Increases in Plasma Oncotic Pressure
During Acute Cardiogenic Pulmonary Edema
JAIME FIGUERAS, M.D., AND
SUMMARY Colloid osmotic pressure (COP) was measured in 95
patients with clinical and radiological evidence of acute cardiogenic
pulmonary edema. Fifty patients who were admitted for coronary
observation but in whom acute myocardial infarction was excluded,
and 21 patients who had sustained acute myocardial infarction
without evidence of left ventricular failure served as controls.
Significantly higher values of COP, total plasma protein, and
hematocrit were observed in patients with pulmonary edema. In-
creases in COP during pulmonary edema were best explained by
transudation of hypooncotic fluid into extravascular spaces. Follow-
IN CLINICAL STUDIES previously reported from this
unit,' acute cardiogenic pulmonary edema (PE) was related
either to increases in hydrostatic pulmonary capillary
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pressures in excess of plasma colloid osmotic pressure
(COP) or to the lowering of COP. The left ventricular filling
pressure alone was not a consistent indicator of the risk of
pulmonary edema. In addition to COP, alterations in tissue
hydrostatic pressure were recognized. The edema fluid which
accumulates in the interstitium and in alveoli in this type of
pulmonary edema is known to be low in protein content,
usually less than one-half of that observed in plasma.2
Since as much as 3 L of fluid may extravasate following
the onset of PE,3 hemoconcentration should be anticipated.
Consequently, the red cell fraction is likely to be increased.
If the extravasated fluid is lower in protein content than that
of circulating blood, the protein concentration and the
colloid osmotic pressure of plasma would be increased.
There is both experimental and clinical evidence of such in-
creases in hematocrit and plasma protein concentration
following onset of pulmonary edema.7 8
The purpose of the present study was to investigate
systematically these issues in patients following onset of
acute PE. Sequential changes in hematocrit, plasma
proteins, and COP were measured prior to and following
emergency treatment of PE which included oxygen,
morphine, and furosemide.
Methods
Patients
A total of 95 patients admitted to the University of
Southern California Center for the Critically Ill between
March 1972 and February 1975 were investigated. There
From the Shock Research Unit and Department of Medicine, University of
Southern California School of Medicine, the Los Angeles County/USC
Medical Center, and the Center for the Critically Ill, Hollywood Presbyterian
Medical Center, Los Angeles, California.
Supported by USPHS Research grants HL-05570 from the National
Heart, Lung, and Blood Institute, GM-16462 from the National Institute of
General Medical Sciences, ROI HS 01474 from the Health Resources Ad-
ministration, and by the Cardiopulmonary Laboratory Research Foundation
of Los Angeles, California.
Dr. Figueras is presently a Clinical Fellow, Department of Cardiology,
Cedars-Sinai Medical Center, Los Angeles, California.
Address for reprints: Max Harry Weil, M.D., Ph.D., Center for the
Critically Ill, University of Southern California School of Medicine, 1300 N.
Vermont Avenue, Los Angeles, California 90027.
Received March 4, 1976; revision accepted July 23, 1976.
MAX HARRY WEIL, M.D., PH.D.
ing treatment of pulmonary edema in 76 patients with furosemide,
morphine, and oxygen, pulmonary edema was reversed in 65 patients.
Reabsorption of hypooncotic fluid from extravascular sites with a
significant decline in COP, total protein and hematocrit followed
reversal of pulmonary edema. No significant changes in these param-
eters were observed in patients who failed to respond to therapy.
These observations implicate filtration of hypooncotic fluid from
the intravascular compartment during onset of cardiogenic
pulmonary edema and reabsorption of hypooncotic fluid into the in-
travascular compartment during reversal of pulmonary edema.
were 52 men and 43 women ranging from 44 to 99 years
(median 70) in age. In each instance, the patient presented
with a past history of heart disease (86 patients) or with un-
equivocal clinical and electrocardiographic evidence of acute
myocardial infarction (9 patients). Primary causes of heart
disease in the patients are summarized in table 1. In each in-
stance respiratory distress of sudden onset, orthopnea, and
bilateral moist rales were documented. Portable
anteroposterior semi-upright chest X-rays at a tube-to-chest
distance of 40 inches were obtained. Radiographic criteria of
interstitial. and/or alveolar pulmonary edema with or
without pleural effusion which conformed to grade 3 or 4
PE, according to the criteria of Turner, Lau, and Jacobson,9
were fulfilled. Patients in whom respiratory distress was
other than of acute onset within a period of six hours prior to
study or who presented with clinical signs of shock were ex-
cluded from study.
Fifty patients, including 24 men and 26 women, ranging in
age from 22 to 86 years (median 62), who were admitted for
coronary observation during the same interval because of
chest pain, served as one control group. In each instance
clinical, electrocardiographic, and routine enzyme
measurements excluded the diagnosis of acute myocardial
infarction. None of the patients had respiratory distress,
pulmonary rales or radiographic criteria of PE. All patients
survived and were discharged. These patients were
designated as control group 1.
An additional group of 21 patients observed during the
same interval of study, including 16 men and 5 women, rang-
ing in age from 37 to 86 years (mean 63), who had sustained
acute myocardial infarction, were designated as control
group 2.1 Diagnosis was based on Q wave and associated ST
and T wave abnormalities consistent with acute myocardial
infarction. Characteristic increases in enzymes including
creatine phosphokinase (CPK), lactic dehydrogenase
(LDH), and serum glutamic oxaloacetic transaminase
(SGOT) were documented. None of the patients had clini-
cal or radiographic signs of heart failure or of PE. Two of
the patients in group 2 died within an interval of two and 14
days after admission.
Methods of Study
Vital signs, fluid intake, and urine output were measured
at hourly intervals. Portable chest X-ray was obtained im-
195
 196 CI RCULATION VOL 55, No 1, JANUARY 1977

