Influence of Blood Temperature on the
Pulmonary Circulation
By
PIERRE M. GALLETTI, M.D.,
P H . D . , PETEB F .
AND ANDRE RIEBEN,
SAUSBURT, M.D.,
PH.D.
B.S.
Innervated, nourished and ventilated dog lungs were perfused in situ with a technic
which afforded adequate control of blood flow, pressures, pH and temperature. Variiitions of the pulmonary (but not of the systemic) blood temperature was followed by
pronounced changes of the pulmonary vascular resistance, believed to be attributable to
pulmonary vasomotion.
D
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into a femoral artery. In this preparation the
pump-gas exchange machine supplies all systemic blood circuits; the pulmonary circulation
is separated from the systemic circulation except
for collateral blood flow to the lungs via bronchial vessels.
Pressures were recorded in the abdominal aorta,
inferior vena cava, pulmonary artery, pulmonary
vein and upper airways with plastic cannulas connected to strain gages, amplifiers and a multichannel direct-writing oscillograph. Flows in both
circuits were varied independently by means of
calibrated pumps. The temperatures of the gasexchange unit and of the blood reservoirs were
controlled. A mercury thermometer and pH electrodes with automatic temperature compensation
were exposed to the blood flowing through a plastic chamber. The pH of the main circulation was
monitored and corrected when necessary by infusion of sodium bicarbonate solution. To avoid
changes of pH in the pulmonary perfusion blood
due to open-circuit ventilation, the lungs were
rhythmically inflated under positive pressure with
an automatically driven rebreathing bag. Special
care was taken to maintain the rectal temperature within the normal range (36 to 38 C.)
throughout the experiment. Collateral blood flow
to the lungs was measured by a previously described method1 when steady conditions were
reached.
At the beginning of each experiment, the flowpressure relationships were studied over a wide
range of pulmonary blood flows with both circulations at normal temperatures. With constant
pulmonary flow, changes of pulmonary blood
temperature of a magnitude of 4 to 20 C. were
then produced within 20 to 40 sec. by connection
of alternative reservoirs with symmetric inflows
and outflows while the systemic perfusion system
remained at normal temperature. Changes of the
pulmonary blood temperature in either direction
usually caused acute rises of the pulmonary artery pressure which returned to an intermediate
URING physiologic studies of total body
perfusion we encountered unexpected
fluctuations of pulmonary vascular pressures
which apparently were related to changes of
the blood temperature. The literature does
not describe adequately controlled experiments concerned with the effect of blood temperature on pulmonary hemodynaniics. We
therefore devised and investigated a preparation in which the innervated, ventilated and
nourished dog lungs were perfused in situ
and in which we analyzed the temperature
factor with minimal interference by other
major variables affecting the pulmonary circulation (pulmonary and systemic blood flow,
ventilatory pressure, composition of alveolar
gas, pH of the circulating blood).
METHODS
In our preparation* blood from one of the several alternative reservoirs was pumped into the
pulmonary artery through a cannula; blood collected from another cannula in the apex of the
left ventricle was returned to the reservoir. The
ascending aorta was clamped off and the root of
the pulmonary artery w a s tied. All systemic venous blood was withdrawn from the right ventricle,
arterialized in a heart-lung machine and pumped
From the Institute for Medical Besearch, Cedars
of Lebanon Hospital, Los Angeles, Calif.
Supported in part by grant H-1158 from the
National Heart Institute, U. S. Public Health Service
and by a grant of the Los Angeles County Tuberculosis and Health Association.
Received for publication December 20, 1957.
*Dogs were anesthetized with pentobarbital, 25 mg./
Kg. (not with 5 mg./Kg. as erroneously reported
earlier1) curarized with tubocurarine 0.4 mg./Kg.
and heparinized with 2 mg./Kg.
275
Circulation Retarch, Vol*m4 VI. May 1918
GALLETTI, SALISBURY AND RIEBEN
276
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Fi0. 1. Dog 11.7 Kg., open chest, positive pressure
breathing. PAP, pulmonary arterial pressure; PVP,
pulmonary venous pressure; SAP, systemic arterial
pressure. The blood flow was kept constant throughout
the experiment. At the arrow the pulmonary vascular
bed was perfused with blood from a low temperature
reservoir (temperature in F.).
value after some minutes. After a new steady
state was reached, the flow-pressure relationships
were again studied over the same range of flows
as before. Hemodynamic studies were usually performed a 4 different temperature levels between
37 and 15 C.: the pulmonary blood temperature
was then returned to the normal value for control purposes. At the end of some experiments,
the effect of hyperthermic blood (40 to 42 C.)
was observed; in other experiments the pulmonary
perfusion blood was replaced with saline.
