Contribution of Plastoelasticity
to the Tone of the Cat Portal Vein
By Robert S. Alexander
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ABSTRACT
Isolated helical strips of cat portal vein were subjected to sudden stresses to
produce immediate elastic extension followed by a slow plastoelastic extension
or "creep." Recovery from this creep was evaluated by restretching with varying
intervals between stretches. In appropriately stimulated vessels, significant
creep recovery continues for periods in excess of 20 minutes. Both the rate and
the ultimate magnitude of the creep recovery were substantially increased by
contractile activity produced by norepinephrine or electrical stimulation. The
rate and ultimate magnitude of creep recovery were decreased by dilator drugs,
although some recovery persisted. The only factors found capable of blocking
creep recovery were complete inactivation of the contractile machinery by
removal of calcium from the system or maintainence of tension on the tissue
during the recovery period. This behavior is explained by a model in which
contracted elements are capable of slowly converting into a stable shortened
configuration capable of passively maintaining venous tone until mechanical
stress causes a plastoelastic extension to the longer configuration.
KEY WORDS
creep of veins
biomechanics
blood vessels
rheology of venous tissue
• Galen first defined muscle tone as the state
in which muscles "are active while not
appearing to move in the least" (1). In the
case of skeletal muscle, the intuitive insight of
Galen has been amply confirmed with the
demonstration that tonic contractions are
produced by the statistical fusion of discrete
randomized twitches of individual motor
units. Bozler (2) presented the thesis that
smooth muscle tone could be explained on the
same basis, and subsequent electrophysiological studies have provided incontrovertible
evidence of this mechanism in many smooth
muscle organs, including blood vessels (3, 4).
A number of observations, however, have
justified the question whether twitch fusion is
the sole basis for tone in smooth muscle.
Conspicuous among these is the fact that
sustained tone often correlates poorly with
phasic contractile activity. Also, in contrast to
From the Department of Physiology, Albany
Medical College, Albany, New York 12208.
This work was supported by a grant from the
National Science Foundation.
Received November 20, 1970. Accepted for
publication February 2,1971.
Circulation Research, Vol. XXV1U, April 1SI71
contraction of veins
smooth muscle tone
skeletal muscle which becomes completely
flaccid when isolated from sources of stimulation, smooth muscle usually exhibits maximal
tone in the spasm observed in freshly isolated
tissues.
Another possible mechanism for vascular
tone is suggested by analogy with the anterior
bysus retractor muscle of the clam, which
appears to have a distinct contractile protein
responsible for the "catch" contractions in
addition to the conventional phasic contractile
machinery (5). Claims that a protein capable
of such a function can be extracted from the
carotid arteries (6) must apparently be
discounted as an artifact of the extraction
procedure (7). We have attempted another
test of this hypothesis by examining the
precise changes in mechanical properties
induced by a wide spectrum of vasoactive
agents, on the assumption that if there were
two types of contractile elements, they should
have distinguishable mechancial characteristics. Although certain ions can produce quantitative alterations in the mechanical properties of veins (8, 9), no evidence was obtained
of a distinctively different mechanical behavior
461
462
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than that observed with the common vasoactive agents (10).
A third possibility is the existence within the
same contractile machinery of two modes of
mechanical action. Stacy (11), conceptualizing the contractile process as the conversion of
long elements to short elements, has pointed
out that both chemical and mechanical factors
can influence the kinetics of this conversion,
but with quite different time constants. In the
carotid artery, the mechanical effect of stress
on the short to long conversion appears to act
several orders of magnitude more slowly than
does the phasic conversion due to chemical
activation. A number of years ago, we
demonstrated in the mesenteric venous bed of
the dog that the recovery from mechanical
stretch followed a time course extending for
some 20 minutes (12) and further observed
that the rate of this recovery could be
influenced by drugs (13). Since such phenomena deal with very slowly reversible changes
which are dependent on applied tension
rather than on rate of stretch (14), we have
characterized them as plastoelastic (15).