TAkBLE 1. Patient Data treatment included intravenous injection of digoxin in 31 of

Arteriosclerotic Heart Disease 64 the patients in amounts ranging from 0.25 to 1.0 mg. In 76
Actute myocardial infarctioin 9 of the 95 patients a second series of measurements was ob-
Pr ior myocardial infarctionl 34 tained within 36 (mean 15.7) hours following start of drug
Other 21 treatment, when clinical improvement was regarded as max-
Rlheumatic Heart Disease 9 imal. Patients who were mechanically ventilated or who sub-
Aortic stenosis 4
Mitral insufficiency :3 sequently received infusions of blood or colloid were ex-
Mitral stenosis 1 cluded from further study.
Aortic insufficieiicv 1 Differences were statistically analyzed by the Student's
Hypertensive Cardiovaseular 1)isease 20 t-test for paired and unpaired observations.
Myocardiopathy 2
Alcoholic 1 Results
Idiopathic 1
Tachypnea, relative hypoxemia during oxygen breathing,
hypercapnia, and acidemia were observed during acute PE.
mediately following admission. Duplicate measurements of In confirmation of previous reports, hypercapnia was fre-
blood pH (pHa) oxygen tension (PaO2), carbon dioxide ten- quently observed even though the patients had no evidence
sion (PaCO2), oxygen saturation (SaO2), hematocrit, total of chronic lung disease.'2 13 In 74 of 95 patients (78%),
plasma protein, plasma colloid osmotic pressure, plasma os- arterial blood lactate was increased to levels exceeding 1.5
molality, plasma sodium, plasma potassium and arterial mM/L, an indication of perfusion failure. Although oxygen
blood lactate (lactatea) were obtained on a single sample of 6 was administered, the arterial oxygen tension and satura-
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ml of heparinized arterial blood. tion were reduced during PE. Differences between patients
Blood gases were measured by standard electrode tech- with PE and the two control groups were highly significant
nique utilizing a Radiometer Model pH M27 System. Oxy- for each of the parameters reflecting respiratory gas ex-
gen saturation was measured with an Instrumentation change (table 2). There were no statistically significant
Laboratory Cooximeter Model 182. Hematocrit was differences between the two control groups.
measured by microhematocrit technique. Total protein was Plasma osmolality was significantly higher in patients
measured by refractometry (American Optical Refrac- with acute PE. In the absence of significant differences in
tometer TS meter Model 10400). Plasma colloid osmotic plasma sodium concentrations, the increase in osmolality
pressure was measured with a transducer-membrane system reflects increases in glucose, urea, and/or acid metabolites.
by methods previously described.'0 Plasma osmolality was Increase in resting heart rate but no significant difference in
measured by freezing point depression utilizing an Advanced arterial pressure was observed during PE.
Digimatic Osmometer Model 3D. Plasma sodium and The findings of specific relevance to the present study were
potassium were measured with an IL Flame Photometer simultaneous increases in plasma COP, plasma total protein
Model 143. Arterial blood lactate was measured by an en- concentration, and hematocrit in patients with PE (table 3).
zymatic technique.'1 Increases in COP were correlated with increases in total pro-
Except for administration of oxygen, baseline measure- tein (r = 0.533). There were no significant differences
ments were completed prior to drug therapy. Treatment was between male and female patients (25.9 and 25.7, respec-
established by protocol and included administration of oxy- tively) in mean COP.
gen by face mask or nasal cannula, furosemide 20 to 160 mg Patients with more advanced ventilatory defects and
(mean 80) by intravenous injection and one or more doses of specifically patients in whom PaCO2 exceeded 45 torr had
morphine sulfate in amounts ranging from 5 to 15 (mean 8) higher levels of total protein and COP than patients in
mg by intramuscular or intravenous injection. Subsequent whom PaCO2 was less than 35 torr (P < 0.05). However, no
TABLE 2. Initial Mlleasurements
Acute PE Control 1 Control 2
(95 pts) (50 pts) (21 pts)
HR, beats/min 109 2.3 81 - 3.1** 81 - 3.3$
SBP, mm Hg 146 = 4.3 136 - 3.6 129 i 6.2
DBP, mm Hg 84 - 2.4 81 - 2.1 74 - 3.6
resp/miin 30 0.7 20 0.5* * 20 - 0.6$
FI02 0.39 = 0.001 0.24 i 0.001** 0.29 = 0.004$
PaO2, torr 79 = 4.0 3.8
102 - 112 = 14.4t
SaO2, %C 87 1.0 96f 0.3 96 0.7$
PaCO2, torr 47.9 - 1.7 38. 4= 0.8** 39.0 = 1.0$
pHa, units 7.26 - 0.01 7.42 i 0.007** 7.40 0.009$
HCO3(a), mEq/L 19.7 - 0.4 23.2 - 0.4** 24.0 - 0.7$
Lactatea, mM/L 3.3 0.2 1.0 - 0.07** 0.9 f 0.06T
Na, mEq/L 139 - 0.3 140 - 0.6 138 - 0.4
K, mEq/L 4.1 - 0.07 3.8 - 0.07* 3.9 - 0.07
Plasma osmolality, mOsm/L 302 1.3 291 .;}** 293 - 2.Ot
The values shown are mean =t standard error of mean.
*P <0.01 (PE vs C1: **P <0.001 (PE vs Cl).
tP <0.005 (PE vs C1); IP <0.001 (PE vs C2).
Abbreviations: PE = pulmonary edema; HR = heart rate; S and DBP systolic and diastolic blood pressure; resp = respirations;
F102 = inspired oxygen fraction; PaO2 = arterial oxygen tension; SaO2 = arterial oxygen saturation; PaCO2 = arterial carbon
dioxide tension; pHa = arterial pH; HC03a = arterial bicarbonate.
 ONCOTIC PRESSURE DURING ACUTE PULMONARY EDEMA/Figueras, Weil 197

