm 2
FIGURE 10
Comparison between the force-velocity curves of canine right
atrial and right ventricular trabeculae at Lmax. Linear extrapolations (dotted lines) demonstrate that Vmax in this atrial
trabecula was about four times that in its ventricular counterpart.
770
URTHALER. WALKER. HEFNER, JAMES
350
Rate: 12 Beats/Minute
300
Temp: 25°C
250
200
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Ventricle
I 150
100
Atrium
•
0.5
y = 111 + 46x
r = 0.82
1.0
Load in g/mm
1.5
2
FIGURE 11
Progressive increase in time to maximum velocity of shortening
as a function of increased load compared in canine atrial and
ventricular trabeculae at Lmai. Even at very low loads the time
to maximum velocity of shortening in ventricular trabeculae was
still about 40% longer than that measured in atrial trabeculae.
groups, the maximum developed tension averaged
approximately 2.5 g/mm2. This relatively low developed tension was due to the fact that we chose a
lower concentration of calcium than that used in
previous study (26). However, the 1.25 mmoles/
liter of calcium utilized in the present study closely
corresponds to the ionized calcium fraction of
canine and human blood. The amount of developed
tension observed was about half that measured in
cats by utilizing 2.50 mmoles/liter of calcium (26).
Although the amount of shortening accomplished by atrial muscle at any given load in excess
of 1.5 g/mm2 was not significantly different from
the shortening measured in the ventricular muscle,
at any load the time to maximum shortening was
significantly briefer in the atrium. At any given
initial muscle length, the maximum rate of tension
rise in the atrium amounted to at least twice the
value measured in the ventricle. At any given load
from 0.5 to 1.5 g/mm2, the maximum velocity of
shortening was significantly greater in the atrium,
and Vmax of an atrial trabecula was about four
times that of a ventricular trabecula. These results
collectively indicate that the contractile performance of a right atrial muscle from the appendage is
in many respects superior to that of a right ventricular apical trabecula.
It is possible that some of the differences between atrial and ventricular muscle found in this
study, such as the greater velocities and briefer
durations in the atrial muscle, are due to the
greater concentration of norepinephrine normally
found in atrial muscle (30). This difference, however, cannot account for the differences noted in
the amount of stretch required to reach L max . It
should also be noted that, since the present study
used only young dogs, it is possible that some or all
of the observed differences are due simply to
differences in the maturation rate between the
atrium and the ventricle. Developed force (31) and
maximum velocity of shortening (32) do increase
with age in certain mammalian species.
Since under normal conditions atrial contractions not only precede but ideally should be completed by the time of onset of ventricular contractions, one would teleologically reason that the time
course of atrial mechanical events must be of brief
duration. But the magnitude of shortening and the
amount of tension developed by our atrial trabeculae are such that one of the most obvious questions
from this study is whether the right atrial appendage is really only a contractile appendix or has
some other important physiological function yet to
be defined.
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Circ Res. 1975;37:762-771
doi: 10.1161/01.RES.37.6.762
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