Recently, Meiss (16) observed similar prolonged changes in the mechanical properties
of intestinal muscle.
The present study was designed to analyze
this phenomenon in greater detail. The
simplest and most accurate method of evaluating this property would seem to be the
measurement of creep observed after sudden
loading of the tissue, inasmuch as in most
tissues, including the carotid artery (11), a
significant portion of the creep proceeds
linearly when plotted as a function of the
logarithm of time. Unfortunately, log-time
linearity was not found to be characteristic of
venous creep. Nevertheless, the technique
yielded clear indications of a mechanical
transformation with a long time constant. This
analysis thus affords positive confirmations by
an essentially independent technique of the
phenomena that had been suggested by our
earlier analysis of hysteresis loops generated
by dynamic stretch cycles.
Methods
The experimental arrangement was conven-
ALEXANDER
tional in most respects. Portal vein segments were
removed from anesthetized cats and cut into
helical strips approximately 2 cm long and 0.5 cm
wide, as previously described (10). Metal skin
clips werefirmlyattached to each end. They were
then transferred into a constant temperature bath
at 36°C Our standard tissue bath solution
contains, in mM: Na, 137; K, 5.9; Ca, 2.5; Mg,
0.6; Cl, 117; HCO3, 25; PO4, 1.2; SO4, 0.6,
glucose, 10. In all experiments in which it was
not necessary to preserve electrical excitability of
the tissue, phasic activity was blocked by a
depolarizing solution whose composition was
identical to the above except that K was
increased to 75 mM and the Na correspondingly
reduced to 62 mM. Solutions were well aerated
with a mixture of 95% O2 and 5% CO,.
The skin clip at the lower end of the strip was
attached to a stainless steel hook which communicated to a Statham force transducer through a lax
rubber diaphragm sealing the bottom of the
chamber. The clip at the upper end of the vein
strip was similarly connected by a steel wire to
the arm of a Harvard isotonic muscle transducer.
Although this transducer is inherently nonlinear
because of its translation of linear motion to radial
motion, its infinite resolution and extremely low
noise permitted high gain amplification of
tangential motion over a very small arc so that no
measurable nonlinearity could be detected in the
calibrations. Compliance of the system with a steel
wire substituted for the vein strip was 0.005
mm/g.
To study creep, moderate loads were suddenly
applied to the vein strip. These loads were in the
form of brass weights hung on an extension of the
isotonic lever arm on the side of the fulcrum
opposite to the point of tissue attachment. For
veins from full grown cats, an effective load of 12
g was empirically selected as suitable; an 8-g load
was used for veins from younger cats. These loads
were achieved by drilling out the weights to
correct for the mechanical advantage of the lever
arm and the effective mass of the lever. To permit
sudden loading of the tissue with minimal
mechanical inertia, a small solenoid was mounted
on the transducer case which, when actuated,
held the loaded lever against a stop. The system
was adjusted so that when the lever was against
this stop, the strip was just lax enough to avoid
any tension development during creep recovery.
Deactivation of the solenoid then resulted in
sudden tissue loading with minimum overshoot of
tension or length. Recordings of tension and
length were obtained with a Hathaway oscillograph.
The interest in this study was to determine the
rate of recovery from the creep. Since the creep
was found to be over 9595 complete within 20
Circulation Research, Vol. XXVIII,
April
1971
463
PLASTOELASTICITY AND VENOUS TONE
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Creep
Recovery
A
FIGURE 1
Schematic representation of the technique for indirect assessment of creep recovery as described in text; not to scale.
seconds, load applications of 20 seconds were
selected as the standard stretch. To maximize
creep recovery, it was necessary to have the tissue
completely unloaded during the recovery phase.