T-BLM, 3. Specific Mleasuremtents of Oncotic Pressure

Acute PE Control 1 PE vs Cl Control 2
(95 pts) (50 pts) P value (21 pts) PE vs C2 Cl vs C2
COP, torr 25.6 - 0.4 23.5 - 0.4 <0.001 23.3 - 0.5 <0.01 NS
TP, g(/o 7.8 0.1 7.1 - 0.1 <0.0(1 7.2 - 0.1 <0.001 NS
HCt., O/o 44.3 - 0.7 41.7 - 0.8 <0.02 42.9 - 1.0 NS NS
The values shown are mean +4 SEM.
Abbreviations: COP = colloid osmotic pressure; TP = total protein; Hct = hematocrit.

significant correlation was found between the initial COP
and PaCO2, pHa, plasma osmolality, plasma sodium and
potassium, lactate, or arterial systolic and diastolic
pressures.
Effects of treatment of pulmonary edema were evaluated
on the basis of clinical signs including reversal of
diaphoresis, warming of the skin, diminution of pulmonary
rales and disappearance of orthopiiea. In 65 patients in
whom clinical signs of pulmonary edema were reversed,
there was negative fluid balance averaging 1412 ml.
Respiratory rate, blood gases, plasma osmolality and blood
lactate were restored to normal within an average of 15.5
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pulmonary edema when the capillary hydrostatic pressure is
increased to the levels commonly observed in patients with
pulmonary edema. 1 5, 15, 16, 18,19 The fluid which escapes
from the intravascular compartment by filtration is hypoon-
cotic with respect to plasma. COP or protein concentration
measured on tracheobronchial fluid in cases of cardiogenic
PE ranged from 32% to 61% of that simultaneously observed
in plasma.2 Micropipette punctures of the pulmonary in-
terstitium after cardiogenic pulmonary edema or hemodilu-
tion in experimental animals also indicate that the edema
fluid has approximately one-half of the protein content of