In another series of experiments, the pulmonary
blood temperature was kept constant at 37 C.
while the blood in the systemic circulation was refrigerated. Replacement of the temperature control of the pump-oxygenator with a cooling device
resulted in a fall of the blood and the rectal
temperatures from 37 to about 28 C. within 10
min. When refrigeration was discontinued and
normal conditions were re-established, the rectal
temperature returned to normal within 20 to 30
min.
RESULTS
Effect of Sudden Changes of Pulmonary
Blood Temperature on Pulmonary Vascular
Pressures. During each series of observations
in one animal the variables pertaining to the
systemic perfusion were kept within a very
narrow range of variation. However, the
systemic circulation varied between individual
animals (now 60 to 80 ml./min./Kg., mean
systemic arterial pressure 60 to 140 mm. Hg,
central venous pressure 2 to 6 mm. Hg, systemic arterial pH 7.30 to 7.45, rectal temperature 36 to 38 C ) . The pulmonary
perfusion pump was set at constant flows
ranging from 21 to 73 ml./min./Kg. and the
pulmonary vascular pressures were registered
for at least 5 min. under constant conditions
of pulmonary pH and temperature. The
temperature in the pulmonary circulation was
then suddenly modified by perfusing the lungs
with the blood from a low-temperature reservoir. The maximal change of the pulmonary artery pressure was generally observed within 30 to 45 sec.; it was followed
in some instances by stabilization of the pulmonary artery pressure at an intermediate
value after 3 to 5 min. perfusion while the
increase of the pulmonary venous pressure
was inconstant and insignificant (fig. 1). This
overshooting effect was more pronounced at
higher flows.
Pulmonary blood temperature was reduced
to 3 levels: 30 to 31 C, 24 to 25 C, and 15
to 18 C. Elevation of the pulmonary artery
pressure without significant simultaneous increase in. pulmonary venous pressure was consistently observed in 29 experiments in 10
dogs. A correlation between the pulmonary
artery pressure response and the pulmonary
blood flow at the time of the temperature
change was not evident.
When the studies at the lowest temperature
level were completed (17 to 25 C ) , the temperature was brought back to about 35 C.
The blood reservoir used for rewarming purposes was set at 37 C. and the system returned
to normal blood temperature in 6 to 10 min.
In all 13 experiments (10 dogs), the pulmonary artery pressure slowly decreased on
rewarming while the pulmonary venous pressure fall was inconsistent. The pressure
variations were asymptotic in nature and some
arbitrary point had to be chosen to characterize the effect of rewarming.
BLOOD TEMPERATURE AXD LUXG CIRCULATION
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All changes of blood temperature were
performed at constant and undisturbed flow
and with blood of the same protein content
and hematoerit value. The variations of the
pulmonary vascular pressures can therefore
be expressed in terms of total pulmonary
resistance. The results calculated during the
peak pressure variation (fig. 2) indicate increased resistance due to lowering the temperature of blood. The decreased resistance
values (bottom, fig. 2) refer to conditions
5 min. after the beginning of the perfusion
with warm blood; this point was selected because experience had shown that about 90
per cent of the resistance variation is completed at this time.
In 3 dogs, elevation of pulmonary blood
temperature (41 to 43 C.) caused a progressive increase of both pulmonar}' arterial and
venous pressures, and pulmonary edema. In
4 dogs, the blood in the pulmonary circuit
was washed out and replaced with saline or
Ringer solution of the same temperature.
Pulmonary artery and venous pressures both
fell, thus lowering pulmonary resistance to
about 50 per cent the initial value. Progressive contamination of the pulmonary circulation by the collateral blood flow prevented
constant composition of the perfusing fluid.
Delayed Effects of Changes of Pulmonary
Blood Temperature on Pulmonary Vascular
Pressures. The influence of pulmonary blood
temperature on flow-pressure relationships
was studied in 8 dogs. The pulmonary blood
flow was varied between 0 and 120 per cent
of the systemic flow (0 to 1500 ml ./min.). The
highest flows, however, could not always be
studied at the lowest temperature because of
the high pulmonary artery pressure which
might have damaged the preparation. The
pressure-flow curves were initiated at the
highest possible perfusion rate2 and subsequent points were obtained with stepwise
decreases of flow, each step being maintained
30 sec. Intermittent, positive-pressure ventilation was maintained at constant inflation
peaks throughout the experiment.
The shape of the flow-pressure curve obtained (fig. 3) is essentially similar to that
277
Fia. 2. Top. Effect of increasing the temperature
of the pulmonary perfusion blood (T, in degree O.) on
the pulmonary vascular resistance (PR).