This vitiated a direct measurement of creep
recovery, since it is not feasible to measure length
changes accurately in a lax tissue. Recognition of
this problem had been anticipated in the solenoid
arrangement described above, which prohibited
length measurements during the unloaded interval
while the lever was held against the stop. An indirect measurement of creep recovery is readily
achieved by reloading the tissue, as illustrated in
Figure 1. The dashed lines in the lower portion of
this figure indicate the portion of the length
changes which could not be recorded. Following
an initial 20-second period of loading, unloading
the tissue will produce an initial elastic retraction,
followed by a slow creep recovery. If the tissue is
restretched after a short period of recovery (A),
the degree of creep recovery (a) should be
indicated by the point that creep is again
initiated by restretching (a')- If a longer period
of recovery is allowed before restretching (B),
the greater degree of creep recovery (b) should
cause a corresponding shift in the loading curve
(b'). The creep observed on reloading the tissue
should, therefore, indicate the degree of creep
recovery during the unloaded interval. To
measure this creep recovery in time, a precise
sequence of stretches was imposed with recovery
times between successive stretches varying from
0.1 to 10 minutes, or in a few experiments to 30
minutes. Long recovery intervals were alternated
with short recovery intervals to avoid bias in the
data.
Two technical problems are encountered in the
analysis of such records. A slight residual
overshoot persisted, which the solenoid loading
technique did not completely eliminate. This
overshoot had dissipated within less than 0.1
seconds of the moment of stretch (Fig. 2). Of
greater importance was the fact that sudden
stretching of a blood vessel evokes a contractile
response (17). The simplest way to eliminate this
was to depolarize the preparation in a high K
solution, in which there was no evidence of
such a contractile response to stretch. In
experiments in which it was necessary to
use the standard solution, contractile activity
was usually evident in an undulation of the length
recording. This undulation appeared as a shortening of the vein starting 0.3 to 0.4 seconds after
the moment of stretch. It was therefore felt that
measurements taken 0.1 seconds after the moment of stretch would avoid die loading artifact
and still precede the contractile response to
stretch. As is evident in Figure 3, the creep
recordings did not demonstrate a log-time
relationship, so that most determinations were
confined to the 0.1-second and 20-second measurements, and the region of the curves where
contractile response to stretch would be manifest
are not included in the analysis of the data. All
results reported here were confirmed with a
minimum of six experiments distributed between
at least three venous strips.
Results
Figure 3 illustrates creep curves obtained
from an experiment in which a supramaximal
Circulation Research, Vol. XXVUI, April
1971
464
ALEXANDER
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FIGURE 2
Initial segment of an original recording showing the
effect of adding an 8 g-load to a strip of cat portal
vein.
dose of 1 fig/ml of norepinephrine was added
to the bath, an additional dose of 0.5 yu.g/ml
being added every 5 minutes to ensure that
supramaximal stimulation was maintained.
The bath in this case contained the depolarizing solution with potassium as the dominant
cation. This not only blocked any active
contraction in response to the sudden stretch,
but also would eliminate random twitch fusion
as an explanation for the tone observed in the
tissue. For each curve, the recovery time in
minutes from the end of the preceding stretch
is indicated. Creep was progressively greater
as longer periods of recovery from the
previous stretch were allowed. Significant
recovery continued in appropriately stimulated preparations for 10 minutes, with some
additional recovery at 20 minutes. Attempts to
extend the recovery period to 30 minutes gave
some suggestion of a small amount of further
recovery, although there was no statistical
reliability in the data beyond 20 minutes,
presumably because of the difficulty in maintaining the preparation at a constant level of
stimulation for such prolonged periods.
Since most of the creep recovery occurred
within the first 10 minutes, we elected to
confine our routine observations to this 10minute interval to facilitate the maintenance
of a constant state of the tissue. It should be
appreciated that even with this abridgment,
the sequence of stretches employed to measure the course of creep recovery for 10
minutes required approximately 22 minutes. It
did not appear feasible to normalize the data
in terms of absolute units of stress and strain
because of difficulties in measuring the
effective strip dimensions, especially in view
of the variation in strip thickness which was
found to average 0.07 mm at the intestinal end
and 0.10 mm at the hepatic end. The data
were therefore normalized by defining creep
recovery for the 10-minute interval under
maximal stimulation as 100% and expressing all
data in reference to this maximum. The creep
recoveries were plotted on a log-time scale as
a convenient method for telescoping the
abscissa.