hours (table 4). A significant decline in heart rate and
diastolic blood pressure were also observed. Colloid osmotic
pressure, TP, and Hct decreased to levels comparable to the
control group (table 5). A representative case in which
changes in COP, TP, and Hct during and after reversal of
PE are demonstrated is shown in figure 1.
To the contrary, no significant change in these parameters
was observed in 11 patients who failed to improve. Contin-
ued lactacidemia indicated continued circulatory failure.
Of the 76 patients in whom the effects of treatment were
objectively evaluated, the changes in COP were weakly cor-
related with simultaneous changes in plasma protein
(r = 0.67) and hematocrit (r = 0.55).
Discussion
An increase in left ventricular filling pressure, and conse-
quently, a corresponding increase in pulmonary capillary
hydrostatic pressure constitute objective criteria of left ven-
plasma.20
Since the transudate into the lung appears to be hypoon-
cotic with respect to plasma, fluid loss from the intravascu-
lar compartment into the lung is accompanied by increases
in protein concentration, COP, and red cell fraction. These
were the changes observed in our patients. The findings are
consistent with experimental data bearing on this issue.
When PE was induced in dogs by balloon obstruction of the
left atrium, Weiser and Grande7 also observed hemoconcen-
tration. Progressive increases in pulmonary extravascular
water were associated with simultaneous increases in
hematocrit and plasma protein concentration.
In patients with cardiogenic pulmonary edema, increases
in hematocrit and plasma proteins have also been
documented, especially following acute myocardial infarc-
tion.8 The coincidence of hypovolemia and pulmonary
edema with increases in plasma proteins and hematocrit was
interpreted by these authors as an indication of plasma
water lOSS.21, 22

tricular failure. Providing that the integrity of the capillary
membrane is not compromised, the egress of fluids into the
pulmonary interstitium and subsequently into the alveoli is
attributed to an increase in hydrostatic pressure and the ex-
cessive fluid flux which results from it.14-17
Experimentally, integrity of the capillary membrane as a
semipermeable membrane is maintained in cardiogenic
In addition, systemic venous hypertension and increased
sympathetic stimulation by which capillary filtration
pressures are augmented may also account for egress of fluid
from systemic capillaries and therefore hemoconcentra-
tion.23-25 Loss of plasma water may also be accentuated by
hyperventilation,28' 27 or muscular exertion.28
In a complementary study reported from this unit, pul-

TABLE 4. Effects of Therapy

Improved (65 pts) Not improved (11 pts)
Post Post
Initial Treatment P Initial Treatment P
Hit, beats/mi1i 108 i 2.8 92 i 2.2 <0.001 109 - 6.2 104 - 8.2 NS
SBP, mmHg 146 - 5.6 140 ( 6.0 NS 133 - 8.6 131 - 7.7 <0.03
DBP, mIn Hg 84 i 3.0 73 ) 1.8 <0.01 88 , 3.4 78 - 6.0 NS
Resp/min 31 - 0.8 22 - 0.3 <0.001 29 - 1.3 27 - 1.8 NS
PaO2, torr 73.8 - 4.2 97.4 - 4.3 <0.001 89.4 - 19.9 73.4 - 8.7 NS
SaO2, % 87 - 1.2 96 - 0.2 <0.001 92 i 2.2 93 - 1.3 NS
PHa, units 7.26 - 0.02 7.44 - 0.009 <0.001 7.35 . 0.02 7.38 - 0.03 NS
PaCO2, torr 49.4 - 2.1 39.4 i 0.8 <0.001 38.9 - 2.3 36.2 - 2.0 NS
Lactate, mM/L 3.4 0.3 1.4 - 0.07 <0.001 2.2 0.4 2.3 0.4 NS
HCO3(a), mEq/L 20.2 - 0.3 26.3 i 0.3 <0.001 21.1 - 0.7 21.7 - 1.3 NS
Plasma osmolality, mOsm/L 302 - 1.3 293 - 1.6 <0.002 293 4 3.4 299 - 3.2 NS
The values shown are mean t SEM.
For abbreviations see table 2.
 ._
198 CIRCULATION VOL 55, No 1, JANUARY 1977

TAtBLE 5. Effects of Therapy on Specific Mleasures of Oncotic Pressure

Improved (65 pts) Not improved (11 pts)
Post Post
Initial Treatment P Initial Treatment P
COP, torr 26.0 - 0.4 22.3 =f0.4 <0.001 24.8 - 1.2 24.5 a 1.3 NS
TP, g %C 7.8 - 0.1 7.0 - 0.1 <0.001 7.5 - 0.2 7.6 - 0.2 N5S
HTct, %C 44.5 - 0.8 41.3 - 0.8 <0.003 42.7 - 2.1 44.2 - 1.8 NS
Urine volume/ml 1412 - 170 924 - 236
The values shown are mean i SEM.
For abbreviations see table 3.