Bottom.
Effect of decreasing the temperature of the pulmonary perfusion blood (T, in degree C.) on the pulmonary vascular resistance (PS).
described by previous authors for perfused
isolated lungs.Hi 4 The curve intercepts the
pressure axis at a positive value ranging from
1 to 3 mm. Hg at 37 C. AVith flows under
200 ml./min. the curve is convex to the pressure axis, with increasing flows it develops
a rectilinear portion characterized in the range
from 400 to 900 ml./min. by a slope of 1.0
(S.D. 0.16) mm. Hg per 100 ml./min. increase of flow. At the highest flows, the
curve sometimes shows a concavity toward
the pressure axis, so that the whole curve
is S-shaped. When the pulmonary blood
temperature is decreased, the pulmonary artery pressure at equivalent flow is increased,
thus the pressure-flow curve is displaced to
the left. The magnitude of shift is directly
related to the decrease of temperature. Below
24 C. the pressure axis intercept (2 to
4 mm. Hg), the convexity toward the pressure axis and the slope of the rectilinear
278
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Fio. 3 Top. Dog 19.0 Kg. Belationahip of the
pulmonary arterial pressure (PAP) and the pulmonary venous pressure (PVP) to flow in the pulmonary vascular bed perfused in situ. The lungs
were perfused with saline and blood at different
temperatures.
Fio. 4 Bottom. Same dog as figure 3. Kelationship of pulmonary vascular resistance (PR) to flow
in the pulmonary vascular bed. Note that the values
of PR at the beginning of the experiment ( • ) and
at the end ( O ) are practically undistinguishable when
taken at the same temperature.
portion (2.0 mm. Hg./lOO ml./min., S.D.
0.13) are definitely greater than at 37 C.
The pulmonary venous pressure increases
slightly from zero mm. Hg at zero flow to
8 mm. Hg at the highest flows. No significant difference related to temperature has
been observed in successful experiments when
the tone of the preparation after reversal of
the temperature conditions was found unchanged.
Variations of pulmonary resistance as a
function of the temperature of the perfusing
blood under steady conditions may be calculated from the data of the flow-pressure
curves. To avoid interference due to the
elastic stretch of the vascular bed by the
GALLETTI, SALISBURY AND RIBBEN
intraluminal pressure, isobaric conditions
must be selected. If one starts with the values
of flow and pulmonary venous pressure for
a pulmonary artery pressure of 15 mm. Hg
and takes the resultant pulmonary resistance,
at 37 C. «= 100 per cent, one finds an average
increase in resistance of 61 per cent at 30 C.
and 144 per cent at 15 C.
Determination of collateral flow to the lungs
showed no consistent correlation with the
temperature of the blood perfusing the lungs.
In 15 experiments where the temperature was
lowered and factors like systemic arterial and
venous pressure did not interfere with the
experimental conditions, the collateral flow
increased in 9, decreased in 3 and remained
unchanged in 3.
Influence of Systemic Blood Temperature
on the Pulmonary Vascular Pressures. In 5
dogs the systemic blood temperature was
lowered while the pulmonary circulation was
perfused at normal temperature. The rectal
temperature fell about 10 C. in 10 min. while
the pulmonary blood temperature usually fell
about 1 C. The pulmonarjr arterial and
venous pressures showed no significant
changes related to temperature variation of
the systemic blood (lowest rectal temperature 26 C.) when both systemic and pulmonary flows were maintained constant. After
observations were made at the lowest temperature in a steady state, the systemic circulation was slowly rewarmed. Xo noteworthy changes in pulmonary arterial or
venous pressures were observed during rewarming.
The systemic arterial pressure fell 10 to
30 mm. Hg almost immediately after starting
the systemic perfusion with cool blood; it
then rose slowly to a higher value than before
hypothermia. During rewarming a diphasic
change of the systemic arterial pressure opposite in direction occurred. The systemic
arterial pressure at the end of the experiment
was almost the same as at the beginning. The
systemic venous pressure did not show noteworthy changes. No attention was given to
possible changes in collateral blood flow to
the lungs.
BLOOD TEMPERATURE AND LUNG CIRCULATION
DISCUSSION
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Any attempt to identify mechanisms of
pulmonary vascular pressure changes must
distinguish between (a) active vasomotion and
(b) passive hemodynamic changes (redistribution of blood between systemic and pulmonary
circulation, back pressure from the left
atrium, altered bronchomotor tone, change of
physicocheniieal properties of the blood).