Figure 4 presents a comparison of the creep
recovery observed in the depolarizing solution
alone, after the addition of a supramaximal
dose of norepinephrine, and after a supramaximal dose of isoproterenol. The control creep
recovery is substantially less than with norepinephrine stimulation and becomes still less
with exposure to the dilator drug. It should be
noted, nevertheless, that some recovery was
Creep curves recorded from a portal vein strip loaded
with 12 g while in a depolarizing solution containing
a supramaximal dose of norepinephrine. Numbers associated with each curve designate the time in minutes
for recovery from the previous stretch.
Circulation Research, Vol. XXV1I1, April
1971
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PLASTOELASTICITY AND VENOUS TONE
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the representative experiment shown in Figure
5 makes it clear that electrical stimulation is
similarly capable of accelerating creep recovery. Between stimulation runs, the strip was
subjected to an anesthetizing dose of procaine
(5 mg/ml). This made the strip refractory to
electrical stimulation and served to lower its
tone appreciably as measured by the rate of
creep recovery. Once again, however, some
creep recovery persisted in spite of the
marked reduction in tone produced by the
anesthesia.
Since it is probable that the contractile
machinery is involved in creep recovery, it
was of interest to determine the effect of
blocking all contractile activity. This was
achieved by changing the bath to a calciumfree solution containing 5 HIM Na-ethyleneglycol bis (/3-aminoethylether) -N,N'-tetr aacetic
-100
/
NOREP
Creep recoveries in a depolarizing solution (control);
after addition of 1 fig/ml of norepinephrine; and after
2 ng/ml of isoproterenol.
still observed in the presence of a rather
massive dose of the dilator agent.
To assess whether electrical stimulation
could effectively duplicate the action of
chemical stimulation, another type of experiment was carried out which required use of
the standard solution with Na as the dominant
cation to preserve tissue excitability. Fine
stimulating wires were connected to the metal
skin clips clamping the opposite ends of the
strip, and during the intervals between
stretches, the strip was subjected to just
maximal electrical shocks (30-msec pulses of
10 v) delivered once per second. Stimulation
was terminated 15 seconds prior to the
following stretch to allow for phasic relaxation
from the stimulus prior to stretching. Although it was not found possible to obtain as
reproducible results in the standard solution,
Circulation Research, Vol. XXV1I1,
April
1971
/
STIM
-75
/
*
CONTROL
1^50
y
PROCAINE
^
0.1
~
.MINUTES
1.0
1
FIGURE 5
Creep recoveries in standard salt solution (control); in
1 )ig/ml of norepinephrine; with electrical stimulation
during recovery period; and in procaine hydrochloride
(5 mg/ml).
466
ALEXANDER
length of the strip during the recovery interval
while the transducer lever arm was held
against the fixed stop. As this strip length was
increased, creep recovery led to the development of measurable tension in the strip prior
to stretch. Although in all cases some creep
recovery was observed in the first 30 seconds,
the continuation of any significant creep
recovery beyond this initial phase was inhibited if significant tension developed in the tissue
(Fig. 7).
-100
/ S
EPI
/
-75
/
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-50
Discussion
/
CONTROL
•
•
/
^
^
_
,
0.1
»-
Co FREE
•—"_ - - •
MINUTES
1.0
1
10
1
FIGURE 6
Creep recoveries in a depolarizing solution containing
2.5 VIM Ca2+ (control) compared with recovery with
epinephrine stimulation (1 ng/ml) and a calcium-free
solution to which the vein had been equilibrated for
20 minutes.
acid (EGTA). Previous experience (8) has
shown that 20-minute exposure to such a
solution almost totally eliminates the plastoelastic behavior of portal vein strips. Under
such circumstances, a small amount of creep
recovery was observed for the first 30 seconds,
but in no experiment was any significant creep
recovery observed beyond the first minute
when calcium had been removed from the
system (Fig. 6).