monary edema was often associated with a reduction in
plasma volume. Following diuresis induced by furosemide,
an increase rather than a decrease in plasma volume was
observed during reversal of PB3' Olesen32 had previously
observed that during diuresis with furosemide the edema
fluid that is cleared from the lungs is returned to the intra-
vascular compartment. This explains, at least in part, the
prompt decline in COP observed by us after treatment.
The immediate therapeutic effects of loop diuretics in-
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be maximal prior to therapy when capillary hydrostatic
pressure is maximal. To the contrary, COP declines during
therapy as these hydrostatic forces are decreased. Moreover,
the concomitant and comparable decrease in hematocrit
during reversal of pulmonary edema makes hemodilution a
more likely mechanism.
The results of the present study in patients with cardio-
genic pulmonary edema contrast with those previously re-
ported from this center on patients with pulmonary edema

clude a reduction of systemic venular and arteriolar tone.33
The resulting increase in vascular capacitance is also
observed after administration of morphine.34 The conse-
quent decrease in venous return accounts for a decrease in
left ventricular filling; with the increase in COP such a
lowering of hydrostatic pressure favors reabsorption of
plasma water. The observed decreases in heart rate and
diastolic pressure with increased plasma water following
effective treatment (table 4) would be consistent with a
reduction in sympathetic activity. This process is analogous
to the "capillary refill" that ensues after blood loss.35 In in-
stances in which therapy failed to reverse pulmonary edema
in patients herein reported, COP, total protein, and
hematocrit are unchanged or increased. The evidence
therefore implicates ingress of fluid of low protein content
during reversal of pulmonary edema.
The possibility that the reduction in TP and COP follow-
ing reversal of PE may be due to selective escape of albumin
from the intravascular compartment cannot be entirely ex-
cluded. However, such "capillary leaks" are more likely to
following protein dilution after infusion of large amounts of
crystalloid fluid.36 Pulmonary edema in the present series of
patients was primarily of hydrostatic cause due to left ven-
tricular failure. In such patients, COP was increased rather
than reduced.
The present report therefore provides additional insight
into the nature of the fluid shifts between the intravascular
and extravascular compartments during acute cardiogenic
pulmonary edema and following its reversal. The observa-
tion of hemoconcentration and increases in oncotic pressure
during onset of pulmonary edema is best explained by the
transudation of fluid which is low in protein content into the
lung. The hemodilution which is associated with reversal of
PE represents redilution of red cells and proteins after
hypooncotic edema fluid is reabsorbed from the interstitial
compartment.
Acknowledgment
We gratefully acknowledge the assistance of Mrs. Sybil Michaels, Chief
Laboratory Technologist, and Mr. Lawrence Portigal, Statistician. We are

4040 FUROSEMIDE, mg, I.V.

30 - FUROSEMIDE,mg, I.V.
25 - COLLOID OSMOTIC PRESS, torr 80 - 4-0S
P02 a, torr
15 - 60 - %ha
EST.PROTEIN, gmoi. F102 . 40
5- q _ART.SAT. *f
70 V
14 7.41
122 7.0 2 _
PHHQ, units
10
45-
501 0PC02 torr

40- HiEMATOCRIT, vol .

35-
2+ RALES 4 LACTATE ,mmol/I
4+ 3+ PULCONG. _we
r . 04
1600 2000 2400 0400 1600 2000 2400 0400
USC-SRUJ M.RW. - J.F
VA. "3 ACJTE PE. HOURS USC-8R
VA.ACUT
M.KW-J.F.
HOURS ASHD 10/5/73 HPMC 94208 E.
ASHD 04/73 HPMC 94208
FIGURE 1. Reversal of hypoxemia, respiratory acidosis, and lactacidemia was accompanied by reduction in COP, es-
timated protein, hemoglobin, and hematocrit in a 63-year-old man following treatment of acute pulmonary edema
associated with arteriosclerotic heart disease. Initial measurements were obtained immediately after admission to the
Emergency Room.
 ONCOTIC PRESSURE DURING ACUTE PULMONARY EDEMA/Figueras, Weil
also grateful to the medical and nursing staffs of the University of Southern
California Center for the Critically Ill for their referral and collaboration in
the care of these patients.
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 Increases in plasma oncotic pressure during acute cardiogenic pulmonary edema.
J Figueras and M H Weil

Circulation. 1977;55:195-199
doi: 10.1161/01.CIR.55.1.195
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