Our preparation excludes blood shifts from
the systemic circulation and changes in ventilatory or gas exchange patterns. However,
the changes of blood viscosity with temperature are expected to cause variations of the
pulmonary vascular pressures; this passive
effect must be differentiated from active pulmonary vasomotion.
Among previous authors Fiihner and Starling5 did not find any change of the pulmonary arterial or venous pressures in a
heart-lung preparation after lowering the
temperature by 11.5 C, but this observation
was made in only 1 dog which had received
pulmonary vasoconstrictor agents. Similarly
Sarnoff and Berglund2 found no change in
the distensibility of the pulmonary vascular
bed when the temperature of the perfusing
blood was decreased. Their lung preparation, however, was not considered to be living.
None of the numerous published investigations
of hemodyuamics during hypothermia or
fever permit deductions concerning the tonus
of pulmonary blood vessels, because far too
few variables were controlled and any given
result can be interpreted in many different
ways. For instance, Nahas et al.6 reported
a fall of pulmonary artery pressure in hypothermia, but the pulmonary blood flow and
the left atrial pressure were not measured
in their experiments, which therefore do not
permit conclusions about the effect of temperature on pulmonary resistance.
In our experiments the systemic or pulmonary blood temperatures were varied
independently of each other while other
factors which might influence pulmonary
vascular pressures (systemic and pulmonary
blood flow, pulmonary blood protein content,
hematoerit, ventilatory pressure, alveolar gas
279
composition) were kept constant. Cooling
the blood at constant carbon dioxide content
necessarily increases its pH.7 With relation
to the pulmonary circulation, this means that
we have to deal not only with the direct effect
of temperature change on blood viscosity and
possibly pulmonary vasomotion, but that the
direct effect of pH changes on blood viscosity
and hindrance of the pulrnonarv vascular bed
has to be considered.
There is no convincing evidence in the
literature that the pH is an important factor
of blood viscosity within the physiologic
range.8 An increase in carbon dioxide content
by bubbling gas through the blood, which
would scarcely fail to produce a pH drop, has
been associated with an increase of the blood
viscosity.9'10 On the other hand, changes in
the viscosity of whole blood following venous
stasis bear no demonstrable relation to the
carbon dioxide or oxygen content.11 Far more
important is the direct effect of blood pH
on the hindrance of pulmonary blood vessels.
It has been shown previously12 that an increase in pH is constantly associated with a
decrease of pulmonary vascular resistance.
This effect far outweighs the change in blood
viscosity (if any) due to the pH variation.
Since cooling the blood increases the pH,
the effect of temperature decrease through
pH displacement at constant carbon dioxide
content, as realized in our experiments, will
tend to dampen the increase in pulmonary
vascular resistance observed and will in no
case exert an additive effect to the phenomenon. The aging of the preparation did
not introduce an error since the initial and
final flow-resistance curves taken at the same
temperature were indistinguishable in successful experiments (fig. 4). The remarkable
stability of the pulmonary vasomotor tone
despite severe experimental interference with
pulmonary perfusion rates may be due to
the separation of the functional and the nutritive circulation in the lungs.
The different effects of cooling of the systemic and of the lesser circulation show that
the action of blood temperature on the pulmonary vascular pressures is local.
GALLETTI, SALISBURY AND RIEBEX
280
nv M i n d
Mood
3D
*£.
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DO
too
non
oo
MO
no
BOO
KM
FW
FIG. 5. Data of figure 3. Relationship of pulmonary
arterial pressure {PAP) to flow in the pulmonary vascular bed. Note the lineiir relationship between log
PAP and log F and the parallelism of the functions
at different temperatures nu<1 viscosity of the perfusate.
The increase in blood viscosity has been
said to range from 0.8 per cent9 to 2 per cent13
and even 3 per cent8 per degree centigrade
of cooling. The effect of pseudoplasticity of
blood in the narrow vessels on the temperature-viscosity function has not yet been investigated, but it is probably of little importance.u In our experiments the increase
of pulmonary resistance per degree of decrease in temperature averaged 5.2 per cent
in acute temperature variations. A change
of this magnitude cannot be explained by an
alteration of the viscosity factor alone, although viscosity contributes to the observed
phenomenon. Even under steady temperature conditions, the increase in pulmonary
resistance with decreased temperature cannot be explained in terms of viscosity changes.