In all of the foregoing experiments, the vein
was maintained in a completely lax condition
during the recovery between stretches on the
assumption that this would maximize the
recovery. To confirm this assumption, the vein
strips were stretched by identical loading
sequences, but between each series the length
transducer was raised so as to increase the
This study confirms the existence of a
prolonged mechanical recovery in venous
tissue following a period of stretch. When
converted to equivalent pressures, the wall
tensions produced by these loadings would
correspond with portal vein pressures on the
order of 20 to 30 mm Hg. Such pressures are
within the upper limit of the functional range
over which the portal vein operates, and
hence these mechanical changes would appear
to be physiologically relevant. The reversibility of the phenomenon would argue against
tissue damage as an explanation for the
observed effects.
Creep recoveries of a portal vein segment in depolarizing solution held at different lengths during the unloaded recovery period as indicated by the numbers to
the right of each curve. At 19 mm, no tension was
developed during creep recovery, at 21 mm, tension
of 0.2 g first developed after 1 minute of recovery and
rose to 0.6 g after 10 minutes of recovery; at 23 mm,
0.5 g of tension developed after 0.5 minutes of recovery and rose to 0.8 g after 10 minutes; at 25 mm,
a tension of 2.0 g developed after 0.1 minutes of recovery and rose to 3.1 g after 10 minutes of recovery.
Tissue length after 20 seconds of creep with an 8-g
load averaged 28.3 mm.
Circulation Research, Vol. XXVIII, April
1971
PLASTOELASTICITY AND VENOUS TONE
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The data indicated some random errors
which prevented a precise characterization of
the creep recovery curves. This presumably
reflects a failure to achieve absolutely constant
vascular tone throughout the interval required
to assess creep recovery. Attempts to improve
the results with drug application by use of a
flow-through perfusion technique were not
successful, perhaps because of the significant
dead space (75 ml) of the muscle bath. In the
electrical stimulation experiments, there may
have been variable degrees of residual contraction in the tissue at the moment of the test
stretch. Such random errors, however, cannot
explain the overall trend of the creep recovery
curves over the significant time intervals
involved in these determinations.
We know of no previously recognized
contraction process of vascular smooth muscle
which demonstrates the time course of the
creep recoveries observed in these experiments. When recorded in the conventional
fashion, the contractile response of the portal
vein to electrical stimulation by the technique
employed in this study reached its maximum
in 15 seconds; we have never observed
intervals in excess of 1 minute for drugs such
as norepinephrine to produce maximal contraction. Creep recoveries continuing in excess
of 10 minutes represent a different order of
magnitude than the usual contractile process.
Another distinction between creep recovery
and phasic contractile behavior is the action of
dilator drugs. Even though such agents as
isoproterenol and procaine are potent relaxers
of venous smooth muscle, some creep recovery
persisted in the presence of these agents,
albeit at a slower rate. Except for the calciumfree experiments, in which presumably an
essential component of the contractile machinery had been removed, some degree of
creep recovery was observed even in the
presence of agents that block phasic contractile activity.
The latter observation might prompt the
inquiry as to whether the agents employed
were simply altering the rate of creep recovery
and whether, given sufficient time, complete
creep recovery would have been observed in
Circulation Research, Vol. XXVlll,
April
1971
467
all situations. The data did not support this
assumption. Of the initial control runs in the
12 vein segments studied, four showed a slight
increase in creep recovery during the 5-minute
to 10-minute interval, five showed a small
decrease, and three showed no measurable
change. For the unstimulated preparation,
there was therefore no statistically significant
increase in creep recovery during the last 5
minutes. As stated earlier, extending the
recovery significantly beyond 10 minutes
would not improve the statistical accuracy
because of the difficulty of maintaining the
preparation in a steady state. It seems
justifiable to conclude, therefore, that stimulating agents have two actions on creep
recovery: to increase its rate and to increase
its ultimate magnitude.
To provide a frame of reference for dealing
with this phenomenon, we would extend the
postulates developed by Buchthal and Kaiser
(18), Polissar (19), and Stacy (11) which
have approached the analysis of the contractile machine in terms of the conversion of long
(L) elements to short (S) elements. We assume two forms for the shortened element,
S' and S:
L
-
S1
Tension^
S' would represent the activated state of the
contractile elements responsible for the usual
phasic contractions. In the unstimulated muscle, the conversion between L and S' heavily
favors the L form, although a finite tendency
for the L to S' conversion persists. The slow
plastoelastic transformation is represented by
the secondary conversion of S' to S. S is regarded as a relatively stable configuration of
the short element except that it is readily susceptible to being converted back to L when
the system is mechanically stressed. This S to L
conversion with externally applied tension
represents creep. Creep recovery requires the
net conversion of L back to S via the S' intermediate. Although the S' to S conversion is the
468
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rate-limiting step, any agent which increases
the population of S' elements, such as chemical
or electrical stimulants, should increase the formation of S. Assumption of a low spontaneous
rate of S to L conversions could explain the
fact that unstimulated tissues can never
achieve maximal creep recovery, since their
recovery would be terminated when the
concentration of S elements had risen to the
point that spontaneous S to L conversions
occurred at the same rate as the L to S' to S
conversions.
Several variations on the scheme above are
equally plausible. Its important component,
however, is the assumption of two possible
states of the shortened contractile elements,
one of which is the labile product of
contractile activation, while the other represents a plastoelastic "set." It is not within the
scope of this presentation to speculate on the
molecular basis of the difference between S'
and S. In general terms, it could represent the
presence or absence of some plasticizing
component at the contractile linkages, or it
could represent the formation of some type of
secondary linkage in the structure. In either
case, an auxiliary "tone" mechanism would be
involved capable of adjusting vascular dimensions without continuous expenditure of
energy.
The scheme outlined would not appear to be
restricted to venous smooth muscle. Meiss
(16) has observed a prolonged augmentation
of stretch resistance following stimulation of
intestinal smooth muscle (i.e., an increased
formation of the S form) which could be dissipated by mechanical stretch. Similar phenomena have been observed in the bladder,
where creep recovery is slowed but not
blocked by the absence of contractile activity
(20).
Whatever its ultimate explanation may be,
it would seem evident that this plastoelastic
property of vascular smooth muscle, operating
over a much longer time course than active
contraction, has the potentiality to contribute
to the phenomenon of vascular tone. The tonic
contraction associated with the fusion of
active twitches of contractile elements will
ALEXANDER
secondarily increase the population of S
elements and hence introduce a passive
contribution to the maintenance of vascular
tone. It is passive in the sense that, insofar as
the population of S elements is increased, the
necessity for a continuing energy supply to
maintain L to S' conversions will be reduced.
In the reservoir function of the venous system,
this interaction should lead to significant
economies of the energy required to mobilize
venous return to the heart. When circumstances have created sustained venomotor
activity to constrict down the venous reservoirs, the plastoelastic set of the veins will
make them able to maintain the constriction
without further energy expenditure. This
passive constriction will persist until sufficient
pressure develops over a long enough time
interval to force creepage of the venous bed
back toward its original volume. Changes in
intracellular calcium (8) or intracellular pH
(9) can further modulate this plastoelastic
behavior. Although twitch fusion would remain as the primary mechanism of venous
tone, this plastoelastic reinforcement appears
capable of serving a significant auxiliary
role.
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Contribution of Plastoelasticity to the Tone of the Cat Portal Vein
ROBERT S. ALEXANDER
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Circ Res. 1971;28:461-469
doi: 10.1161/01.RES.28.4.461
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