This observation is not felt to contradict
previous studies of isolated denervated vascular beds15 where resistance changes were
completely explained by considerations of
viscosity: our lung preparation was not deprived of its nervous connections. Furthermore, considerations of blood viscosity could
not explain the changes of the pulmonary
artery pressure after sudden temperature
reductions where a pressure peak is followed
by stabilization of the pulmonary artery pres-
sure at an intermediate value, a response
which almost mimics intrapulmonary injection of a vasocoastrictor drug. Since we did
not attempt to measure the blood temperature
at the precapillary level, it is impossible to
exclude that the pulmonary artery pressure
peak was due to an "overshooting" of the
temperature change. On the other hand, such
a biphasic response to a unidirectional temperature change has been observed on isolated
arteries.16 "We believe that the decrease of
the temperature of the blood perfusing the
lungs causes pulmonary vasoconstriction.
Pulmonary artery pressure responses to
increase of the blood temperature from hypothermic values to normal can be explained
by changes in viscosity alone. The slow,
regular fall of the pulmonary artery pressure
with increasing temperature and also the
effect on resistance of 2.1 per cent per degree
rise, are arguments for a physical mechanism
rather than for a biologic one, although a
combination of both is possible. The slower
rate of temperature variation while rewarming could have lessened the vasomotor response, since it has been shown10'1T that
vasomotion is not manifest when the rate of
temperature change is above or below a critical value.
Hydrodynamic considerations on perfnsions in vivo and limitations of Poiseuille's
law when applied to blood flowing through
small vessels have been discussed extensively
in the last years.18"21 The effect of temperature on the pressure-flow relationship which
is described here is similar to changes seen
in other vascular beds after increasing the
hematocrit,22 after adding increasing amounts
of a vasoconstrictor drug,28 or after exciting
the sympathetic fibers with stimuli of increasing intensity.20 The positive-pressure
intercept with its arteriovenous pressure
gradient at zero-flow corresponds to a very
low "critical closing pressure. " The convexity
of the curve iu the low flow range is not explained by considerations of apparent viscosity and pseudoplastic flow because it was
observed to the same extent while perfusing
with saline or hemolyzed blood. The slope
BLOOD TEMPERATUBE AND LUNG CIRCULATION
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of the linear part of the function is in good
agreement with estimates derived from similar
preparations by other authors. This slope
increases when temperature decreases, but remains far less steep than in systemic vascular
beds. In some experiments where the flow
was increased above 1500 ml./min., the pulmonary artery pressure rose rapidly, thereby
giving to the upper part of the curve a curvature opposite in direction to the one observed
in the low flow range. In our preparation
the tip of the registration cannula in a lobar
branch of the left pulmonary artery pointed
"upstream." It is therefore not excluded that
at very high flows some of the kinetic energy
of the blood could be converted back into
potential energy, added to the "ideal" lateral
pressure reading and explaining the " S "
shape. A relative "stenosis" of our left
ventricular outflow would also cause a rise
of the pulmonary venous pressure and secondarily of the pulmonary artery pressure.
Our pressure-flow data are well described
by the empirical formula proposed by Green
et al.24 : F -= h PAP n where k and n are
constants for a particular hindrance and
blood (fig. 5). Considering that temperature
influences both vasomotor tone (hindrance)
and viscosity, it appears not possible at the
present time to decide whether this parallelism is significant or only the result of
opposing factors. Our data on the pulmonary
circulation are still too scarce to describe
the pressure-flow relationship in terms of
physical principles. The rapidly expanding
knowledge of non-Newtonian flow will contribute to future understanding of this
problem.
SUMMARY
Pulmonary arterial and venous pressures
were recorded in dog preparations in which
the systemic and pulmonary cimilations were
perfused separately and which afforded complete control of variables which are known
to influence pulmonary hemodynaniies. With
constant pulmonary blood flow, variations of
the pulmonary (but not of the systemic) blood
temperature were followed by pronounced
changes of the pulmonary arterial pressure,
281
believed to be attributable to pulmonary
vasomotion.
SUMMAKIO IX INTEKLIXGUA
Le pressiones pulmono-arterial e venose
esseva registrate in preparatos cauin in que
le circulationes systemic e pulmonar esseva
perfundite separatemente e in que omne le
variabiles que exerce cognoscitemente un influentia super le hemodynamica poteva esser
regulate con complete libertate. In le presentia de un constante fluxo de sanguine pulmonar, variationes in le temperatura del
sanguine pulmonar—sed non in le temperatura del sanguine systemic—esseva sequite
per pronunciate alterationes del pression
pulmono-arterial. Es postulate que iste
phenomeno es attribuibile a vasomotion pulmonar.
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Influence of Blood Temperature on the Pulmonary Circulation
PIERRE M. GALLETTI, PETER F. SALISBURY and ANDRE RIEBEN
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Circ Res. 1958;6:275-282
doi: 10.1161/01.RES.6.3.275
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